Bhalerao, Rishikesh P - Molecular control of growth adaptation in plants

@article{pandey_regulatory_2024,
	title = {A regulatory module mediating temperature control of cell-cell communication facilitates tree bud dormancy release},
	issn = {0261-4189},
	url = {https://www.embopress.org/doi/full/10.1038/s44318-024-00256-5},
	doi = {10.1038/s44318-024-00256-5},
	abstract = {The control of cell–cell communication via plasmodesmata (PD) plays a key role in plant development. In tree buds, low-temperature conditions (LT) induce a switch in plasmodesmata from a closed to an open state, which restores cell-to-cell communication in the shoot apex and releases dormancy. Using genetic and cell-biological approaches, we have identified a previously uncharacterized transcription factor, Low-temperature-Induced MADS-box 1 (LIM1), as an LT-induced, direct upstream activator of the gibberellic acid (GA) pathway. The LIM1-GA module mediates low temperature-induced plasmodesmata opening, by negatively regulating callose accumulation to promote dormancy release. LIM1 also activates expression of FT1 (FLOWERING LOCUS T), another LT-induced factor, with LIM1-FT1 forming a coherent feedforward loop converging on low-temperature regulation of gibberellin signaling in dormancy release. Mathematical modeling and experimental validation suggest that negative feedback regulation of LIM1 by gibberellin could play a crucial role in maintaining the robust temporal regulation of bud responses to low temperature. These results reveal genetic factors linking temperature control of cell–cell communication with regulation of seasonally-aligned growth crucial for adaptation of trees.},
	urldate = {2024-10-03},
	journal = {The EMBO Journal},
	author = {Pandey, Shashank K and Maurya, Jay Prakash and Aryal, Bibek and Drynda, Kamil and Nair, Aswin and Miskolczi, Pal and Singh, Rajesh Kumar and Wang, Xiaobin and Ma, Yujiao and de Souza Moraes, Tatiana and Bayer, Emmanuelle M and Farcot, Etienne and Bassel, George W and Band, Leah R and Bhalerao, Rishikesh P},
	month = oct,
	year = {2024},
	note = {Num Pages: 20
Publisher: John Wiley \& Sons, Ltd},
	keywords = {Callose, Dormancy, Gibberellins, Plasmodesmata, Temperature},
	pages = {1--20},
}

The control of cell–cell communication via plasmodesmata (PD) plays a key role in plant development. In tree buds, low-temperature conditions (LT) induce a switch in plasmodesmata from a closed to an open state, which restores cell-to-cell communication in the shoot apex and releases dormancy. Using genetic and cell-biological approaches, we have identified a previously uncharacterized transcription factor, Low-temperature-Induced MADS-box 1 (LIM1), as an LT-induced, direct upstream activator of the gibberellic acid (GA) pathway. The LIM1-GA module mediates low temperature-induced plasmodesmata opening, by negatively regulating callose accumulation to promote dormancy release. LIM1 also activates expression of FT1 (FLOWERING LOCUS T), another LT-induced factor, with LIM1-FT1 forming a coherent feedforward loop converging on low-temperature regulation of gibberellin signaling in dormancy release. Mathematical modeling and experimental validation suggest that negative feedback regulation of LIM1 by gibberellin could play a crucial role in maintaining the robust temporal regulation of bud responses to low temperature. These results reveal genetic factors linking temperature control of cell–cell communication with regulation of seasonally-aligned growth crucial for adaptation of trees.

@article{yang_genomic_2024,
	title = {Genomic basis of the distinct biosynthesis of β-glucogallin, a biochemical marker for hydrolyzable tannin production, in three oak species},
	volume = {242},
	copyright = {© 2024 The Authors New Phytologist © 2024 New Phytologist Foundation},
	issn = {1469-8137},
	url = {https://onlinelibrary.wiley.com/doi/abs/10.1111/nph.19711},
	doi = {10.1111/nph.19711},
	abstract = {Hydrolyzable tannins (HTs), predominant polyphenols in oaks, are widely used in grape wine aging, feed additives, and human healthcare. However, the limited availability of a high-quality reference genome of oaks greatly hampered the recognition of the mechanism of HT biosynthesis. Here, high-quality reference genomes of three Asian oak species (Quercus variabilis, Quercus aliena, and Quercus dentata) that have different HT contents were generated. Multi-omics studies were carried out to identify key genes regulating HT biosynthesis. In vitro enzyme activity assay was also conducted. Dual-luciferase and yeast one-hybrid assays were used to reveal the transcriptional regulation. Our results revealed that β-glucogallin was a biochemical marker for HT production in the cupules of the three Asian oaks. UGT84A13 was confirmed as the key enzyme for β-glucogallin biosynthesis. The differential expression of UGT84A13, rather than enzyme activity, was the main reason for different β-glucogallin and HT accumulation. Notably, sequence variations in UGT84A13 promoters led to different trans-activating activities of WRKY32/59, explaining the different expression patterns of UGT84A13 among the three species. Our findings provide three high-quality new reference genomes for oak trees and give new insights into different transcriptional regulation for understanding β-glucogallin and HT biosynthesis in closely related oak species.},
	language = {en},
	number = {6},
	urldate = {2024-05-24},
	journal = {New Phytologist},
	author = {Yang, Qinsong and Li, Jinjin and Wang, Yan and Wang, Zefu and Pei, Ziqi and Street, Nathaniel R. and Bhalerao, Rishikesh P. and Yu, Zhaowei and Gao, Yuhao and Ni, Junbei and Jiao, Yang and Sun, Minghui and Yang, Xiong and Chen, Yixin and Liu, Puyuan and Wang, Jiaxi and Liu, Yong and Li, Guolei},
	year = {2024},
	note = {\_eprint: https://onlinelibrary.wiley.com/doi/pdf/10.1111/nph.19711},
	keywords = {UGT84A13, hydrolyzable tannin, oak, whole-genome sequencing, β-glucogallin},
	pages = {2702--2718},
}

Hydrolyzable tannins (HTs), predominant polyphenols in oaks, are widely used in grape wine aging, feed additives, and human healthcare. However, the limited availability of a high-quality reference genome of oaks greatly hampered the recognition of the mechanism of HT biosynthesis. Here, high-quality reference genomes of three Asian oak species (Quercus variabilis, Quercus aliena, and Quercus dentata) that have different HT contents were generated. Multi-omics studies were carried out to identify key genes regulating HT biosynthesis. In vitro enzyme activity assay was also conducted. Dual-luciferase and yeast one-hybrid assays were used to reveal the transcriptional regulation. Our results revealed that β-glucogallin was a biochemical marker for HT production in the cupules of the three Asian oaks. UGT84A13 was confirmed as the key enzyme for β-glucogallin biosynthesis. The differential expression of UGT84A13, rather than enzyme activity, was the main reason for different β-glucogallin and HT accumulation. Notably, sequence variations in UGT84A13 promoters led to different trans-activating activities of WRKY32/59, explaining the different expression patterns of UGT84A13 among the three species. Our findings provide three high-quality new reference genomes for oak trees and give new insights into different transcriptional regulation for understanding β-glucogallin and HT biosynthesis in closely related oak species.

@article{ding_molecular_2024,
	title = {Molecular advances in bud dormancy in trees},
	volume = {75},
	issn = {0022-0957},
	url = {https://doi.org/10.1093/jxb/erae183},
	doi = {10.1093/jxb/erae183},
	abstract = {Seasonal bud dormancy in perennial woody plants is a crucial and intricate process that is vital for the survival and development of plants. Over the past few decades, significant advancements have been made in understanding many features of bud dormancy, particularly in model species, where certain molecular mechanisms underlying this process have been elucidated. We provide an overview of recent molecular progress in understanding bud dormancy in trees, with a specific emphasis on the integration of common signaling and molecular mechanisms identified across different tree species. Additionally, we address some challenges that have emerged from our current understanding of bud dormancy and offer insights for future studies.},
	number = {19},
	urldate = {2024-10-18},
	journal = {Journal of Experimental Botany},
	author = {Ding, Jihua and Wang, Kejing and Pandey, Shashank and Perales, Mariano and Allona, Isabel and Khan, Md Rezaul Islam and Busov, Victor B and Bhalerao, Rishikesh P},
	month = oct,
	year = {2024},
	pages = {6063--6075},
}

Seasonal bud dormancy in perennial woody plants is a crucial and intricate process that is vital for the survival and development of plants. Over the past few decades, significant advancements have been made in understanding many features of bud dormancy, particularly in model species, where certain molecular mechanisms underlying this process have been elucidated. We provide an overview of recent molecular progress in understanding bud dormancy in trees, with a specific emphasis on the integration of common signaling and molecular mechanisms identified across different tree species. Additionally, we address some challenges that have emerged from our current understanding of bud dormancy and offer insights for future studies.

@article{lathe_nks1elmo4_2024,
	title = {{NKS1}/{ELMO4} is an integral protein of a pectin synthesis protein complex and maintains {Golgi} morphology and cell adhesion in {Arabidopsis}},
	volume = {121},
	url = {https://www.pnas.org/doi/10.1073/pnas.2321759121},
	doi = {10.1073/pnas.2321759121},
	abstract = {Adjacent plant cells are connected by specialized cell wall regions, called middle lamellae, which influence critical agricultural characteristics, including fruit ripening and organ abscission. Middle lamellae are enriched in pectin polysaccharides, specifically homogalacturonan (HG). Here, we identify a plant-specific Arabidopsis DUF1068 protein, called NKS1/ELMO4, that is required for middle lamellae integrity and cell adhesion. NKS1 localizes to the Golgi apparatus and loss of NKS1 results in changes to Golgi structure and function. The nks1 mutants also display HG deficient phenotypes, including reduced seedling growth, changes to cell wall composition, and tissue integrity defects. These phenotypes are comparable to qua1 and qua2 mutants, which are defective in HG biosynthesis. Notably, genetic interactions indicate that NKS1 and the QUAs work in a common pathway. Protein interaction analyses and modeling corroborate that they work together in a stable protein complex with other pectin-related proteins. We propose that NKS1 is an integral part of a large pectin synthesis protein complex and that proper function of this complex is important to support Golgi structure and function.},
	number = {15},
	urldate = {2024-04-12},
	journal = {Proceedings of the National Academy of Sciences},
	author = {Lathe, Rahul S. and McFarlane, Heather E. and Kesten, Christopher and Wang, Liu and Khan, Ghazanfar Abbas and Ebert, Berit and Ramírez-Rodríguez, Eduardo Antonio and Zheng, Shuai and Noord, Niels and Frandsen, Kristian and Bhalerao, Rishikesh P. and Persson, Staffan},
	month = apr,
	year = {2024},
	note = {Publisher: Proceedings of the National Academy of Sciences},
	pages = {e2321759121},
}

Adjacent plant cells are connected by specialized cell wall regions, called middle lamellae, which influence critical agricultural characteristics, including fruit ripening and organ abscission. Middle lamellae are enriched in pectin polysaccharides, specifically homogalacturonan (HG). Here, we identify a plant-specific Arabidopsis DUF1068 protein, called NKS1/ELMO4, that is required for middle lamellae integrity and cell adhesion. NKS1 localizes to the Golgi apparatus and loss of NKS1 results in changes to Golgi structure and function. The nks1 mutants also display HG deficient phenotypes, including reduced seedling growth, changes to cell wall composition, and tissue integrity defects. These phenotypes are comparable to qua1 and qua2 mutants, which are defective in HG biosynthesis. Notably, genetic interactions indicate that NKS1 and the QUAs work in a common pathway. Protein interaction analyses and modeling corroborate that they work together in a stable protein complex with other pectin-related proteins. We propose that NKS1 is an integral part of a large pectin synthesis protein complex and that proper function of this complex is important to support Golgi structure and function.

@article{baral_typhon_2024,
	title = {{TYPHON} proteins are {RAB}-dependent mediators of the trans-{Golgi} network secretory pathway},
	issn = {1040-4651},
	url = {https://doi.org/10.1093/plcell/koae280},
	doi = {10.1093/plcell/koae280},
	abstract = {The trans-Golgi network (TGN), a key compartment in endomembrane trafficking, participates in both secretion to and endocytosis from the plasma membrane. Consequently, the TGN plays a key role in plant growth and development. Understanding how proteins are sorted for secretion or endocytic recycling at the TGN is critical for elucidating mechanisms of plant development. We previously showed that the protein ECHIDNA is essential for phytohormonal control of hypocotyl bending because it mediates secretion of cell wall components and the auxin influx carrier AUXIN RESISTANT 1 (AUX1) from the TGN. Despite the critical role of ECHIDNA in TGN-mediated trafficking, its mode of action remains unknown in Arabidopsis (Arabidopsis thaliana). We therefore performed a suppressor screen on the ech mutant. Here, we report the identification of TGN-localized TYPHON 1 (TPN1) and TPN2 proteins. A single amino acid change in either TPN protein causes dominant suppression of the ech mutant’s defects in growth and AUX1 secretion, while also restoring wild-type-like ethylene-responsive hypocotyl bending. Importantly, genetic and cell biological evidence shows that TPN1 acts through RAS-ASSOCIATED BINDING H1b (RABH1b), a TGN localized RAB-GTPase. These results provide insights into ECHIDNA-mediated secretory trafficking of cell wall and auxin carriers at the TGN, as well as its role in controlling plant growth.},
	urldate = {2024-10-16},
	journal = {The Plant Cell},
	author = {Baral, Anirban and Gendre, Delphine and Aryal, Bibek and Fougère, Louise and Di Fino, Luciano Martin and Ohori, Chihiro and Sztojka, Bernadette and Uemura, Tomohiro and Ueda, Takashi and Marhavý, Peter and Boutté, Yohann and Bhalerao, Rishikesh P},
	month = oct,
	year = {2024},
	pages = {koae280},
}

The trans-Golgi network (TGN), a key compartment in endomembrane trafficking, participates in both secretion to and endocytosis from the plasma membrane. Consequently, the TGN plays a key role in plant growth and development. Understanding how proteins are sorted for secretion or endocytic recycling at the TGN is critical for elucidating mechanisms of plant development. We previously showed that the protein ECHIDNA is essential for phytohormonal control of hypocotyl bending because it mediates secretion of cell wall components and the auxin influx carrier AUXIN RESISTANT 1 (AUX1) from the TGN. Despite the critical role of ECHIDNA in TGN-mediated trafficking, its mode of action remains unknown in Arabidopsis (Arabidopsis thaliana). We therefore performed a suppressor screen on the ech mutant. Here, we report the identification of TGN-localized TYPHON 1 (TPN1) and TPN2 proteins. A single amino acid change in either TPN protein causes dominant suppression of the ech mutant’s defects in growth and AUX1 secretion, while also restoring wild-type-like ethylene-responsive hypocotyl bending. Importantly, genetic and cell biological evidence shows that TPN1 acts through RAS-ASSOCIATED BINDING H1b (RABH1b), a TGN localized RAB-GTPase. These results provide insights into ECHIDNA-mediated secretory trafficking of cell wall and auxin carriers at the TGN, as well as its role in controlling plant growth.

@article{davis_toward_2024,
	title = {Toward uncovering an operating system in plant organs},
	volume = {29},
	issn = {1360-1385},
	url = {https://www.sciencedirect.com/science/article/pii/S1360138523003655},
	doi = {10.1016/j.tplants.2023.11.006},
	abstract = {Molecular motifs can explain information processing within single cells, while how assemblies of cells collectively achieve this remains less well understood. Plant fitness and survival depend upon robust and accurate decision-making in their decentralised multicellular organ systems. Mobile agents, including hormones, metabolites, and RNAs, have a central role in coordinating multicellular collective decision-making, yet mechanisms describing how cell–cell communication scales to organ-level transitions is poorly understood. Here, we explore how unified outputs may emerge in plant organs by distributed information processing across different scales and using different modalities. Mathematical and computational representations of these events are also explored toward understanding how these events take place and are leveraged to manipulate plant development in response to the environment.},
	number = {7},
	urldate = {2024-07-17},
	journal = {Trends in Plant Science},
	author = {Davis, Gwendolyn V. and de Souza Moraes, Tatiana and Khanapurkar, Swanand and Dromiack, Hannah and Ahmad, Zaki and Bayer, Emmanuelle M. and Bhalerao, Rishikesh P. and Walker, Sara I. and Bassel, George W.},
	month = jul,
	year = {2024},
	keywords = {Cellular Automata, collective behaviour, decentralised information processing, decision-making, plant development},
	pages = {742--753},
}

Molecular motifs can explain information processing within single cells, while how assemblies of cells collectively achieve this remains less well understood. Plant fitness and survival depend upon robust and accurate decision-making in their decentralised multicellular organ systems. Mobile agents, including hormones, metabolites, and RNAs, have a central role in coordinating multicellular collective decision-making, yet mechanisms describing how cell–cell communication scales to organ-level transitions is poorly understood. Here, we explore how unified outputs may emerge in plant organs by distributed information processing across different scales and using different modalities. Mathematical and computational representations of these events are also explored toward understanding how these events take place and are leveraged to manipulate plant development in response to the environment.

@article{bourdon_ectopic_2023,
	title = {Ectopic callose deposition into woody biomass modulates the nano-architecture of macrofibrils},
	volume = {9},
	copyright = {2023 The Author(s)},
	issn = {2055-0278},
	url = {https://www.nature.com/articles/s41477-023-01459-0},
	doi = {10.1038/s41477-023-01459-0},
	abstract = {Plant biomass plays an increasingly important role in the circular bioeconomy, replacing non-renewable fossil resources. Genetic engineering of this lignocellulosic biomass could benefit biorefinery transformation chains by lowering economic and technological barriers to industrial processing. However, previous efforts have mostly targeted the major constituents of woody biomass: cellulose, hemicellulose and lignin. Here we report the engineering of wood structure through the introduction of callose, a polysaccharide novel to most secondary cell walls. Our multiscale analysis of genetically engineered poplar trees shows that callose deposition modulates cell wall porosity, water and lignin contents and increases the lignin–cellulose distance, ultimately resulting in substantially decreased biomass recalcitrance. We provide a model of the wood cell wall nano-architecture engineered to accommodate the hydrated callose inclusions. Ectopic polymer introduction into biomass manifests in new physico-chemical properties and offers new avenues when considering lignocellulose engineering.},
	language = {en},
	number = {9},
	urldate = {2023-09-22},
	journal = {Nature Plants},
	author = {Bourdon, Matthieu and Lyczakowski, Jan J. and Cresswell, Rosalie and Amsbury, Sam and Vilaplana, Francisco and Le Guen, Marie-Joo and Follain, Nadège and Wightman, Raymond and Su, Chang and Alatorre-Cobos, Fulgencio and Ritter, Maximilian and Liszka, Aleksandra and Terrett, Oliver M. and Yadav, Shri Ram and Vatén, Anne and Nieminen, Kaisa and Eswaran, Gugan and Alonso-Serra, Juan and Müller, Karin H. and Iuga, Dinu and Miskolczi, Pal Csaba and Kalmbach, Lothar and Otero, Sofia and Mähönen, Ari Pekka and Bhalerao, Rishikesh and Bulone, Vincent and Mansfield, Shawn D. and Hill, Stefan and Burgert, Ingo and Beaugrand, Johnny and Benitez-Alfonso, Yoselin and Dupree, Ray and Dupree, Paul and Helariutta, Ykä},
	month = sep,
	year = {2023},
	note = {Number: 9
Publisher: Nature Publishing Group},
	keywords = {Biofuels, Molecular engineering in plants},
	pages = {1530--1546},
}

Plant biomass plays an increasingly important role in the circular bioeconomy, replacing non-renewable fossil resources. Genetic engineering of this lignocellulosic biomass could benefit biorefinery transformation chains by lowering economic and technological barriers to industrial processing. However, previous efforts have mostly targeted the major constituents of woody biomass: cellulose, hemicellulose and lignin. Here we report the engineering of wood structure through the introduction of callose, a polysaccharide novel to most secondary cell walls. Our multiscale analysis of genetically engineered poplar trees shows that callose deposition modulates cell wall porosity, water and lignin contents and increases the lignin–cellulose distance, ultimately resulting in substantially decreased biomass recalcitrance. We provide a model of the wood cell wall nano-architecture engineered to accommodate the hydrated callose inclusions. Ectopic polymer introduction into biomass manifests in new physico-chemical properties and offers new avenues when considering lignocellulose engineering.

@article{topcu_growths_2023,
	title = {Growth’s secret maestros: {LBD11}–{ROS} harmony drives vascular cambium activity in {Arabidopsis}},
	volume = {16},
	issn = {1674-2052},
	shorttitle = {Growth’s secret maestros},
	url = {https://www.cell.com/molecular-plant/abstract/S1674-2052(23)00214-9},
	doi = {10.1016/j.molp.2023.07.012},
	abstract = {Integration of metabolic products such as reactive oxygen species (ROS) into vital
processes play essential roles in plants. ROS refers to oxygen-derived free radicals,
which exhibit a higher reactivity compared to the diatomic oxygen molecule (O2) (Waszczak
et al., 2018). Numerous forms of ROS have been identified in plants with various degrees
of stability: singlet oxygen (1O2), superoxide anion (O2·−), hydrogen peroxide (H2O2),
and hydroxyl radical (HO·) are the major forms. ROS are generated during normal plant
growth as products of aerobic metabolism in almost all cellular compartments, including
chloroplasts, mitochondria, and peroxisomes as well as in apoplast.},
	language = {English},
	number = {8},
	urldate = {2023-08-28},
	journal = {Molecular Plant},
	author = {Topcu, Melis Kucukoglu and Bhalerao, Rishikesh P.},
	month = aug,
	year = {2023},
	pmid = {37528579},
	note = {Publisher: Elsevier},
	pages = {1246--1248},
}

Integration of metabolic products such as reactive oxygen species (ROS) into vital processes play essential roles in plants. ROS refers to oxygen-derived free radicals, which exhibit a higher reactivity compared to the diatomic oxygen molecule (O2) (Waszczak et al., 2018). Numerous forms of ROS have been identified in plants with various degrees of stability: singlet oxygen (1O2), superoxide anion (O2·−), hydrogen peroxide (H2O2), and hydroxyl radical (HO·) are the major forms. ROS are generated during normal plant growth as products of aerobic metabolism in almost all cellular compartments, including chloroplasts, mitochondria, and peroxisomes as well as in apoplast.

@article{jonsson_multiple_2023,
	title = {Multiple mechanisms behind plant bending},
	volume = {9},
	copyright = {2022 Springer Nature Limited},
	issn = {2055-0278},
	url = {https://www.nature.com/articles/s41477-022-01310-y},
	doi = {10.1038/s41477-022-01310-y},
	abstract = {To survive, plants constantly adapt their body shape to their environment. This often involves remarkably rapid bending of their organs such as stems, leaves and roots. Since plant cells are enclosed by stiff cell walls, they use various strategies for bending their organs, which differ from bending mechanisms of soft animal tissues and involve larger physical forces. Here we attempt to summarize and link different viewpoints on bending mechanisms: genes and signalling, mathematical modelling and biomechanics. We argue that quantifying cell growth and physical forces could open a new level in our understanding of bending and resolve some of its paradoxes.},
	language = {en},
	number = {1},
	urldate = {2023-02-03},
	journal = {Nature Plants},
	author = {Jonsson, Kristoffer and Ma, Yuan and Routier-Kierzkowska, Anne-Lise and Bhalerao, Rishikesh P.},
	month = jan,
	year = {2023},
	keywords = {Plant morphogenesis, Tropism},
	pages = {13--21},
}

To survive, plants constantly adapt their body shape to their environment. This often involves remarkably rapid bending of their organs such as stems, leaves and roots. Since plant cells are enclosed by stiff cell walls, they use various strategies for bending their organs, which differ from bending mechanisms of soft animal tissues and involve larger physical forces. Here we attempt to summarize and link different viewpoints on bending mechanisms: genes and signalling, mathematical modelling and biomechanics. We argue that quantifying cell growth and physical forces could open a new level in our understanding of bending and resolve some of its paradoxes.

@article{liu_plant_2023,
	title = {The plant trans-{Golgi} network component {ECHIDNA} regulates defense, cell death, and endoplasmic reticulum stress},
	volume = {191},
	issn = {0032-0889},
	url = {https://doi.org/10.1093/plphys/kiac400},
	doi = {10.1093/plphys/kiac400},
	abstract = {The trans-Golgi network (TGN) acts as a central platform for sorting and secreting various cargoes to the cell surface, thus being essential for the full execution of plant immunity. However, the fine-tuned regulation of TGN components in plant defense and stress response has been not fully elucidated. Our study revealed that despite largely compromising penetration resistance, the loss-of-function mutation of the TGN component protein ECHIDNA (ECH) induced enhanced postinvasion resistance to powdery mildew in Arabidopsis thaliana. Genetic and transcriptome analyses and hormone profiling demonstrated that ECH loss resulted in salicylic acid (SA) hyperaccumulation via the ISOCHORISMATE SYNTHASE 1 biosynthesis pathway, thereby constitutively activating SA-dependent innate immunity that was largely responsible for the enhanced postinvasion resistance. Furthermore, the ech mutant displayed accelerated SA-independent spontaneous cell death and constitutive POWDERY MILDEW RESISTANCE 4-mediated callose depositions. In addition, ECH loss led to a chronically prolonged endoplasmic reticulum stress in the ech mutant. These results provide insights into understanding the role of TGN components in the regulation of plant immunity and stress responses.},
	number = {1},
	urldate = {2023-01-09},
	journal = {Plant Physiology},
	author = {Liu, Lijiang and Qin, Li and Safdar, Luqman Bin and Zhao, Chuanji and Cheng, Xiaohui and Xie, Meili and Zhang, Yi and Gao, Feng and Bai, Zetao and Huang, Junyan and Bhalerao, Rishikesh P and Liu, Shengyi and Wei, Yangdou},
	month = jan,
	year = {2023},
	pages = {558--574},
}

The trans-Golgi network (TGN) acts as a central platform for sorting and secreting various cargoes to the cell surface, thus being essential for the full execution of plant immunity. However, the fine-tuned regulation of TGN components in plant defense and stress response has been not fully elucidated. Our study revealed that despite largely compromising penetration resistance, the loss-of-function mutation of the TGN component protein ECHIDNA (ECH) induced enhanced postinvasion resistance to powdery mildew in Arabidopsis thaliana. Genetic and transcriptome analyses and hormone profiling demonstrated that ECH loss resulted in salicylic acid (SA) hyperaccumulation via the ISOCHORISMATE SYNTHASE 1 biosynthesis pathway, thereby constitutively activating SA-dependent innate immunity that was largely responsible for the enhanced postinvasion resistance. Furthermore, the ech mutant displayed accelerated SA-independent spontaneous cell death and constitutive POWDERY MILDEW RESISTANCE 4-mediated callose depositions. In addition, ECH loss led to a chronically prolonged endoplasmic reticulum stress in the ech mutant. These results provide insights into understanding the role of TGN components in the regulation of plant immunity and stress responses.

@article{ma_endoreplication_2022,
	title = {Endoreplication mediates cell size control via mechanochemical signaling from cell wall},
	volume = {8},
	url = {https://www.science.org/doi/10.1126/sciadv.abq2047},
	doi = {10.1126/sciadv.abq2047},
	abstract = {Endoreplication is an evolutionarily conserved mechanism for increasing nuclear DNA content (ploidy). Ploidy frequently scales with final cell and organ size, suggesting a key role for endoreplication in these processes. However, exceptions exist, and, consequently, the endoreplication-size nexus remains enigmatic. Here, we show that prolonged tissue folding at the apical hook in Arabidopsis requires endoreplication asymmetry under the control of an auxin gradient. We identify a molecular pathway linking endoreplication levels to cell size through cell wall remodeling and stiffness modulation. We find that endoreplication is not only permissive for growth: Endoreplication reduction enhances wall stiffening, actively reducing cell size. The cell wall integrity kinase THESEUS plays a key role in this feedback loop. Our data thus explain the nonlinearity between ploidy levels and size while also providing a molecular mechanism linking mechanochemical signaling with endoreplication-mediated dynamic control of cell growth.},
	number = {49},
	urldate = {2022-12-16},
	journal = {Science Advances},
	author = {Ma, Yuan and Jonsson, Kristoffer and Aryal, Bibek and De Veylder, Lieven and Hamant, Olivier and Bhalerao, Rishikesh P.},
	month = dec,
	year = {2022},
	pages = {eabq2047},
}

Endoreplication is an evolutionarily conserved mechanism for increasing nuclear DNA content (ploidy). Ploidy frequently scales with final cell and organ size, suggesting a key role for endoreplication in these processes. However, exceptions exist, and, consequently, the endoreplication-size nexus remains enigmatic. Here, we show that prolonged tissue folding at the apical hook in Arabidopsis requires endoreplication asymmetry under the control of an auxin gradient. We identify a molecular pathway linking endoreplication levels to cell size through cell wall remodeling and stiffness modulation. We find that endoreplication is not only permissive for growth: Endoreplication reduction enhances wall stiffening, actively reducing cell size. The cell wall integrity kinase THESEUS plays a key role in this feedback loop. Our data thus explain the nonlinearity between ploidy levels and size while also providing a molecular mechanism linking mechanochemical signaling with endoreplication-mediated dynamic control of cell growth.

@article{mehra_hydraulic_2022,
	title = {Hydraulic flux–responsive hormone redistribution determines root branching},
	volume = {378},
	url = {https://www.science.org/doi/10.1126/science.add3771},
	doi = {10.1126/science.add3771},
	abstract = {Plant roots exhibit plasticity in their branching patterns to forage efficiently for heterogeneously distributed resources, such as soil water. The xerobranching response represses lateral root formation when roots lose contact with water. Here, we show that xerobranching is regulated by radial movement of the phloem-derived hormone abscisic acid, which disrupts intercellular communication between inner and outer cell layers through plasmodesmata. Closure of these intercellular pores disrupts the inward movement of the hormone signal auxin, blocking lateral root branching. Once root tips regain contact with moisture, the abscisic acid response rapidly attenuates. Our study reveals how roots adapt their branching pattern to heterogeneous soil water conditions by linking changes in hydraulic flux with dynamic hormone redistribution.},
	number = {6621},
	urldate = {2022-11-24},
	journal = {Science},
	author = {Mehra, Poonam and Pandey, Bipin K. and Melebari, Dalia and Banda, Jason and Leftley, Nicola and Couvreur, Valentin and Rowe, James and Anfang, Moran and De Gernier, Hugues and Morris, Emily and Sturrock, Craig J. and Mooney, Sacha J. and Swarup, Ranjan and Faulkner, Christine and Beeckman, Tom and Bhalerao, Rishikesh P. and Shani, Eilon and Jones, Alexander M. and Dodd, Ian C. and Sharp, Robert E. and Sadanandom, Ari and Draye, Xavier and Bennett, Malcolm J.},
	month = nov,
	year = {2022},
	pages = {762--768},
}

Plant roots exhibit plasticity in their branching patterns to forage efficiently for heterogeneously distributed resources, such as soil water. The xerobranching response represses lateral root formation when roots lose contact with water. Here, we show that xerobranching is regulated by radial movement of the phloem-derived hormone abscisic acid, which disrupts intercellular communication between inner and outer cell layers through plasmodesmata. Closure of these intercellular pores disrupts the inward movement of the hormone signal auxin, blocking lateral root branching. Once root tips regain contact with moisture, the abscisic acid response rapidly attenuates. Our study reveals how roots adapt their branching pattern to heterogeneous soil water conditions by linking changes in hydraulic flux with dynamic hormone redistribution.

@article{miao_katanin-dependent_2022,
	title = {Katanin-{Dependent} {Microtubule} {Ordering} in {Association} with {ABA} {Is} {Important} for {Root} {Hydrotropism}},
	volume = {23},
	copyright = {http://creativecommons.org/licenses/by/3.0/},
	issn = {1422-0067},
	url = {https://www.mdpi.com/1422-0067/23/7/3846},
	doi = {10.3390/ijms23073846},
	abstract = {Root hydrotropism refers to root directional growth toward soil moisture. Cortical microtubule arrays are essential for determining the growth axis of the elongating cells in plants. However, the role of microtubule reorganization in root hydrotropism remains elusive. Here, we demonstrate that the well-ordered microtubule arrays and the microtubule-severing protein KATANIN (KTN) play important roles in regulating root hydrotropism in Arabidopsis. We found that the root hydrotropic bending of the ktn1 mutant was severely attenuated but not root gravitropism. After hydrostimulation, cortical microtubule arrays in cells of the elongation zone of wild-type (WT) Col-0 roots were reoriented from transverse into an oblique array along the axis of cell elongation, whereas the microtubule arrays in the ktn1 mutant remained in disorder. Moreover, we revealed that abscisic acid (ABA) signaling enhanced the root hydrotropism of WT and partially rescued the oryzalin (a microtubule destabilizer) alterative root hydrotropism of WT but not ktn1 mutants. These results suggest that katanin-dependent microtubule ordering is required for root hydrotropism, which might work downstream of ABA signaling pathways for plant roots to search for water.},
	language = {en},
	number = {7},
	urldate = {2022-04-19},
	journal = {International Journal of Molecular Sciences},
	author = {Miao, Rui and Siao, Wei and Zhang, Na and Lei, Zuliang and Lin, Deshu and Bhalerao, Rishikesh P. and Lu, Congming and Xu, Weifeng},
	month = jan,
	year = {2022},
	keywords = {KATANIN, abscisic acid, cortical microtubule arrays, oryzalin, root hydrotropism},
	pages = {3846},
}

Root hydrotropism refers to root directional growth toward soil moisture. Cortical microtubule arrays are essential for determining the growth axis of the elongating cells in plants. However, the role of microtubule reorganization in root hydrotropism remains elusive. Here, we demonstrate that the well-ordered microtubule arrays and the microtubule-severing protein KATANIN (KTN) play important roles in regulating root hydrotropism in Arabidopsis. We found that the root hydrotropic bending of the ktn1 mutant was severely attenuated but not root gravitropism. After hydrostimulation, cortical microtubule arrays in cells of the elongation zone of wild-type (WT) Col-0 roots were reoriented from transverse into an oblique array along the axis of cell elongation, whereas the microtubule arrays in the ktn1 mutant remained in disorder. Moreover, we revealed that abscisic acid (ABA) signaling enhanced the root hydrotropism of WT and partially rescued the oryzalin (a microtubule destabilizer) alterative root hydrotropism of WT but not ktn1 mutants. These results suggest that katanin-dependent microtubule ordering is required for root hydrotropism, which might work downstream of ABA signaling pathways for plant roots to search for water.

@article{jonsson_plant_2022,
	title = {Plant cell walls as mechanical signaling hubs for morphogenesis},
	volume = {32},
	issn = {0960-9822},
	url = {https://www.sciencedirect.com/science/article/pii/S0960982222002585},
	doi = {10.1016/j.cub.2022.02.036},
	abstract = {The instructive role of mechanical cues during morphogenesis is increasingly being recognized in all kingdoms. Patterns of mechanical stress depend on shape, growth and external factors. In plants, the cell wall integrates these three parameters to function as a hub for mechanical feedback. Plant cells are interconnected by cell walls that provide structural integrity and yet are flexible enough to act as both targets and transducers of mechanical cues. Such cues may act locally at the subcellular level or across entire tissues, requiring tight control of both cell-wall composition and cell–cell adhesion. Here we focus on how changes in cell-wall chemistry and mechanics act in communicating diverse cues to direct growth asymmetries required for plant morphogenesis. We explore the role of cellulose microfibrils, microtubule arrays and pectin methylesterification in the transduction of mechanical cues during morphogenesis. Plant hormones can affect the mechanochemical composition of the cell wall and, in turn, the cell wall can modulate hormone signaling pathways, as well as the tissue-level distribution of these hormones. This also leads us to revisit the position of biochemical growth factors, such as plant hormones, acting both upstream and downstream of mechanical signaling. Finally, while the structure of the cell wall is being elucidated with increasing precision, existing data clearly show that the integration of genetic, biochemical and theoretical studies will be essential for a better understanding of the role of the cell wall as a hub for the mechanical control of plant morphogenesis.},
	language = {en},
	number = {7},
	urldate = {2022-05-20},
	journal = {Current Biology},
	author = {Jonsson, Kristoffer and Hamant, Olivier and Bhalerao, Rishikesh P.},
	month = apr,
	year = {2022},
	pages = {R334--R340},
}

The instructive role of mechanical cues during morphogenesis is increasingly being recognized in all kingdoms. Patterns of mechanical stress depend on shape, growth and external factors. In plants, the cell wall integrates these three parameters to function as a hub for mechanical feedback. Plant cells are interconnected by cell walls that provide structural integrity and yet are flexible enough to act as both targets and transducers of mechanical cues. Such cues may act locally at the subcellular level or across entire tissues, requiring tight control of both cell-wall composition and cell–cell adhesion. Here we focus on how changes in cell-wall chemistry and mechanics act in communicating diverse cues to direct growth asymmetries required for plant morphogenesis. We explore the role of cellulose microfibrils, microtubule arrays and pectin methylesterification in the transduction of mechanical cues during morphogenesis. Plant hormones can affect the mechanochemical composition of the cell wall and, in turn, the cell wall can modulate hormone signaling pathways, as well as the tissue-level distribution of these hormones. This also leads us to revisit the position of biochemical growth factors, such as plant hormones, acting both upstream and downstream of mechanical signaling. Finally, while the structure of the cell wall is being elucidated with increasing precision, existing data clearly show that the integration of genetic, biochemical and theoretical studies will be essential for a better understanding of the role of the cell wall as a hub for the mechanical control of plant morphogenesis.

@article{hasegawa_tgnee_2022,
	title = {The {TGN}/{EE} {SNARE} protein {SYP61} and the ubiquitin ligase {ATL31} cooperatively regulate plant responses to carbon/nitrogen conditions in {Arabidopsis}},
	volume = {34},
	issn = {1040-4651},
	url = {https://doi.org/10.1093/plcell/koac014},
	doi = {10.1093/plcell/koac014},
	abstract = {Ubiquitination is a post-translational modification involving the reversible attachment of the small protein ubiquitin to a target protein. Ubiquitination is involved in numerous cellular processes, including the membrane trafficking of cargo proteins. However, the ubiquitination of the trafficking machinery components and their involvement in environmental responses are not well understood. Here, we report that the Arabidopsis thaliana trans-Golgi network/early endosome localized SNARE (soluble N-ethylmaleimide-sensitive factor attachment protein receptor) protein SYP61 interacts with the transmembrane ubiquitin ligase ATL31, a key regulator of resistance to disrupted carbon (C)/nitrogen/(N)-nutrient conditions. SYP61 is a key component of membrane trafficking in Arabidopsis. The subcellular localization of ATL31 was disrupted in knockdown mutants of SYP61, and the insensitivity of ATL31-overexpressing plants to high C/low N-stress was repressed in these mutants, suggesting that SYP61 and ATL31 cooperatively function in plant responses to nutrient stress. SYP61 is ubiquitinated in plants, and its ubiquitination level is upregulated under low C/high N-nutrient conditions. These findings provide important insights into the ubiquitin signaling and membrane trafficking machinery in plants.},
	number = {4},
	urldate = {2022-04-08},
	journal = {The Plant Cell},
	author = {Hasegawa, Yoko and Huarancca Reyes, Thais and Uemura, Tomohiro and Baral, Anirban and Fujimaki, Akari and Luo, Yongming and Morita, Yoshie and Saeki, Yasushi and Maekawa, Shugo and Yasuda, Shigetaka and Mukuta, Koki and Fukao, Yoichiro and Tanaka, Keiji and Nakano, Akihiko and Takagi, Junpei and Bhalerao, Rishikesh P and Yamaguchi, Junji and Sato, Takeo},
	month = apr,
	year = {2022},
	pages = {1354--1374},
}

Ubiquitination is a post-translational modification involving the reversible attachment of the small protein ubiquitin to a target protein. Ubiquitination is involved in numerous cellular processes, including the membrane trafficking of cargo proteins. However, the ubiquitination of the trafficking machinery components and their involvement in environmental responses are not well understood. Here, we report that the Arabidopsis thaliana trans-Golgi network/early endosome localized SNARE (soluble N-ethylmaleimide-sensitive factor attachment protein receptor) protein SYP61 interacts with the transmembrane ubiquitin ligase ATL31, a key regulator of resistance to disrupted carbon (C)/nitrogen/(N)-nutrient conditions. SYP61 is a key component of membrane trafficking in Arabidopsis. The subcellular localization of ATL31 was disrupted in knockdown mutants of SYP61, and the insensitivity of ATL31-overexpressing plants to high C/low N-stress was repressed in these mutants, suggesting that SYP61 and ATL31 cooperatively function in plant responses to nutrient stress. SYP61 is ubiquitinated in plants, and its ubiquitination level is upregulated under low C/high N-nutrient conditions. These findings provide important insights into the ubiquitin signaling and membrane trafficking machinery in plants.

@article{li_towards_2022,
	title = {Towards understanding the biological foundations of perenniality},
	volume = {27},
	issn = {1360-1385},
	url = {https://www.sciencedirect.com/science/article/pii/S1360138521002181},
	doi = {10.1016/j.tplants.2021.08.007},
	abstract = {Perennial life cycles enable plants to have remarkably long lifespans, as exemplified by trees that can live for thousands of years. For this, they require sophisticated regulatory networks that sense environmental changes and initiate adaptive responses in their growth patterns. Recent research has gradually elucidated fundamental mechanisms underlying the perennial life cycle. Intriguingly, several conserved components of the floral transition pathway in annuals such as Arabidopsis thaliana also participate in these regulatory mechanisms underpinning perenniality. Here, we provide an overview of perennials’ physiological features and summarise their recently discovered molecular foundations. We also highlight the importance of deepening our understanding of perenniality in the development of perennial grain crops, which are promising elements of future sustainable agriculture.},
	language = {en},
	number = {1},
	urldate = {2021-09-30},
	journal = {Trends in Plant Science},
	author = {Li, Zheng and Lathe, Rahul S. and Li, Jinping and He, Hong and Bhalerao, Rishikesh P.},
	month = jan,
	year = {2022},
	keywords = {perenniality, polycarpy, seasonal adaptation, sustainable agriculture},
	pages = {56--68},
}

Perennial life cycles enable plants to have remarkably long lifespans, as exemplified by trees that can live for thousands of years. For this, they require sophisticated regulatory networks that sense environmental changes and initiate adaptive responses in their growth patterns. Recent research has gradually elucidated fundamental mechanisms underlying the perennial life cycle. Intriguingly, several conserved components of the floral transition pathway in annuals such as Arabidopsis thaliana also participate in these regulatory mechanisms underpinning perenniality. Here, we provide an overview of perennials’ physiological features and summarise their recently discovered molecular foundations. We also highlight the importance of deepening our understanding of perenniality in the development of perennial grain crops, which are promising elements of future sustainable agriculture.

@article{singh_when_2022,
	title = {When to branch: seasonal control of shoot architecture in trees},
	volume = {289},
	issn = {1742-4658},
	shorttitle = {When to branch},
	url = {https://onlinelibrary.wiley.com/doi/abs/10.1111/febs.16227},
	doi = {10.1111/febs.16227},
	abstract = {Long-lived perennial plants optimize their shoot architecture by responding to seasonal cues. The main strategy used by plants of temperate and boreal regions with respect to surviving the extremely unfavourable conditions of winter comprises the protection of their apical and lateral meristematic tissues. This involves myriads of transcriptional, translational and metabolic changes in the plants because shoot architecture is controlled by multiple pathways that regulate processes such as bud formation and flowering, small RNAs, environmental factors (especially light quality, photoperiod and temperature), hormones, and sugars. Recent studies have begun to reveal how these pathways are recruited for the seasonal adaptation and regulation of shoot architecture in perennial plants, including the role of a regulatory module consisting of antagonistic players terminal flower 1 (TFL1) and like-ap1 (LAP1) in the hybrid aspen. Here, we review recent progress in our understanding of the genetic control of shoot architecture in perennials compared to in annuals.},
	language = {en},
	number = {24},
	urldate = {2022-12-30},
	journal = {The FEBS Journal},
	author = {Singh, Rajesh Kumar and Bhalerao, Rishikesh P. and Maurya, Jay P.},
	month = oct,
	year = {2022},
	keywords = {Axillary buds, Branching, Photoperiod, Seasonal growth, Shoot Architecture, axillary buds, branching, photoperiod, seasonal growth, shoot architecture, temperature},
	pages = {8062--8070},
}

Long-lived perennial plants optimize their shoot architecture by responding to seasonal cues. The main strategy used by plants of temperate and boreal regions with respect to surviving the extremely unfavourable conditions of winter comprises the protection of their apical and lateral meristematic tissues. This involves myriads of transcriptional, translational and metabolic changes in the plants because shoot architecture is controlled by multiple pathways that regulate processes such as bud formation and flowering, small RNAs, environmental factors (especially light quality, photoperiod and temperature), hormones, and sugars. Recent studies have begun to reveal how these pathways are recruited for the seasonal adaptation and regulation of shoot architecture in perennial plants, including the role of a regulatory module consisting of antagonistic players terminal flower 1 (TFL1) and like-ap1 (LAP1) in the hybrid aspen. Here, we review recent progress in our understanding of the genetic control of shoot architecture in perennials compared to in annuals.

@article{azeez_early_2021,
	title = {{EARLY} {BUD}-{BREAK} 1 and {EARLY} {BUD}-{BREAK} 3 control resumption of poplar growth after winter dormancy},
	volume = {12},
	issn = {2041-1723},
	url = {http://www.nature.com/articles/s41467-021-21449-0},
	doi = {10/gkcr78},
	abstract = {Abstract
            
              Bud-break is an economically and environmentally important process in trees and shrubs from boreal and temperate latitudes, but its molecular mechanisms are poorly understood. Here, we show that two previously reported transcription factors, EARLY BUD BREAK 1 (EBB1) and SHORT VEGETATIVE PHASE-Like (SVL) directly interact to control bud-break. EBB1 is a positive regulator of bud-break, whereas SVL is a negative regulator of bud-break. EBB1 directly and negatively regulates
              SVL
              expression. We further report the identification and characterization of the EBB3 gene. EBB3 is a temperature-responsive, epigenetically-regulated, positive regulator of bud-break that provides a direct link to activation of the cell cycle during bud-break. EBB3 is an AP2/ERF transcription factor that positively and directly regulates
              CYCLIND3.1
              gene. Our results reveal the architecture of a putative regulatory module that links temperature-mediated control of bud-break with activation of cell cycle.},
	language = {en},
	number = {1},
	urldate = {2021-06-03},
	journal = {Nature Communications},
	author = {Azeez, Abdul and Zhao, Yiru Chen and Singh, Rajesh Kumar and Yordanov, Yordan S. and Dash, Madhumita and Miskolczi, Pal and Stojkovič, Katja and Strauss, Steve H. and Bhalerao, Rishikesh P. and Busov, Victor B.},
	month = dec,
	year = {2021},
	pages = {1123},
}

Abstract Bud-break is an economically and environmentally important process in trees and shrubs from boreal and temperate latitudes, but its molecular mechanisms are poorly understood. Here, we show that two previously reported transcription factors, EARLY BUD BREAK 1 (EBB1) and SHORT VEGETATIVE PHASE-Like (SVL) directly interact to control bud-break. EBB1 is a positive regulator of bud-break, whereas SVL is a negative regulator of bud-break. EBB1 directly and negatively regulates SVL expression. We further report the identification and characterization of the EBB3 gene. EBB3 is a temperature-responsive, epigenetically-regulated, positive regulator of bud-break that provides a direct link to activation of the cell cycle during bud-break. EBB3 is an AP2/ERF transcription factor that positively and directly regulates CYCLIND3.1 gene. Our results reveal the architecture of a putative regulatory module that links temperature-mediated control of bud-break with activation of cell cycle.

@article{baral_external_2021,
	title = {External {Mechanical} {Cues} {Reveal} a {Katanin}-{Independent} {Mechanism} behind {Auxin}-{Mediated} {Tissue} {Bending} in {Plants}},
	volume = {56},
	issn = {15345807},
	url = {https://linkinghub.elsevier.com/retrieve/pii/S1534580720309837},
	doi = {10/ghtbf9},
	language = {en},
	number = {1},
	urldate = {2021-06-03},
	journal = {Developmental Cell},
	author = {Baral, Anirban and Aryal, Bibek and Jonsson, Kristoffer and Morris, Emily and Demes, Elsa and Takatani, Shogo and Verger, Stéphane and Xu, Tongda and Bennett, Malcolm and Hamant, Olivier and Bhalerao, Rishikesh P.},
	month = jan,
	year = {2021},
	pages = {67--80.e3},
}

@article{singh_growing_2021,
	title = {Growing in time: exploring the molecular mechanisms of tree growth},
	volume = {41},
	issn = {1758-4469},
	shorttitle = {Growing in time},
	url = {https://academic.oup.com/treephys/article/41/4/657/5848548},
	doi = {10.1093/treephys/tpaa065},
	abstract = {Abstract
            Trees cover vast areas of the Earth’s landmasses. They mitigate erosion, capture carbon dioxide, produce oxygen and support biodiversity, and also are a source of food, raw materials and energy for human populations. Understanding the growth cycles of trees is fundamental for many areas of research. Trees, like most other organisms, have evolved a circadian clock to synchronize their growth and development with the daily and seasonal cycles of the environment. These regular changes in light, daylength and temperature are perceived via a range of dedicated receptors and cause resetting of the circadian clock to local time. This allows anticipation of daily and seasonal fluctuations and enables trees to co-ordinate their metabolism and physiology to ensure vital processes occur at the optimal times. In this review, we explore the current state of knowledge concerning the regulation of growth and seasonal dormancy in trees, using information drawn from model systems such as Populus spp.},
	language = {en},
	number = {4},
	urldate = {2021-06-07},
	journal = {Tree Physiology},
	author = {Singh, Rajesh Kumar and Bhalerao, Rishikesh P. and Eriksson, Maria E.},
	editor = {Polle, Andrea},
	month = apr,
	year = {2021},
	pages = {657--678},
}

Abstract Trees cover vast areas of the Earth’s landmasses. They mitigate erosion, capture carbon dioxide, produce oxygen and support biodiversity, and also are a source of food, raw materials and energy for human populations. Understanding the growth cycles of trees is fundamental for many areas of research. Trees, like most other organisms, have evolved a circadian clock to synchronize their growth and development with the daily and seasonal cycles of the environment. These regular changes in light, daylength and temperature are perceived via a range of dedicated receptors and cause resetting of the circadian clock to local time. This allows anticipation of daily and seasonal fluctuations and enables trees to co-ordinate their metabolism and physiology to ensure vital processes occur at the optimal times. In this review, we explore the current state of knowledge concerning the regulation of growth and seasonal dormancy in trees, using information drawn from model systems such as Populus spp.

@article{jonsson_mechanochemical_2021,
	title = {Mechanochemical feedback mediates tissue bending required for seedling emergence},
	volume = {31},
	issn = {0960-9822},
	url = {https://www.cell.com/current-biology/abstract/S0960-9822(20)31836-4},
	doi = {10.1016/j.cub.2020.12.016},
	language = {en},
	number = {6},
	urldate = {2021-06-03},
	journal = {Current Biology},
	author = {Jonsson, Kristoffer and Lathe, Rahul S. and Kierzkowski, Daniel and Routier-Kierzkowska, Anne-Lise and Hamant, Olivier and Bhalerao, Rishikesh P.},
	month = mar,
	year = {2021},
	keywords = {Arabidopsis, PIN proteins, PMEI, apical hook, auxin, cell wall, development, differential growth, pectin methylesterification},
	pages = {1154--1164.e3},
}

@article{robinson_variation_2021,
	title = {Variation in non-target traits in genetically modified hybrid aspens does not exceed natural variation},
	volume = {64},
	issn = {1871-6784},
	url = {https://www.sciencedirect.com/science/article/pii/S1871678421000625},
	doi = {10.1016/j.nbt.2021.05.005},
	abstract = {Genetically modified hybrid aspens (Populus tremula L. x P. tremuloides Michx.), selected for increased growth under controlled conditions, have been grown in highly replicated field trials to evaluate how the target trait (growth) translated to natural conditions. Moreover, the variation was compared among genotypes of ecologically important non-target traits: number of shoots, bud set, pathogen infection, amount of insect herbivory, composition of the insect herbivore community and flower bud induction. This variation was compared with the variation in a population of randomly selected natural accessions of P. tremula grown in common garden trials, to estimate how the “unintended variation” present in transgenic trees, which in the future may be commercialized, compares with natural variation. The natural variation in the traits was found to be typically significantly greater. The data suggest that when authorities evaluate the potential risks associated with a field experiment or commercial introduction of transgenic trees, risk evaluation should focus on target traits and that unintentional variation in non-target traits is of less concern.},
	language = {en},
	urldate = {2021-09-21},
	journal = {New Biotechnology},
	author = {Robinson, Kathryn M. and Möller, Linus and Bhalerao, Rishikesh P. and Hertzberg, Magnus and Nilsson, Ove and Jansson, Stefan},
	month = sep,
	year = {2021},
	keywords = {European aspen, Field experiment, Genetically modified, Hybrid aspen, Natural variation, Non-target traits},
	pages = {27--36},
}

Genetically modified hybrid aspens (Populus tremula L. x P. tremuloides Michx.), selected for increased growth under controlled conditions, have been grown in highly replicated field trials to evaluate how the target trait (growth) translated to natural conditions. Moreover, the variation was compared among genotypes of ecologically important non-target traits: number of shoots, bud set, pathogen infection, amount of insect herbivory, composition of the insect herbivore community and flower bud induction. This variation was compared with the variation in a population of randomly selected natural accessions of P. tremula grown in common garden trials, to estimate how the “unintended variation” present in transgenic trees, which in the future may be commercialized, compares with natural variation. The natural variation in the traits was found to be typically significantly greater. The data suggest that when authorities evaluate the potential risks associated with a field experiment or commercial introduction of transgenic trees, risk evaluation should focus on target traits and that unintentional variation in non-target traits is of less concern.

@article{velasquez_xyloglucan_2021,
	title = {Xyloglucan {Remodeling} {Defines} {Auxin}-{Dependent} {Differential} {Tissue} {Expansion} in {Plants}},
	volume = {22},
	issn = {1422-0067},
	doi = {10.3390/ijms22179222},
	abstract = {Size control is a fundamental question in biology, showing incremental complexity in plants, whose cells possess a rigid cell wall. The phytohormone auxin is a vital growth regulator with central importance for differential growth control. Our results indicate that auxin-reliant growth programs affect the molecular complexity of xyloglucans, the major type of cell wall hemicellulose in eudicots. Auxin-dependent induction and repression of growth coincide with reduced and enhanced molecular complexity of xyloglucans, respectively. In agreement with a proposed function in growth control, genetic interference with xyloglucan side decorations distinctly modulates auxin-dependent differential growth rates. Our work proposes that auxin-dependent growth programs have a spatially defined effect on xyloglucan's molecular structure, which in turn affects cell wall mechanics and specifies differential, gravitropic hypocotyl growth.},
	language = {eng},
	number = {17},
	journal = {International Journal of Molecular Sciences},
	author = {Velasquez, Silvia Melina and Guo, Xiaoyuan and Gallemi, Marçal and Aryal, Bibek and Venhuizen, Peter and Barbez, Elke and Dünser, Kai Alexander and Darino, Martin and Pĕnčík, Aleš and Novák, Ondřej and Kalyna, Maria and Mouille, Gregory and Benková, Eva and P Bhalerao, Rishikesh and Mravec, Jozef and Kleine-Vehn, Jürgen},
	month = aug,
	year = {2021},
	keywords = {Arabidopsis, Cell Wall, Fluorescent Antibody Technique, Gene Expression Regulation, Plant, Glucans, Indoleacetic Acids, Peas, Plant Cells, Plant Development, Plant Physiological Phenomena, Signal Transduction, Xylans, auxin, cell wall, gravitropism, growth, hypocotyls, xyloglucans},
	pages = {9222},
}

Size control is a fundamental question in biology, showing incremental complexity in plants, whose cells possess a rigid cell wall. The phytohormone auxin is a vital growth regulator with central importance for differential growth control. Our results indicate that auxin-reliant growth programs affect the molecular complexity of xyloglucans, the major type of cell wall hemicellulose in eudicots. Auxin-dependent induction and repression of growth coincide with reduced and enhanced molecular complexity of xyloglucans, respectively. In agreement with a proposed function in growth control, genetic interference with xyloglucan side decorations distinctly modulates auxin-dependent differential growth rates. Our work proposes that auxin-dependent growth programs have a spatially defined effect on xyloglucan's molecular structure, which in turn affects cell wall mechanics and specifies differential, gravitropic hypocotyl growth.

@article{maurya_genetic_2020,
	title = {A genetic framework for regulation and seasonal adaptation of shoot architecture in hybrid aspen},
	volume = {117},
	issn = {0027-8424, 1091-6490},
	url = {http://www.pnas.org/lookup/doi/10.1073/pnas.2004705117},
	doi = {10.1073/pnas.2004705117},
	abstract = {Shoot architecture is critical for optimizing plant adaptation and productivity. In contrast with annuals, branching in perennials native to temperate and boreal regions must be coordinated with seasonal growth cycles. How branching is coordinated with seasonal growth is poorly understood. We identified key components of the genetic network that controls branching and its regulation by seasonal cues in the model tree hybrid aspen. Our results demonstrate that branching and its control by seasonal cues is mediated by mutually antagonistic action of aspen orthologs of the flowering regulators
              TERMINAL FLOWER 1
              (
              TFL1
              ) and
              APETALA1
              (
              LIKE APETALA 1/LAP1
              ).
              LAP1
              promotes branching through local action in axillary buds.
              LAP1
              acts in a cytokinin-dependent manner, stimulating expression of the cell-cycle regulator
              AIL1
              and suppressing
              BRANCHED1
              expression to promote branching. Short photoperiod and low temperature, the major seasonal cues heralding winter, suppress branching by simultaneous activation of
              TFL1
              and repression of the
              LAP1
              pathway. Our results thus reveal the genetic network mediating control of branching and its regulation by environmental cues facilitating integration of branching with seasonal growth control in perennial trees.},
	language = {en},
	number = {21},
	urldate = {2021-06-07},
	journal = {Proceedings of the National Academy of Sciences},
	author = {Maurya, Jay P. and Miskolczi, Pal C. and Mishra, Sanatkumar and Singh, Rajesh Kumar and Bhalerao, Rishikesh P.},
	month = may,
	year = {2020},
	pages = {11523--11530},
}

Shoot architecture is critical for optimizing plant adaptation and productivity. In contrast with annuals, branching in perennials native to temperate and boreal regions must be coordinated with seasonal growth cycles. How branching is coordinated with seasonal growth is poorly understood. We identified key components of the genetic network that controls branching and its regulation by seasonal cues in the model tree hybrid aspen. Our results demonstrate that branching and its control by seasonal cues is mediated by mutually antagonistic action of aspen orthologs of the flowering regulators TERMINAL FLOWER 1 ( TFL1 ) and APETALA1 ( LIKE APETALA 1/LAP1 ). LAP1 promotes branching through local action in axillary buds. LAP1 acts in a cytokinin-dependent manner, stimulating expression of the cell-cycle regulator AIL1 and suppressing BRANCHED1 expression to promote branching. Short photoperiod and low temperature, the major seasonal cues heralding winter, suppress branching by simultaneous activation of TFL1 and repression of the LAP1 pathway. Our results thus reveal the genetic network mediating control of branching and its regulation by environmental cues facilitating integration of branching with seasonal growth control in perennial trees.

@article{maurya_branching_2020,
	title = {Branching {Regulator} {BRC1} {Mediates} {Photoperiodic} {Control} of {Seasonal} {Growth} in {Hybrid} {Aspen}},
	volume = {30},
	issn = {09609822},
	url = {https://linkinghub.elsevier.com/retrieve/pii/S096098221931440X},
	doi = {10.1016/j.cub.2019.11.001},
	language = {en},
	number = {1},
	urldate = {2021-06-07},
	journal = {Current Biology},
	author = {Maurya, Jay P. and Singh, Rajesh Kumar and Miskolczi, Pal C. and Prasad, Amritha N. and Jonsson, Kristoffer and Wu, Feng and Bhalerao, Rishikesh P.},
	month = jan,
	year = {2020},
	pages = {122--126.e2},
}

@article{aryal_interplay_2020,
	title = {Interplay between {Cell} {Wall} and {Auxin} {Mediates} the {Control} of {Differential} {Cell} {Elongation} during {Apical} {Hook} {Development}},
	volume = {30},
	issn = {09609822},
	url = {https://linkinghub.elsevier.com/retrieve/pii/S0960982220302621},
	doi = {10.1016/j.cub.2020.02.055},
	language = {en},
	number = {9},
	urldate = {2021-06-07},
	journal = {Current Biology},
	author = {Aryal, Bibek and Jonsson, Kristoffer and Baral, Anirban and Sancho-Andres, Gloria and Routier- Kierzkowska, Anne-Lise and Kierzkowski, Daniel and Bhalerao, Rishikesh P.},
	month = may,
	year = {2020},
	pages = {1733--1739.e3},
}

@article{yu_ralf1-feronia_2020,
	title = {The {RALF1}-{FERONIA} interaction modulates endocytosis to mediate control of root growth in \textit{{Arabidopsis}}},
	issn = {1477-9129, 0950-1991},
	url = {https://journals.biologists.com/dev/article/doi/10.1242/dev.189902/266898/The-RALF1-FERONIA-interaction-modulates},
	doi = {10.1242/dev.189902},
	abstract = {The interaction between the receptor-like kinase (RLK) FERONIA (FER) and the secreted peptide Rapid Alkalinization Factor 1 (RALF1) is vital for development and stress responses in Arabidopsis. Ligand-induced membrane dynamics affect the function of several RLKs, but the effects of the RALF1-FER interaction on the dynamics of FER and the ensuing effects on its functionality are poorly understood. Here, we show that RALF1 modulated the dynamics and partitioning of FER-GFP at the plasma membrane (PM). Moreover, FER was internalized by both clathrin-mediated endocytosis (CME) and clathrin-independent endocytosis (CIE) under steady state conditions. After RALF1 treatment, FER-GFP internalization was primarily enhanced via the CME pathway, raising FER-GFP levels in the vacuole. RALF1 treatment also modulated trafficking of other PM proteins such as PIN2-GFP and BRI1-GFP, increasing their vacuolar levels by enhancing their internalization. Importantly, blocking CME attenuated RALF1-mediated root growth inhibition independently of RALF1-induced early signaling, suggesting that the RALF1 can also exert its effects via the CME pathway. These findings reveal that the RALF1-FER interaction modulates plant growth and development and this may also involve endocytosis of PM proteins.},
	language = {en},
	urldate = {2021-06-07},
	journal = {Development},
	author = {Yu, Meng and Li, Ruili and Cui, Yaning and Chen, Weijun and Li, Bin and Zhang, Xi and Bu, Yufen and Cao, Yangyang and Xing, Jingjing and Jewaria, Pawan Kumar and Li, Xiaojuan and Bhalerao, Rishikesh P. and Yu, Feng and Lin, Jinxing},
	month = jan,
	year = {2020},
	pages = {dev.189902},
}

The interaction between the receptor-like kinase (RLK) FERONIA (FER) and the secreted peptide Rapid Alkalinization Factor 1 (RALF1) is vital for development and stress responses in Arabidopsis. Ligand-induced membrane dynamics affect the function of several RLKs, but the effects of the RALF1-FER interaction on the dynamics of FER and the ensuing effects on its functionality are poorly understood. Here, we show that RALF1 modulated the dynamics and partitioning of FER-GFP at the plasma membrane (PM). Moreover, FER was internalized by both clathrin-mediated endocytosis (CME) and clathrin-independent endocytosis (CIE) under steady state conditions. After RALF1 treatment, FER-GFP internalization was primarily enhanced via the CME pathway, raising FER-GFP levels in the vacuole. RALF1 treatment also modulated trafficking of other PM proteins such as PIN2-GFP and BRI1-GFP, increasing their vacuolar levels by enhancing their internalization. Importantly, blocking CME attenuated RALF1-mediated root growth inhibition independently of RALF1-induced early signaling, suggesting that the RALF1 can also exert its effects via the CME pathway. These findings reveal that the RALF1-FER interaction modulates plant growth and development and this may also involve endocytosis of PM proteins.

@article{zhang_chromatin-modifying_2020,
	title = {The chromatin-modifying protein {HUB2} is involved in the regulation of lignin composition in xylem vessels},
	volume = {71},
	issn = {0022-0957, 1460-2431},
	url = {https://academic.oup.com/jxb/article/71/18/5484/5849544},
	doi = {10.1093/jxb/eraa264},
	abstract = {Abstract
            PIRIN2 (PRN2) was earlier reported to suppress syringyl (S)-type lignin accumulation of xylem vessels of Arabidopsis thaliana. In the present study, we report yeast two-hybrid results supporting the interaction of PRN2 with HISTONE MONOUBIQUITINATION2 (HUB2) in Arabidopsis. HUB2 has been previously implicated in several plant developmental processes, but not in lignification. Interaction between PRN2 and HUB2 was verified by β-galactosidase enzymatic and co-immunoprecipitation assays. HUB2 promoted the deposition of S-type lignin in the secondary cell walls of both stem and hypocotyl tissues, as analysed by pyrolysis-GC/MS. Chemical fingerprinting of individual xylem vessel cell walls by Raman and Fourier transform infrared microspectroscopy supported the function of HUB2 in lignin deposition. These results, together with a genetic analysis of the hub2 prn2 double mutant, support the antagonistic function of PRN2 and HUB2 in deposition of S-type lignin. Transcriptome analyses indicated the opposite regulation of the S-type lignin biosynthetic gene FERULATE-5-HYDROXYLASE1 by PRN2 and HUB2 as the underlying mechanism. PRN2 and HUB2 promoter activities co-localized in cells neighbouring the xylem vessel elements, suggesting that the S-type lignin-promoting function of HUB2 is antagonized by PRN2 for the benefit of the guaiacyl (G)-type lignin enrichment of the neighbouring xylem vessel elements.},
	language = {en},
	number = {18},
	urldate = {2021-06-07},
	journal = {Journal of Experimental Botany},
	author = {Zhang, Bo and Sztojka, Bernadette and Seyfferth, Carolin and Escamez, Sacha and Miskolczi, Pál and Chantreau, Maxime and Bakó, László and Delhomme, Nicolas and Gorzsás, András and Bhalerao, Rishikesh P. and Tuominen, Hannele},
	editor = {Turner, Simon},
	month = sep,
	year = {2020},
	pages = {5484--5494},
}

Abstract PIRIN2 (PRN2) was earlier reported to suppress syringyl (S)-type lignin accumulation of xylem vessels of Arabidopsis thaliana. In the present study, we report yeast two-hybrid results supporting the interaction of PRN2 with HISTONE MONOUBIQUITINATION2 (HUB2) in Arabidopsis. HUB2 has been previously implicated in several plant developmental processes, but not in lignification. Interaction between PRN2 and HUB2 was verified by β-galactosidase enzymatic and co-immunoprecipitation assays. HUB2 promoted the deposition of S-type lignin in the secondary cell walls of both stem and hypocotyl tissues, as analysed by pyrolysis-GC/MS. Chemical fingerprinting of individual xylem vessel cell walls by Raman and Fourier transform infrared microspectroscopy supported the function of HUB2 in lignin deposition. These results, together with a genetic analysis of the hub2 prn2 double mutant, support the antagonistic function of PRN2 and HUB2 in deposition of S-type lignin. Transcriptome analyses indicated the opposite regulation of the S-type lignin biosynthetic gene FERULATE-5-HYDROXYLASE1 by PRN2 and HUB2 as the underlying mechanism. PRN2 and HUB2 promoter activities co-localized in cells neighbouring the xylem vessel elements, suggesting that the S-type lignin-promoting function of HUB2 is antagonized by PRN2 for the benefit of the guaiacyl (G)-type lignin enrichment of the neighbouring xylem vessel elements.

@article{singh_tree_2019,
	title = {A {Tree} {Ortholog} of {SHORT} {VEGETATIVE} {PHASE} {Floral} {Repressor} {Mediates} {Photoperiodic} {Control} of {Bud} {Dormancy}},
	volume = {29},
	issn = {09609822},
	url = {https://linkinghub.elsevier.com/retrieve/pii/S0960982218314726},
	doi = {10.1016/j.cub.2018.11.006},
	language = {en},
	number = {1},
	urldate = {2021-06-07},
	journal = {Current Biology},
	author = {Singh, Rajesh Kumar and Miskolczi, Pal and Maurya, Jay P. and Bhalerao, Rishikesh P.},
	month = jan,
	year = {2019},
	pages = {128--133.e2},
}

@article{yu_abscisic_2019,
	title = {Abscisic acid signalling mediates biomass trade‐off and allocation in poplar},
	volume = {223},
	issn = {0028-646X, 1469-8137},
	url = {https://onlinelibrary.wiley.com/doi/abs/10.1111/nph.15878},
	doi = {10/ghtbhc},
	language = {en},
	number = {3},
	urldate = {2021-06-07},
	journal = {New Phytologist},
	author = {Yu, Dade and Wildhagen, Henning and Tylewicz, Szymon and Miskolczi, Pal C. and Bhalerao, Rishikesh P. and Polle, Andrea},
	month = aug,
	year = {2019},
	pages = {1192--1203},
}

@article{miskolczi_long-range_2019,
	title = {Long-range mobile signals mediate seasonal control of shoot growth},
	volume = {116},
	issn = {0027-8424, 1091-6490},
	url = {http://www.pnas.org/lookup/doi/10.1073/pnas.1902199116},
	doi = {10/gg4gdt},
	abstract = {In perennial plants, seasonal shifts provide cues that control adaptive growth patterns of the shoot apex. However, where these seasonal cues are sensed and communicated to the shoot apex remains unknown. We demonstrate that systemic signals from leaves play key roles in seasonal control of shoot growth in model tree hybrid aspen. Grafting experiments reveal that the tree ortholog of
              Arabidopsis
              flowering time regulator
              FLOWERING LOCUS T
              (
              FT
              ) and the plant hormone gibberellic acid (GA) systemically convey seasonal cues to the shoot apex. GA (unlike
              FT
              ) also acts locally in shoot apex, downstream of
              FT
              in seasonal growth control. At the shoot apex, antagonistic factors—
              LAP1
              , a target of
              FT
              and the
              FT
              antagonist
              TERMINAL FLOWER 1
              (
              TFL1
              )—act locally to promote and suppress seasonal growth, respectively. These data reveal seasonal changes perceived in leaves that are communicated to the shoot apex by systemic signals that, in concert with locally acting components, control adaptive growth patterns.},
	language = {en},
	number = {22},
	urldate = {2021-06-07},
	journal = {Proceedings of the National Academy of Sciences},
	author = {Miskolczi, Pál and Singh, Rajesh Kumar and Tylewicz, Szymon and Azeez, Abdul and Maurya, Jay P. and Tarkowská, Danuše and Novák, Ondřej and Jonsson, Kristoffer and Bhalerao, Rishikesh P.},
	month = may,
	year = {2019},
	pages = {10852--10857},
}

In perennial plants, seasonal shifts provide cues that control adaptive growth patterns of the shoot apex. However, where these seasonal cues are sensed and communicated to the shoot apex remains unknown. We demonstrate that systemic signals from leaves play key roles in seasonal control of shoot growth in model tree hybrid aspen. Grafting experiments reveal that the tree ortholog of Arabidopsis flowering time regulator FLOWERING LOCUS T ( FT ) and the plant hormone gibberellic acid (GA) systemically convey seasonal cues to the shoot apex. GA (unlike FT ) also acts locally in shoot apex, downstream of FT in seasonal growth control. At the shoot apex, antagonistic factors— LAP1 , a target of FT and the FT antagonist TERMINAL FLOWER 1 ( TFL1 )—act locally to promote and suppress seasonal growth, respectively. These data reveal seasonal changes perceived in leaves that are communicated to the shoot apex by systemic signals that, in concert with locally acting components, control adaptive growth patterns.

@article{gendre_rho--plant-activated_2019,
	title = {Rho-of-plant-activated root hair formation requires \textit{{Arabidopsis} {YIP4a}/b} gene function},
	issn = {1477-9129, 0950-1991},
	url = {https://journals.biologists.com/dev/article/doi/10.1242/dev.168559/264580/Rho-of-plant-activated-root-hair-formation},
	doi = {10/ghtbhf},
	abstract = {Root hairs are protrusions from root epidermal cells with critical roles in plant soil interactions. While much is known about patterning, polarity and tip growth of root hairs, contributions of membrane trafficking to hair initiation remain poorly understood. Here we demonstrate that the trans-Golgi network-localized YPT-INTERACTING PROTEINS 4a/b contribute to activation and plasma membrane accumulation of Rho-of-plant (ROP) small GTPases during hair initiation, identifying YIP4a/b as central trafficking components in ROP-dependent root hair formation.},
	language = {en},
	urldate = {2021-06-07},
	journal = {Development},
	author = {Gendre, Delphine and Baral, Anirban and Dang, Xie and Esnay, Nicolas and Boutté, Yohann and Stanislas, Thomas and Vain, Thomas and Claverol, Stéphane and Gustavsson, Anna and Lin, Deshu and Grebe, Markus and Bhalerao, Rishikesh P.},
	month = jan,
	year = {2019},
	pages = {dev.168559},
}

Root hairs are protrusions from root epidermal cells with critical roles in plant soil interactions. While much is known about patterning, polarity and tip growth of root hairs, contributions of membrane trafficking to hair initiation remain poorly understood. Here we demonstrate that the trans-Golgi network-localized YPT-INTERACTING PROTEINS 4a/b contribute to activation and plasma membrane accumulation of Rho-of-plant (ROP) small GTPases during hair initiation, identifying YIP4a/b as central trafficking components in ROP-dependent root hair formation.

@article{taylor_sustainable_2019,
	title = {Sustainable bioenergy for climate mitigation: developing drought-tolerant trees and grasses},
	volume = {124},
	issn = {0305-7364, 1095-8290},
	shorttitle = {Sustainable bioenergy for climate mitigation},
	url = {https://academic.oup.com/aob/article/124/4/513/5609063},
	doi = {10.1093/aob/mcz146},
	abstract = {Abstract
            
              Background and Aims
              Bioenergy crops are central to climate mitigation strategies that utilize biogenic carbon, such as BECCS (bioenergy with carbon capture and storage), alongside the use of biomass for heat, power, liquid fuels and, in the future, biorefining to chemicals. Several promising lignocellulosic crops are emerging that have no food role – fast-growing trees and grasses – but are well suited as bioenergy feedstocks, including Populus, Salix, Arundo, Miscanthus, Panicum and Sorghum.
            
            
              Scope
              These promising crops remain largely undomesticated and, until recently, have had limited germplasm resources. In order to avoid competition with food crops for land and nature conservation, it is likely that future bioenergy crops will be grown on marginal land that is not needed for food production and is of poor quality and subject to drought stress. Thus, here we define an ideotype for drought tolerance that will enable biomass production to be maintained in the face of moderate drought stress. This includes traits that can readily be measured in wide populations of several hundred unique genotypes for genome-wide association studies, alongside traits that are informative but can only easily be assessed in limited numbers or training populations that may be more suitable for genomic selection. Phenotyping, not genotyping, is now the major bottleneck for progress, since in all lignocellulosic crops studied extensive use has been made of next-generation sequencing such that several thousand markers are now available and populations are emerging that will enable rapid progress for drought-tolerance breeding. The emergence of novel technologies for targeted genotyping by sequencing are particularly welcome. Genome editing has already been demonstrated for Populus and offers significant potential for rapid deployment of drought-tolerant crops through manipulation of ABA receptors, as demonstrated in Arabidopsis, with other gene targets yet to be tested.
            
            
              Conclusions
              Bioenergy is predicted to be the fastest-developing renewable energy over the coming decade and significant investment over the past decade has been made in developing genomic resources and in collecting wild germplasm from within the natural ranges of several tree and grass crops. Harnessing these resources for climate-resilient crops for the future remains a challenge but one that is likely to be successful.},
	language = {en},
	number = {4},
	urldate = {2021-06-07},
	journal = {Annals of Botany},
	author = {Taylor, G and Donnison, I S and Murphy-Bokern, D and Morgante, M and Bogeat-Triboulot, M-B and Bhalerao, Rishikesh P. and Hertzberg, M and Polle, A and Harfouche, A and Alasia, F and Petoussi, V and Trebbi, D and Schwarz, K and Keurentjes, J J B and Centritto, M and Genty, B and Flexas, J and Grill, E and Salvi, S and Davies, W J},
	month = oct,
	year = {2019},
	pages = {513--520},
}

Abstract Background and Aims Bioenergy crops are central to climate mitigation strategies that utilize biogenic carbon, such as BECCS (bioenergy with carbon capture and storage), alongside the use of biomass for heat, power, liquid fuels and, in the future, biorefining to chemicals. Several promising lignocellulosic crops are emerging that have no food role – fast-growing trees and grasses – but are well suited as bioenergy feedstocks, including Populus, Salix, Arundo, Miscanthus, Panicum and Sorghum. Scope These promising crops remain largely undomesticated and, until recently, have had limited germplasm resources. In order to avoid competition with food crops for land and nature conservation, it is likely that future bioenergy crops will be grown on marginal land that is not needed for food production and is of poor quality and subject to drought stress. Thus, here we define an ideotype for drought tolerance that will enable biomass production to be maintained in the face of moderate drought stress. This includes traits that can readily be measured in wide populations of several hundred unique genotypes for genome-wide association studies, alongside traits that are informative but can only easily be assessed in limited numbers or training populations that may be more suitable for genomic selection. Phenotyping, not genotyping, is now the major bottleneck for progress, since in all lignocellulosic crops studied extensive use has been made of next-generation sequencing such that several thousand markers are now available and populations are emerging that will enable rapid progress for drought-tolerance breeding. The emergence of novel technologies for targeted genotyping by sequencing are particularly welcome. Genome editing has already been demonstrated for Populus and offers significant potential for rapid deployment of drought-tolerant crops through manipulation of ABA receptors, as demonstrated in Arabidopsis, with other gene targets yet to be tested. Conclusions Bioenergy is predicted to be the fastest-developing renewable energy over the coming decade and significant investment over the past decade has been made in developing genomic resources and in collecting wild germplasm from within the natural ranges of several tree and grass crops. Harnessing these resources for climate-resilient crops for the future remains a challenge but one that is likely to be successful.

@article{fischer_dynamics_2019,
	title = {The {Dynamics} of {Cambial} {Stem} {Cell} {Activity}},
	volume = {70},
	issn = {1543-5008, 1545-2123},
	url = {https://www.annualreviews.org/doi/10.1146/annurev-arplant-050718-100402},
	doi = {10/gjcsp3},
	abstract = {Stem cell populations in meristematic tissues at distinct locations in the plant body provide the potency of continuous plant growth. Primary meristems, at the apices of the plant body, contribute mainly to the elongation of the main plant axes, whereas secondary meristems in lateral positions are responsible for the thickening of these axes. The stem cells of the vascular cambium—a secondary lateral meristem—produce the secondary phloem (bast) and secondary xylem (wood). The sites of primary and secondary growth are spatially separated, and mobile signals are expected to coordinate growth rates between apical and lateral stem cell populations. Although the underlying mechanisms have not yet been uncovered, it seems likely that hormones, peptides, and mechanical cues orchestrate primary and secondary growth. In this review, we highlight the current knowledge and recent discoveries of how cambial stem cell activity is regulated, with a focus on mobile signals and the response of cambial activity to environmental and stress factors.},
	language = {en},
	number = {1},
	urldate = {2021-06-07},
	journal = {Annual Review of Plant Biology},
	author = {Fischer, Urs and Kucukoglu, Melis and Helariutta, Ykä and Bhalerao, Rishikesh P.},
	month = apr,
	year = {2019},
	pages = {293--319},
}

Stem cell populations in meristematic tissues at distinct locations in the plant body provide the potency of continuous plant growth. Primary meristems, at the apices of the plant body, contribute mainly to the elongation of the main plant axes, whereas secondary meristems in lateral positions are responsible for the thickening of these axes. The stem cells of the vascular cambium—a secondary lateral meristem—produce the secondary phloem (bast) and secondary xylem (wood). The sites of primary and secondary growth are spatially separated, and mobile signals are expected to coordinate growth rates between apical and lateral stem cell populations. Although the underlying mechanisms have not yet been uncovered, it seems likely that hormones, peptides, and mechanical cues orchestrate primary and secondary growth. In this review, we highlight the current knowledge and recent discoveries of how cambial stem cell activity is regulated, with a focus on mobile signals and the response of cambial activity to environmental and stress factors.

@article{singh_genetic_2018,
	title = {A genetic network mediating the control of bud break in hybrid aspen},
	volume = {9},
	issn = {2041-1723},
	url = {http://www.nature.com/articles/s41467-018-06696-y},
	doi = {10/gffvjm},
	language = {en},
	number = {1},
	urldate = {2021-06-07},
	journal = {Nature Communications},
	author = {Singh, Rajesh Kumar and Maurya, Jay P. and Azeez, Abdul and Miskolczi, Pal and Tylewicz, Szymon and Stojkovič, Katja and Delhomme, Nicolas and Busov, Victor and Bhalerao, Rishikesh P.},
	month = dec,
	year = {2018},
	pages = {4173},
}

@article{eklund_evolutionarily_2018,
	title = {An {Evolutionarily} {Conserved} {Abscisic} {Acid} {Signaling} {Pathway} {Regulates} {Dormancy} in the {Liverwort} {Marchantia} polymorpha},
	volume = {28},
	issn = {09609822},
	url = {https://linkinghub.elsevier.com/retrieve/pii/S0960982218313472},
	doi = {10/gfpxm6},
	language = {en},
	number = {22},
	urldate = {2021-06-07},
	journal = {Current Biology},
	author = {Eklund, D. Magnus and Kanei, Masakazu and Flores-Sandoval, Eduardo and Ishizaki, Kimitsune and Nishihama, Ryuichi and Kohchi, Takayuki and Lagercrantz, Ulf and Bhalerao, Rishikesh P. and Sakata, Yoichi and Bowman, John L.},
	month = nov,
	year = {2018},
	pages = {3691--3699.e3},
}

@article{maurya_environmentally_2018,
	title = {Environmentally {Sensitive} {Molecular} {Switches} {Drive} {Poplar} {Phenology}},
	volume = {9},
	issn = {1664-462X},
	url = {https://www.frontiersin.org/article/10.3389/fpls.2018.01873/full},
	doi = {10.3389/fpls.2018.01873},
	urldate = {2021-06-07},
	journal = {Frontiers in Plant Science},
	author = {Maurya, Jay P. and Triozzi, Paolo M. and Bhalerao, Rishikesh P. and Perales, Mariano},
	month = dec,
	year = {2018},
	pages = {1873},
}

@article{ravikumar_independent_2018,
	title = {Independent yet overlapping pathways ensure the robustness and responsiveness of trans-{Golgi} network functions in \textit{{Arabidopsis}}},
	volume = {145},
	issn = {1477-9129, 0950-1991},
	url = {https://journals.biologists.com/dev/article/145/21/dev169201/48526/Independent-yet-overlapping-pathways-ensure-the},
	doi = {10/gfqn3d},
	abstract = {ABSTRACT
            The trans-Golgi-network (TGN) has essential housekeeping functions in secretion, endocytosis and protein sorting, but also more specialized functions in plant development. How the robustness of basal TGN function is ensured while specialized functions are differentially regulated is poorly understood. Here, we investigate two key regulators of TGN structure and function, ECHIDNA and the Transport Protein Particle II (TRAPPII) tethering complex. An analysis of physical, network and genetic interactions suggests that two network communities are implicated in TGN function and that ECHIDNA and TRAPPII belong to distinct yet overlapping pathways. Whereas ECHIDNA and TRAPPII colocalized at the TGN in interphase cells, their localization diverged in dividing cells. Moreover, ECHIDNA and TRAPPII localization patterns were mutually independent. TGN structure, endocytosis and sorting decisions were differentially impacted in echidna and trappii mutants. Our analyses point to a partitioning of specialized TGN functions, with ECHIDNA being required for cell elongation and TRAPPII for cytokinesis. Two independent pathways able to compensate for each other might contribute to the robustness of TGN housekeeping functions and to the responsiveness and fine tuning of its specialized functions.},
	language = {en},
	number = {21},
	urldate = {2021-06-07},
	journal = {Development},
	author = {Ravikumar, Raksha and Kalbfuß, Nils and Gendre, Delphine and Steiner, Alexander and Altmann, Melina and Altmann, Stefan and Rybak, Katarzyna and Edelmann, Holger and Stephan, Friederike and Lampe, Marko and Facher, Eva and Wanner, Gerhard and Falter-Braun, Pascal and Bhalerao, Rishikesh P. and Assaad, Farhah F.},
	month = nov,
	year = {2018},
	pages = {dev169201},
}

ABSTRACT The trans-Golgi-network (TGN) has essential housekeeping functions in secretion, endocytosis and protein sorting, but also more specialized functions in plant development. How the robustness of basal TGN function is ensured while specialized functions are differentially regulated is poorly understood. Here, we investigate two key regulators of TGN structure and function, ECHIDNA and the Transport Protein Particle II (TRAPPII) tethering complex. An analysis of physical, network and genetic interactions suggests that two network communities are implicated in TGN function and that ECHIDNA and TRAPPII belong to distinct yet overlapping pathways. Whereas ECHIDNA and TRAPPII colocalized at the TGN in interphase cells, their localization diverged in dividing cells. Moreover, ECHIDNA and TRAPPII localization patterns were mutually independent. TGN structure, endocytosis and sorting decisions were differentially impacted in echidna and trappii mutants. Our analyses point to a partitioning of specialized TGN functions, with ECHIDNA being required for cell elongation and TRAPPII for cytokinesis. Two independent pathways able to compensate for each other might contribute to the robustness of TGN housekeeping functions and to the responsiveness and fine tuning of its specialized functions.

@article{tylewicz_photoperiodic_2018,
	title = {Photoperiodic control of seasonal growth is mediated by {ABA} acting on cell-cell communication},
	volume = {360},
	issn = {0036-8075, 1095-9203},
	url = {https://www.sciencemag.org/lookup/doi/10.1126/science.aan8576},
	doi = {10/gc8wcn},
	language = {en},
	number = {6385},
	urldate = {2021-06-07},
	journal = {Science},
	author = {Tylewicz, S. and Petterle, A. and Marttila, S. and Miskolczi, P. and Azeez, A. and Singh, R. K. and Immanen, J. and Mähler, N. and Hvidsten, T. R. and Eklund, D. M. and Bowman, J. L. and Helariutta, Y. and Bhalerao, Rishikesh P.},
	month = apr,
	year = {2018},
	pages = {212--215},
}

@article{grimberg_storage_2018,
	title = {Storage lipid accumulation is controlled by photoperiodic signal acting via regulators of growth cessation and dormancy in hybrid aspen},
	volume = {219},
	issn = {0028646X},
	url = {http://doi.wiley.com/10.1111/nph.15197},
	doi = {10.1111/nph.15197},
	language = {en},
	number = {2},
	urldate = {2021-06-07},
	journal = {New Phytologist},
	author = {Grimberg, Åsa and Lager, Ida and Street, Nathaniel R. and Robinson, Kathryn M. and Marttila, Salla and Mähler, Niklas and Ingvarsson, Pär K. and Bhalerao, Rishikesh P.},
	month = jul,
	year = {2018},
	pages = {619--630},
}

@article{bhalerao_environmental_2017,
	title = {Environmental and hormonal control of cambial stem cell dynamics},
	volume = {68},
	issn = {0022-0957, 1460-2431},
	url = {https://academic.oup.com/jxb/article-lookup/doi/10.1093/jxb/erw466},
	doi = {10.1093/jxb/erw466},
	language = {en},
	number = {1},
	urldate = {2021-06-07},
	journal = {Journal of Experimental Botany},
	author = {Bhalerao, Rishikesh P. and Fischer, Urs},
	month = jan,
	year = {2017},
	pages = {79--87},
}

@article{jonsson_ethylene_2017,
	title = {Ethylene {Regulates} {Differential} {Growth} via {BIG} {ARF}-{GEF}-{Dependent} {Post}-{Golgi} {Secretory} {Trafficking} in {Arabidopsis}},
	volume = {29},
	issn = {1040-4651, 1532-298X},
	url = {https://academic.oup.com/plcell/article/29/5/1039-1052/6099211},
	doi = {10.1105/tpc.16.00743},
	language = {en},
	number = {5},
	urldate = {2021-06-07},
	journal = {The Plant Cell},
	author = {Jonsson, Kristoffer and Boutté, Yohann and Singh, Rajesh Kumar and Gendre, Delphine and Bhalerao, Rishikesh P.},
	month = may,
	year = {2017},
	pages = {1039--1052},
}

@article{maurya_photoperiod-_2017,
	title = {Photoperiod- and temperature-mediated control of growth cessation and dormancy in trees: a molecular perspective},
	volume = {120},
	issn = {1095-8290},
	shorttitle = {Photoperiod- and temperature-mediated control of growth cessation and dormancy in trees},
	doi = {10/gbx6rk},
	abstract = {Background: How plants adapt their developmental patterns to regular seasonal changes is an important question in biology. The annual growth cycle in perennial long-lived trees is yet another example of how plants can adapt to seasonal changes. The two main signals that plants rely on to respond to seasonal changes are photoperiod and temperature, and these signals have critical roles in the temporal regulation of the annual growth cycle of trees.
Scope: This review presents the latest findings to provide insight into the molecular mechanisms that underlie how photoperiodic and temperature signals regulate seasonal growth in trees.
Conclusion: The results point to a high level of conservation in the signalling pathways that mediate photoperiodic control of seasonal growth in trees and flowering in annual plants such as arabidopsis. Furthermore, the data indicate that symplastic communication may mediate certain aspects of seasonal growth. Although considerable insight into the control of phenology in model plants such as poplar and spruce has been obtained, the future challenge is extending these studies to other, non-model trees.},
	language = {eng},
	number = {3},
	journal = {Annals of Botany},
	author = {Maurya, Jay P. and Bhalerao, Rishikesh P.},
	month = sep,
	year = {2017},
	pmid = {28605491},
	pmcid = {PMC5591416},
	keywords = {Hybrid aspen (Populus tremula × P. tremuloides), Photoperiod, Picea, Plant Dormancy, Populus, Seasons, Temperature, Trees, dormancy, ecodormant, endodormant, growth cessation, phenology, seasonal growth},
	pages = {351--360},
}

Background: How plants adapt their developmental patterns to regular seasonal changes is an important question in biology. The annual growth cycle in perennial long-lived trees is yet another example of how plants can adapt to seasonal changes. The two main signals that plants rely on to respond to seasonal changes are photoperiod and temperature, and these signals have critical roles in the temporal regulation of the annual growth cycle of trees. Scope: This review presents the latest findings to provide insight into the molecular mechanisms that underlie how photoperiodic and temperature signals regulate seasonal growth in trees. Conclusion: The results point to a high level of conservation in the signalling pathways that mediate photoperiodic control of seasonal growth in trees and flowering in annual plants such as arabidopsis. Furthermore, the data indicate that symplastic communication may mediate certain aspects of seasonal growth. Although considerable insight into the control of phenology in model plants such as poplar and spruce has been obtained, the future challenge is extending these studies to other, non-model trees.

@article{immanen_cytokinin_2016,
	title = {Cytokinin and {Auxin} {Display} {Distinct} but {Interconnected} {Distribution} and {Signaling} {Profiles} to {Stimulate} {Cambial} {Activity}},
	volume = {26},
	issn = {09609822},
	url = {https://linkinghub.elsevier.com/retrieve/pii/S0960982216305504},
	doi = {10/f82nd5},
	language = {en},
	number = {15},
	urldate = {2021-06-07},
	journal = {Current Biology},
	author = {Immanen, Juha and Nieminen, Kaisa and Smolander, Olli-Pekka and Kojima, Mikiko and Alonso Serra, Juan and Koskinen, Patrik and Zhang, Jing and Elo, Annakaisa and Mähönen, Ari Pekka and Street, Nathaniel and Bhalerao, Rishikesh P. and Paulin, Lars and Auvinen, Petri and Sakakibara, Hitoshi and Helariutta, Ykä},
	month = aug,
	year = {2016},
	pages = {1990--1997},
}

@article{wattelet-boyer_enrichment_2016,
	title = {Enrichment of hydroxylated {C24}- and {C26}-acyl-chain sphingolipids mediates {PIN2} apical sorting at trans-{Golgi} network subdomains},
	volume = {7},
	issn = {2041-1723},
	url = {http://www.nature.com/articles/ncomms12788},
	doi = {10/ghtbhj},
	language = {en},
	number = {1},
	urldate = {2021-06-07},
	journal = {Nature Communications},
	author = {Wattelet-Boyer, Valérie and Brocard, Lysiane and Jonsson, Kristoffer and Esnay, Nicolas and Joubès, Jérôme and Domergue, Frédéric and Mongrand, Sébastien and Raikhel, Natasha and Bhalerao, Rishikesh P. and Moreau, Patrick and Boutté, Yohann},
	month = nov,
	year = {2016},
	pages = {12788},
}

@article{baral_exploring_2016,
	title = {Exploring exocytosis using chemical genomics},
	volume = {113},
	issn = {0027-8424, 1091-6490},
	url = {http://www.pnas.org/lookup/doi/10.1073/pnas.1522317113},
	doi = {10.1073/pnas.1522317113},
	language = {en},
	number = {1},
	urldate = {2021-06-07},
	journal = {Proceedings of the National Academy of Sciences},
	author = {Baral, Anirban and Bhalerao, Rishikesh P.},
	month = jan,
	year = {2016},
	pages = {14--16},
}

@article{randall_aintegumenta_2015,
	title = {{AINTEGUMENTA} and the {D}-type cyclin {CYCD3};1 regulate root secondary growth and respond to cytokinins},
	volume = {4},
	issn = {2046-6390 (Print) 2046-6390 (Linking)},
	url = {https://www.ncbi.nlm.nih.gov/pubmed/26340943},
	doi = {10.1242/bio.013128},
	abstract = {Higher plant vasculature is characterized by two distinct developmental phases. Initially, a well-defined radial primary pattern is established. In eudicots, this is followed by secondary growth, which involves development of the cambium and is required for efficient water and nutrient transport and wood formation. Regulation of secondary growth involves several phytohormones, and cytokinins have been implicated as key players, particularly in the activation of cell proliferation, but the molecular mechanisms mediating this hormonal control remain unknown. Here we show that the genes encoding the transcription factor AINTEGUMENTA (ANT) and the D-type cyclin CYCD3;1 are expressed in the vascular cambium of Arabidopsis roots, respond to cytokinins and are both required for proper root secondary thickening. Cytokinin regulation of ANT and CYCD3 also occurs during secondary thickening of poplar stems, suggesting this represents a conserved regulatory mechanism.},
	language = {en},
	number = {10},
	urldate = {2021-06-07},
	journal = {Biol Open},
	author = {Randall, R. S. and Miyashima, S. and Blomster, T. and Zhang, J. and Elo, A. and Karlberg, A. and Immanen, J. and Nieminen, K. and Lee, J. Y. and Kakimoto, T. and Blajecka, K. and Melnyk, C. W. and Alcasabas, A. and Forzani, C. and Matsumoto-Kitano, M. and Mahonen, A. P. and Bhalerao, Rishikesh P. and Dewitte, W. and Helariutta, Y. and Murray, J. A.},
	month = sep,
	year = {2015},
	note = {Edition: 2015/09/06},
	keywords = {Aintegumenta, Cyclin D, Cytokinins, Root development, Secondary growth},
	pages = {1229--36},
}

Higher plant vasculature is characterized by two distinct developmental phases. Initially, a well-defined radial primary pattern is established. In eudicots, this is followed by secondary growth, which involves development of the cambium and is required for efficient water and nutrient transport and wood formation. Regulation of secondary growth involves several phytohormones, and cytokinins have been implicated as key players, particularly in the activation of cell proliferation, but the molecular mechanisms mediating this hormonal control remain unknown. Here we show that the genes encoding the transcription factor AINTEGUMENTA (ANT) and the D-type cyclin CYCD3;1 are expressed in the vascular cambium of Arabidopsis roots, respond to cytokinins and are both required for proper root secondary thickening. Cytokinin regulation of ANT and CYCD3 also occurs during secondary thickening of poplar stems, suggesting this represents a conserved regulatory mechanism.

@article{eklund_auxin_2015,
	title = {Auxin {Produced} by the {Indole}-3-{Pyruvic} {Acid} {Pathway} {Regulates} {Development} and {Gemmae} {Dormancy} in the {Liverwort} {Marchantia} polymorpha},
	volume = {27},
	issn = {1532-298X (Electronic) 1040-4651 (Linking)},
	url = {https://www.ncbi.nlm.nih.gov/pubmed/26036256},
	doi = {10.1105/tpc.15.00065},
	abstract = {The plant hormone auxin (indole-3-acetic acid [IAA]) has previously been suggested to regulate diverse forms of dormancy in both seed plants and liverworts. Here, we use loss- and gain-of-function alleles for auxin synthesis- and signaling-related genes, as well as pharmacological approaches, to study how auxin regulates development and dormancy in the gametophyte generation of the liverwort Marchantia polymorpha. We found that M. polymorpha possess the smallest known toolkit for the indole-3-pyruvic acid (IPyA) pathway in any land plant and that this auxin synthesis pathway mainly is active in meristematic regions of the thallus. Previously a Trp-independent auxin synthesis pathway has been suggested to produce a majority of IAA in bryophytes. Our results indicate that the Trp-dependent IPyA pathway produces IAA that is essential for proper development of the gametophyte thallus of M. polymorpha. Furthermore, we show that dormancy of gemmae is positively regulated by auxin synthesized by the IPyA pathway in the apex of the thallus. Our results indicate that auxin synthesis, transport, and signaling, in addition to its role in growth and development, have a critical role in regulation of gemmae dormancy in M. polymorpha.},
	language = {en},
	number = {6},
	urldate = {2021-06-07},
	journal = {Plant Cell},
	author = {Eklund, D. M. and Ishizaki, K. and Flores-Sandoval, E. and Kikuchi, S. and Takebayashi, Y. and Tsukamoto, S. and Hirakawa, Y. and Nonomura, M. and Kato, H. and Kouno, M. and Bhalerao, Rishikesh P. and Lagercrantz, U. and Kasahara, H. and Kohchi, T. and Bowman, J. L.},
	month = jun,
	year = {2015},
	note = {Edition: 2015/06/04},
	keywords = {Indoleacetic Acids/*metabolism, Indoles/metabolism, Marchantia/*growth \& development/physiology, Plant Components, Aerial/*growth \& development, Plant Dormancy/*physiology, Plant Growth Regulators/metabolism/*physiology},
	pages = {1650--69},
}

The plant hormone auxin (indole-3-acetic acid [IAA]) has previously been suggested to regulate diverse forms of dormancy in both seed plants and liverworts. Here, we use loss- and gain-of-function alleles for auxin synthesis- and signaling-related genes, as well as pharmacological approaches, to study how auxin regulates development and dormancy in the gametophyte generation of the liverwort Marchantia polymorpha. We found that M. polymorpha possess the smallest known toolkit for the indole-3-pyruvic acid (IPyA) pathway in any land plant and that this auxin synthesis pathway mainly is active in meristematic regions of the thallus. Previously a Trp-independent auxin synthesis pathway has been suggested to produce a majority of IAA in bryophytes. Our results indicate that the Trp-dependent IPyA pathway produces IAA that is essential for proper development of the gametophyte thallus of M. polymorpha. Furthermore, we show that dormancy of gemmae is positively regulated by auxin synthesized by the IPyA pathway in the apex of the thallus. Our results indicate that auxin synthesis, transport, and signaling, in addition to its role in growth and development, have a critical role in regulation of gemmae dormancy in M. polymorpha.

@article{tylewicz_dual_2015,
	title = {Dual role of tree florigen activation complex component {FD} in photoperiodic growth control and adaptive response pathways},
	volume = {112},
	issn = {1091-6490 (Electronic) 0027-8424 (Linking)},
	url = {https://www.ncbi.nlm.nih.gov/pubmed/25713384},
	doi = {10.1073/pnas.1423440112},
	abstract = {A complex consisting of evolutionarily conserved FD, flowering locus T (FT) proteins is a regulator of floral transition. Intriguingly, FT orthologs are also implicated in developmental transitions distinct from flowering, such as photoperiodic control of bulbing in onions, potato tuberization, and growth cessation in trees. However, whether an FT-FD complex participates in these transitions and, if so, its mode of action, are unknown. We identified two closely related FD homologs, FD-like 1 (FDL1) and FD-like 2 (FDL2), in the model tree hybrid aspen. Using gain of function and RNAi-suppressed FDL1 and FDL2 transgenic plants, we show that FDL1 and FDL2 have distinct functions and a complex consisting of FT and FDL1 mediates in photoperiodic control of seasonal growth. The downstream target of the FT-FD complex in photoperiodic control of growth is Like AP1 (LAP1), a tree ortholog of the floral meristem identity gene APETALA1. Intriguingly, FDL1 also participates in the transcriptional control of adaptive response and bud maturation pathways, independent of its interaction with FT, presumably via interaction with abscisic acid insensitive 3 (ABI3) transcription factor, a component of abscisic acid (ABA) signaling. Our data reveal that in contrast to its primary role in flowering, FD has dual roles in the photoperiodic control of seasonal growth and stress tolerance in trees. Thus, the functions of FT and FD have diversified during evolution, and FD homologs have acquired roles that are independent of their interaction with FT.},
	language = {en},
	number = {10},
	urldate = {2021-06-07},
	journal = {Proc Natl Acad Sci U S A},
	author = {Tylewicz, S. and Tsuji, H. and Miskolczi, P. and Petterle, A. and Azeez, A. and Jonsson, K. and Shimamoto, K. and Bhalerao, Rishikesh P.},
	month = mar,
	year = {2015},
	note = {Edition: 2015/02/26},
	keywords = {*Adaptation, Physiological, *Photoperiod, Florigen/*metabolism, Trees/growth \& development/*physiology, adaptive response, bud set, growth cessation, hybrid aspen, seasonal growth},
	pages = {3140--5},
}

A complex consisting of evolutionarily conserved FD, flowering locus T (FT) proteins is a regulator of floral transition. Intriguingly, FT orthologs are also implicated in developmental transitions distinct from flowering, such as photoperiodic control of bulbing in onions, potato tuberization, and growth cessation in trees. However, whether an FT-FD complex participates in these transitions and, if so, its mode of action, are unknown. We identified two closely related FD homologs, FD-like 1 (FDL1) and FD-like 2 (FDL2), in the model tree hybrid aspen. Using gain of function and RNAi-suppressed FDL1 and FDL2 transgenic plants, we show that FDL1 and FDL2 have distinct functions and a complex consisting of FT and FDL1 mediates in photoperiodic control of seasonal growth. The downstream target of the FT-FD complex in photoperiodic control of growth is Like AP1 (LAP1), a tree ortholog of the floral meristem identity gene APETALA1. Intriguingly, FDL1 also participates in the transcriptional control of adaptive response and bud maturation pathways, independent of its interaction with FT, presumably via interaction with abscisic acid insensitive 3 (ABI3) transcription factor, a component of abscisic acid (ABA) signaling. Our data reveal that in contrast to its primary role in flowering, FD has dual roles in the photoperiodic control of seasonal growth and stress tolerance in trees. Thus, the functions of FT and FD have diversified during evolution, and FD homologs have acquired roles that are independent of their interaction with FT.

@article{marin-de_la_rosa_genome_2015,
	title = {Genome {Wide} {Binding} {Site} {Analysis} {Reveals} {Transcriptional} {Coactivation} of {Cytokinin}-{Responsive} {Genes} by {DELLA} {Proteins}},
	volume = {11},
	issn = {1553-7404 (Electronic) 1553-7390 (Linking)},
	url = {https://www.ncbi.nlm.nih.gov/pubmed/26134422},
	doi = {10.1371/journal.pgen.1005337},
	abstract = {The ability of plants to provide a plastic response to environmental cues relies on the connectivity between signaling pathways. DELLA proteins act as hubs that relay environmental information to the multiple transcriptional circuits that control growth and development through physical interaction with transcription factors from different families. We have analyzed the presence of one DELLA protein at the Arabidopsis genome by chromatin immunoprecipitation coupled to large-scale sequencing and we find that it binds at the promoters of multiple genes. Enrichment analysis shows a strong preference for cis elements recognized by specific transcription factor families. In particular, we demonstrate that DELLA proteins are recruited by type-B ARABIDOPSIS RESPONSE REGULATORS (ARR) to the promoters of cytokinin-regulated genes, where they act as transcriptional co-activators. The biological relevance of this mechanism is underpinned by the necessity of simultaneous presence of DELLAs and ARRs to restrict root meristem growth and to promote photomorphogenesis.},
	language = {en},
	number = {7},
	urldate = {2021-06-07},
	journal = {PLoS Genet},
	author = {Marin-de la Rosa, N. and Pfeiffer, A. and Hill, K. and Locascio, A. and Bhalerao, Rishikesh P. and Miskolczi, P. and Gronlund, A. L. and Wanchoo-Kohli, A. and Thomas, S. G. and Bennett, M. J. and Lohmann, J. U. and Blazquez, M. A. and Alabadi, D.},
	month = jul,
	year = {2015},
	note = {Edition: 2015/07/03},
	keywords = {Arabidopsis Proteins/genetics/*metabolism, Arabidopsis/*embryology, Base Sequence, Binding Sites/genetics, Chromatin Immunoprecipitation, Cytokinins/*metabolism, DNA, Plant/genetics, DNA-Binding Proteins/*metabolism, Gene Expression Regulation, Plant, Plant Development/physiology, Plant Roots/growth \& development, Promoter Regions, Genetic/genetics, Repressor Proteins/genetics/metabolism, Sequence Analysis, DNA, Signal Transduction, Transcription Factors/*metabolism, Transcriptional Activation/*genetics},
	pages = {e1005337},
}

The ability of plants to provide a plastic response to environmental cues relies on the connectivity between signaling pathways. DELLA proteins act as hubs that relay environmental information to the multiple transcriptional circuits that control growth and development through physical interaction with transcription factors from different families. We have analyzed the presence of one DELLA protein at the Arabidopsis genome by chromatin immunoprecipitation coupled to large-scale sequencing and we find that it binds at the promoters of multiple genes. Enrichment analysis shows a strong preference for cis elements recognized by specific transcription factor families. In particular, we demonstrate that DELLA proteins are recruited by type-B ARABIDOPSIS RESPONSE REGULATORS (ARR) to the promoters of cytokinin-regulated genes, where they act as transcriptional co-activators. The biological relevance of this mechanism is underpinned by the necessity of simultaneous presence of DELLAs and ARRs to restrict root meristem growth and to promote photomorphogenesis.

@article{gendre_journey_2015,
	title = {Journey to the cell surface—the central role of the trans-{Golgi} network in plants},
	volume = {252},
	issn = {0033-183X, 1615-6102},
	url = {http://link.springer.com/10.1007/s00709-014-0693-1},
	doi = {10/f3rqn7},
	language = {en},
	number = {2},
	urldate = {2021-06-08},
	journal = {Protoplasma},
	author = {Gendre, Delphine and Jonsson, Kristoffer and Boutté, Yohann and Bhalerao, Rishikesh P.},
	month = mar,
	year = {2015},
	pages = {385--398},
}

@article{grimberg_transcriptional_2015,
	title = {Transcriptional transitions in {Nicotiana} benthamiana leaves upon induction of oil synthesis by {WRINKLED1} homologs from diverse species and tissues},
	volume = {15},
	issn = {1471-2229 (Electronic) 1471-2229 (Linking)},
	url = {https://www.ncbi.nlm.nih.gov/pubmed/26253704},
	doi = {10.1186/s12870-015-0579-1},
	abstract = {BACKGROUND: Carbon accumulation and remobilization are essential mechanisms in plants to ensure energy transfer between plant tissues with different functions or metabolic needs and to support new generations. Knowledge about the regulation of carbon allocation into oil (triacylglycerol) in plant storage tissue can be of great economic and environmental importance for developing new high-yielding oil crops. Here, the effect on global gene expression as well as on physiological changes in leaves transiently expressing five homologs of the transcription factor WRINKLED1 (WRI1) originating from diverse species and tissues; Arabidopsis thaliana and potato (Solanum tuberosum) seed embryo, poplar (Populus trichocarpa) stem cambium, oat (Avena sativa) grain endosperm, and nutsedge (Cyperus esculentus) tuber parenchyma, were studied by agroinfiltration in Nicotiana benthamiana. RESULTS: All WRI1 homologs induced oil accumulation when expressed in leaf tissue. Transcriptome sequencing revealed that all homologs induced the same general patterns with a drastic shift in gene expression profiles of leaves from that of a typical source tissue to a source-limited sink-like tissue: Transcripts encoding enzymes for plastid uptake and metabolism of phosphoenolpyruvate, fatty acid and oil biosynthesis were up-regulated, as were also transcripts encoding starch degradation. Transcripts encoding enzymes in photosynthesis and starch synthesis were instead down-regulated. Moreover, transcripts representing fatty acid degradation were up-regulated indicating that fatty acids might be degraded to feed the increased need to channel carbons into fatty acid synthesis creating a futile cycle. RT-qPCR analysis of leaves expressing Arabidopsis WRI1 showed the temporal trends of transcripts selected as 'markers' for key metabolic pathways one to five days after agroinfiltration. Chlorophyll fluorescence measurements of leaves expressing Arabidopsis WRI1 showed a significant decrease in photosynthesis, even though effect on starch content could not be observed. CONCLUSIONS: This data gives for the first time a general view on the transcriptional transitions in leaf tissue upon induction of oil synthesis by WRI1. This yields important information about what effects WRI1 may exert on global gene expression during seed and embryo development. The results suggest why high oil content in leaf tissue cannot be achieved by solely transcriptional activation by WRI1, which can be essential knowledge in the development of new high-yielding oil crops.},
	language = {en},
	number = {1},
	urldate = {2021-06-07},
	journal = {BMC Plant Biol},
	author = {Grimberg, A. and Carlsson, A. S. and Marttila, S. and Bhalerao, Rishikesh P. and Hofvander, P.},
	month = aug,
	year = {2015},
	note = {Edition: 2015/08/09},
	keywords = {*Gene Expression Regulation, Plant, Arabidopsis Proteins/*genetics/metabolism, Avena/genetics/metabolism, Carbohydrate Metabolism, Cyperus/genetics/metabolism, Plant Leaves/genetics/metabolism, Plants, Genetically Modified/genetics/metabolism, Populus/genetics/metabolism, Real-Time Polymerase Chain Reaction, Solanum tuberosum/genetics/metabolism, Tobacco/*genetics/metabolism, Transcription Factors/*genetics/metabolism},
	pages = {192},
}

BACKGROUND: Carbon accumulation and remobilization are essential mechanisms in plants to ensure energy transfer between plant tissues with different functions or metabolic needs and to support new generations. Knowledge about the regulation of carbon allocation into oil (triacylglycerol) in plant storage tissue can be of great economic and environmental importance for developing new high-yielding oil crops. Here, the effect on global gene expression as well as on physiological changes in leaves transiently expressing five homologs of the transcription factor WRINKLED1 (WRI1) originating from diverse species and tissues; Arabidopsis thaliana and potato (Solanum tuberosum) seed embryo, poplar (Populus trichocarpa) stem cambium, oat (Avena sativa) grain endosperm, and nutsedge (Cyperus esculentus) tuber parenchyma, were studied by agroinfiltration in Nicotiana benthamiana. RESULTS: All WRI1 homologs induced oil accumulation when expressed in leaf tissue. Transcriptome sequencing revealed that all homologs induced the same general patterns with a drastic shift in gene expression profiles of leaves from that of a typical source tissue to a source-limited sink-like tissue: Transcripts encoding enzymes for plastid uptake and metabolism of phosphoenolpyruvate, fatty acid and oil biosynthesis were up-regulated, as were also transcripts encoding starch degradation. Transcripts encoding enzymes in photosynthesis and starch synthesis were instead down-regulated. Moreover, transcripts representing fatty acid degradation were up-regulated indicating that fatty acids might be degraded to feed the increased need to channel carbons into fatty acid synthesis creating a futile cycle. RT-qPCR analysis of leaves expressing Arabidopsis WRI1 showed the temporal trends of transcripts selected as 'markers' for key metabolic pathways one to five days after agroinfiltration. Chlorophyll fluorescence measurements of leaves expressing Arabidopsis WRI1 showed a significant decrease in photosynthesis, even though effect on starch content could not be observed. CONCLUSIONS: This data gives for the first time a general view on the transcriptional transitions in leaf tissue upon induction of oil synthesis by WRI1. This yields important information about what effects WRI1 may exert on global gene expression during seed and embryo development. The results suggest why high oil content in leaf tissue cannot be achieved by solely transcriptional activation by WRI1, which can be essential knowledge in the development of new high-yielding oil crops.

@article{azeez_tree_2014,
	title = {A {Tree} {Ortholog} of {APETALA1} {Mediates} {Photoperiodic} {Control} of {Seasonal} {Growth}},
	volume = {24},
	issn = {09609822},
	url = {https://linkinghub.elsevier.com/retrieve/pii/S096098221400205X},
	doi = {10/f3ndt6},
	language = {en},
	number = {7},
	urldate = {2021-06-08},
	journal = {Current Biology},
	author = {Azeez, Abdul and Miskolczi, Pál and Tylewicz, Szymon and Bhalerao, Rishikesh P.},
	month = mar,
	year = {2014},
	pages = {717--724},
}

@article{legue_adventitious_2014,
	title = {Adventitious root formation in tree species: involvement of transcription factors},
	volume = {151},
	issn = {00319317},
	shorttitle = {Adventitious root formation in tree species},
	url = {http://doi.wiley.com/10.1111/ppl.12197},
	doi = {10/f3m23c},
	language = {en},
	number = {2},
	urldate = {2021-06-08},
	journal = {Physiologia Plantarum},
	author = {Legué, Valérie and Rigal, Adeline and Bhalerao, Rishikesh P.},
	month = jun,
	year = {2014},
	pages = {192--198},
}

@article{bhalerao_auxin_2014,
	title = {Auxin gradients across wood - instructive or incidental?},
	volume = {151},
	issn = {00319317},
	url = {http://doi.wiley.com/10.1111/ppl.12134},
	doi = {10/f3p7dx},
	language = {en},
	number = {1},
	urldate = {2021-06-08},
	journal = {Physiologia Plantarum},
	author = {Bhalerao, Rishikesh P. and Fischer, Urs},
	month = may,
	year = {2014},
	pages = {43--51},
}

@article{la_rosa_large-scale_2014,
	title = {Large-{Scale} {Identification} of {Gibberellin}-{Related} {Transcription} {Factors} {Defines} {Group} {VII} {ETHYLENE} {RESPONSE} {FACTORS} as {Functional} {DELLA} {Partners}},
	volume = {166},
	issn = {0032-0889, 1532-2548},
	url = {https://academic.oup.com/plphys/article/166/2/1022-1032/6113228},
	doi = {10/f3p5k4},
	language = {en},
	number = {2},
	urldate = {2021-06-08},
	journal = {PLANT PHYSIOLOGY},
	author = {la Rosa, N. M.-d. and Sotillo, B. and Miskolczi, P. and Gibbs, D. J. and Vicente, J. and Carbonero, P. and Onate-Sanchez, L. and Holdsworth, M. J. and Bhalerao, Rishikesh P. and Alabadi, D. and Blazquez, M. A.},
	month = oct,
	year = {2014},
	pages = {1022--1032},
}

@article{mcfarlane_cell_2013,
	title = {Cell {Wall} {Polysaccharides} are {Mislocalized} to the {Vacuole} in echidna {Mutants}},
	volume = {54},
	issn = {1471-9053, 0032-0781},
	url = {https://academic.oup.com/pcp/article-lookup/doi/10.1093/pcp/pct129},
	doi = {10/f23zf4},
	language = {en},
	number = {11},
	urldate = {2021-06-08},
	journal = {Plant and Cell Physiology},
	author = {McFarlane, Heather E. and Watanabe, Yoichiro and Gendre, Delphine and Carruthers, Kimberley and Levesque-Tremblay, Gabriel and Haughn, George W. and Bhalerao, Rishikesh P. and Samuels, Lacey},
	month = nov,
	year = {2013},
	pages = {1867--1880},
}

@article{petterle_daylength_2013,
	title = {Daylength mediated control of seasonal growth patterns in perennial trees},
	volume = {16},
	issn = {13695266},
	url = {https://linkinghub.elsevier.com/retrieve/pii/S1369526613000241},
	doi = {10/f2zsrv},
	language = {en},
	number = {3},
	urldate = {2021-06-08},
	journal = {Current Opinion in Plant Biology},
	author = {Petterle, Anna and Karlberg, Anna and Bhalerao, Rishikesh P.},
	month = jun,
	year = {2013},
	pages = {301--306},
}

@article{boutte_echidna-mediated_2013,
	title = {{ECHIDNA}-mediated post-{Golgi} trafficking of auxin carriers for differential cell elongation},
	volume = {110},
	issn = {0027-8424, 1091-6490},
	url = {http://www.pnas.org/cgi/doi/10.1073/pnas.1309057110},
	doi = {10/f2z6v9},
	language = {en},
	number = {40},
	urldate = {2021-06-08},
	journal = {Proceedings of the National Academy of Sciences},
	author = {Boutte, Y. and Jonsson, K. and McFarlane, H. E. and Johnson, E. and Gendre, D. and Swarup, R. and Friml, J. and Samuels, L. and Robert, S. and Bhalerao, Rishikesh P.},
	month = oct,
	year = {2013},
	pages = {16259--16264},
}

@article{duan_endodermal_2013,
	title = {Endodermal {ABA} {Signaling} {Promotes} {Lateral} {Root} {Quiescence} during {Salt} {Stress} in \textit{{Arabidopsis}} {Seedlings}},
	volume = {25},
	issn = {1532-298X, 1040-4651},
	url = {https://academic.oup.com/plcell/article/25/1/324/6097782},
	doi = {10/f2zqb8},
	abstract = {Abstract
            The endodermal tissue layer is found in the roots of vascular plants and functions as a semipermeable barrier, regulating the transport of solutes from the soil into the vascular stream. As a gateway for solutes, the endodermis may also serve as an important site for sensing and responding to useful or toxic substances in the environment. Here, we show that high salinity, an environmental stress widely impacting agricultural land, regulates growth of the seedling root system through a signaling network operating primarily in the endodermis. We report that salt stress induces an extended quiescent phase in postemergence lateral roots (LRs) whereby the rate of growth is suppressed for several days before recovery begins. Quiescence is correlated with sustained abscisic acid (ABA) response in LRs and is dependent upon genes necessary for ABA biosynthesis, signaling, and transcriptional regulation. We use a tissue-specific strategy to identify the key cell layers where ABA signaling acts to regulate growth. In the endodermis, misexpression of the ABA insensitive1-1 mutant protein, which dominantly inhibits ABA signaling, leads to a substantial recovery in LR growth under salt stress conditions. Gibberellic acid signaling, which antagonizes the ABA pathway, also acts primarily in the endodermis, and we define the crosstalk between these two hormones. Our results identify the endodermis as a gateway with an ABA-dependent guard, which prevents root growth into saline environments.},
	language = {en},
	number = {1},
	urldate = {2021-06-08},
	journal = {The Plant Cell},
	author = {Duan, Lina and Dietrich, Daniela and Ng, Chong Han and Chan, Penny Mei Yeen and Bhalerao, Rishikesh P. and Bennett, Malcolm J. and Dinneny, José R.},
	month = feb,
	year = {2013},
	pages = {324--341},
}

Abstract The endodermal tissue layer is found in the roots of vascular plants and functions as a semipermeable barrier, regulating the transport of solutes from the soil into the vascular stream. As a gateway for solutes, the endodermis may also serve as an important site for sensing and responding to useful or toxic substances in the environment. Here, we show that high salinity, an environmental stress widely impacting agricultural land, regulates growth of the seedling root system through a signaling network operating primarily in the endodermis. We report that salt stress induces an extended quiescent phase in postemergence lateral roots (LRs) whereby the rate of growth is suppressed for several days before recovery begins. Quiescence is correlated with sustained abscisic acid (ABA) response in LRs and is dependent upon genes necessary for ABA biosynthesis, signaling, and transcriptional regulation. We use a tissue-specific strategy to identify the key cell layers where ABA signaling acts to regulate growth. In the endodermis, misexpression of the ABA insensitive1-1 mutant protein, which dominantly inhibits ABA signaling, leads to a substantial recovery in LR growth under salt stress conditions. Gibberellic acid signaling, which antagonizes the ABA pathway, also acts primarily in the endodermis, and we define the crosstalk between these two hormones. Our results identify the endodermis as a gateway with an ABA-dependent guard, which prevents root growth into saline environments.

@article{nystedt_norway_2013,
	title = {The {Norway} spruce genome sequence and conifer genome evolution},
	volume = {497},
	issn = {0028-0836, 1476-4687},
	url = {http://www.nature.com/articles/nature12211},
	doi = {10/f2zsx6},
	language = {en},
	number = {7451},
	urldate = {2021-06-08},
	journal = {Nature},
	author = {Nystedt, Björn and Street, Nathaniel R. and Wetterbom, Anna and Zuccolo, Andrea and Lin, Yao-Cheng and Scofield, Douglas G. and Vezzi, Francesco and Delhomme, Nicolas and Giacomello, Stefania and Alexeyenko, Andrey and Vicedomini, Riccardo and Sahlin, Kristoffer and Sherwood, Ellen and Elfstrand, Malin and Gramzow, Lydia and Holmberg, Kristina and Hällman, Jimmie and Keech, Olivier and Klasson, Lisa and Koriabine, Maxim and Kucukoglu, Melis and Käller, Max and Luthman, Johannes and Lysholm, Fredrik and Niittylä, Totte and Olson, Åke and Rilakovic, Nemanja and Ritland, Carol and Rosselló, Josep A. and Sena, Juliana and Svensson, Thomas and Talavera-López, Carlos and Theißen, Günter and Tuominen, Hannele and Vanneste, Kevin and Wu, Zhi-Qiang and Zhang, Bo and Zerbe, Philipp and Arvestad, Lars and Bhalerao, Rishikesh P. and Bohlmann, Joerg and Bousquet, Jean and Garcia Gil, Rosario and Hvidsten, Torgeir R. and de Jong, Pieter and MacKay, John and Morgante, Michele and Ritland, Kermit and Sundberg, Björn and Lee Thompson, Stacey and Van de Peer, Yves and Andersson, Björn and Nilsson, Ove and Ingvarsson, Pär K. and Lundeberg, Joakim and Jansson, Stefan},
	month = may,
	year = {2013},
	pages = {579--584},
}

@article{gendre_trans-golgi_2013,
	title = {Trans-{Golgi} {Network} {Localized} {ECHIDNA}/{Ypt} {Interacting} {Protein} {Complex} {Is} {Required} for the {Secretion} of {Cell} {Wall} {Polysaccharides} in {Arabidopsis}},
	volume = {25},
	issn = {1040-4651},
	url = {https://doi.org/10.1105/tpc.113.112482},
	doi = {10/f22fqp},
	abstract = {The secretion of cell wall polysaccharides through the trans-Golgi network (TGN) is required for plant cell elongation. However, the components mediating the post-Golgi secretion of pectin and hemicellulose, the two major cell wall polysaccharides, are largely unknown. We identified evolutionarily conserved YPT/RAB GTPase Interacting Protein 4a (YIP4a) and YIP4b (formerly YIP2), which form a TGN-localized complex with ECHIDNA (ECH) in Arabidopsis thaliana. The localization of YIP4 and ECH proteins at the TGN is interdependent and influences the localization of VHA-a1 and SYP61, which are key components of the TGN. YIP4a and YIP4b act redundantly, and the yip4a yip4b double mutants have a cell elongation defect. Genetic, biochemical, and cell biological analyses demonstrate that the ECH/YIP4 complex plays a key role in TGN-mediated secretion of pectin and hemicellulose to the cell wall in dark-grown hypocotyls and in secretory cells of the seed coat. In keeping with these observations, Fourier transform infrared microspectroscopy analysis revealed that the ech and yip4a yip4b mutants exhibit changes in their cell wall composition. Overall, our results reveal a TGN subdomain defined by ECH/YIP4 that is required for the secretion of pectin and hemicellulose and distinguishes the role of the TGN in secretion from its roles in endocytic and vacuolar trafficking.},
	number = {7},
	urldate = {2021-06-21},
	journal = {The Plant Cell},
	author = {Gendre, Delphine and McFarlane, Heather E. and Johnson, Errin and Mouille, Gregory and Sjödin, Andreas and Oh, Jaesung and Levesque-Tremblay, Gabriel and Watanabe, Yoichiro and Samuels, Lacey and Bhalerao, Rishikesh P.},
	month = jul,
	year = {2013},
	pages = {2633--2646},
}

The secretion of cell wall polysaccharides through the trans-Golgi network (TGN) is required for plant cell elongation. However, the components mediating the post-Golgi secretion of pectin and hemicellulose, the two major cell wall polysaccharides, are largely unknown. We identified evolutionarily conserved YPT/RAB GTPase Interacting Protein 4a (YIP4a) and YIP4b (formerly YIP2), which form a TGN-localized complex with ECHIDNA (ECH) in Arabidopsis thaliana. The localization of YIP4 and ECH proteins at the TGN is interdependent and influences the localization of VHA-a1 and SYP61, which are key components of the TGN. YIP4a and YIP4b act redundantly, and the yip4a yip4b double mutants have a cell elongation defect. Genetic, biochemical, and cell biological analyses demonstrate that the ECH/YIP4 complex plays a key role in TGN-mediated secretion of pectin and hemicellulose to the cell wall in dark-grown hypocotyls and in secretory cells of the seed coat. In keeping with these observations, Fourier transform infrared microspectroscopy analysis revealed that the ech and yip4a yip4b mutants exhibit changes in their cell wall composition. Overall, our results reveal a TGN subdomain defined by ECH/YIP4 that is required for the secretion of pectin and hemicellulose and distinguishes the role of the TGN in secretion from its roles in endocytic and vacuolar trafficking.

@article{kaewthai_group_2012,
	title = {Group {III}-{A} \textit{{XTH}} {Genes} of {Arabidopsis} {Encode} {Predominant} {Xyloglucan} {Endohydrolases} {That} {Are} {Dispensable} for {Normal} {Growth}},
	volume = {161},
	issn = {1532-2548},
	url = {https://academic.oup.com/plphys/article/161/1/440/6110726},
	doi = {10/f24f58},
	abstract = {Abstract
            The molecular basis of primary wall extension endures as one of the central enigmas in plant cell morphogenesis. Classical cell wall models suggest that xyloglucan endo-transglycosylase activity is the primary catalyst (together with expansins) of controlled cell wall loosening through the transient cleavage and religation of xyloglucan-cellulose cross links. The genome of Arabidopsis (Arabidopsis thaliana) contains 33 phylogenetically diverse XYLOGLUCAN ENDO-TRANSGLYCOSYLASE/HYDROLASE (XTH) gene products, two of which were predicted to be predominant xyloglucan endohydrolases due to clustering into group III-A. Enzyme kinetic analysis of recombinant AtXTH31 confirmed this prediction and indicated that this enzyme had similar catalytic properties to the nasturtium (Tropaeolum majus) xyloglucanase1 responsible for storage xyloglucan hydrolysis during germination. Global analysis of Genevestigator data indicated that AtXTH31 and the paralogous AtXTH32 were abundantly expressed in expanding tissues. Microscopy analysis, utilizing the resorufin β-glycoside of the xyloglucan oligosaccharide XXXG as an in situ probe, indicated significant xyloglucan endohydrolase activity in specific regions of both roots and hypocotyls, in good correlation with transcriptomic data. Moreover, this hydrolytic activity was essentially completely eliminated in AtXTH31/AtXTH32 double knockout lines. However, single and double knockout lines, as well as individual overexpressing lines, of AtXTH31 and AtXTH32 did not demonstrate significant growth or developmental phenotypes. These results suggest that although xyloglucan polysaccharide hydrolysis occurs in parallel with primary wall expansion, morphological effects are subtle or may be compensated by other mechanisms. We hypothesize that there is likely to be an interplay between these xyloglucan endohydrolases and recently discovered apoplastic exo-glycosidases in the hydrolytic modification of matrix xyloglucans.},
	language = {en},
	number = {1},
	urldate = {2021-06-08},
	journal = {Plant Physiology},
	author = {Kaewthai, Nomchit and Gendre, Delphine and Eklöf, Jens M. and Ibatullin, Farid M. and Ezcurra, Ines and Bhalerao, Rishikesh P. and Brumer, Harry},
	month = dec,
	year = {2012},
	pages = {440--454},
}

Abstract The molecular basis of primary wall extension endures as one of the central enigmas in plant cell morphogenesis. Classical cell wall models suggest that xyloglucan endo-transglycosylase activity is the primary catalyst (together with expansins) of controlled cell wall loosening through the transient cleavage and religation of xyloglucan-cellulose cross links. The genome of Arabidopsis (Arabidopsis thaliana) contains 33 phylogenetically diverse XYLOGLUCAN ENDO-TRANSGLYCOSYLASE/HYDROLASE (XTH) gene products, two of which were predicted to be predominant xyloglucan endohydrolases due to clustering into group III-A. Enzyme kinetic analysis of recombinant AtXTH31 confirmed this prediction and indicated that this enzyme had similar catalytic properties to the nasturtium (Tropaeolum majus) xyloglucanase1 responsible for storage xyloglucan hydrolysis during germination. Global analysis of Genevestigator data indicated that AtXTH31 and the paralogous AtXTH32 were abundantly expressed in expanding tissues. Microscopy analysis, utilizing the resorufin β-glycoside of the xyloglucan oligosaccharide XXXG as an in situ probe, indicated significant xyloglucan endohydrolase activity in specific regions of both roots and hypocotyls, in good correlation with transcriptomic data. Moreover, this hydrolytic activity was essentially completely eliminated in AtXTH31/AtXTH32 double knockout lines. However, single and double knockout lines, as well as individual overexpressing lines, of AtXTH31 and AtXTH32 did not demonstrate significant growth or developmental phenotypes. These results suggest that although xyloglucan polysaccharide hydrolysis occurs in parallel with primary wall expansion, morphological effects are subtle or may be compensated by other mechanisms. We hypothesize that there is likely to be an interplay between these xyloglucan endohydrolases and recently discovered apoplastic exo-glycosidases in the hydrolytic modification of matrix xyloglucans.

@article{rigal_aintegumenta_2012,
	title = {The {AINTEGUMENTA} {LIKE1} homeotic transcription factor {PtAIL1} controls the formation of adventitious root primordia in poplar},
	volume = {160},
	issn = {1532-2548},
	doi = {10/f2ztb6},
	abstract = {Adventitious rooting is an essential but sometimes rate-limiting step in the clonal multiplication of elite tree germplasm, because the ability to form roots declines rapidly with age in mature adult plant tissues. In spite of the importance of adventitious rooting, the mechanism behind this developmental process remains poorly understood. We have described the transcriptional profiles that are associated with the developmental stages of adventitious root formation in the model tree poplar (Populus trichocarpa). Transcriptome analyses indicate a highly specific temporal induction of the AINTEGUMENTA LIKE1 (PtAIL1) transcription factor of the AP2 family during adventitious root formation. Transgenic poplar samples that overexpressed PtAIL1 were able to grow an increased number of adventitious roots, whereas RNA interference mediated the down-expression of PtAIL1 expression, which led to a delay in adventitious root formation. Microarray analysis showed that the expression of 15 genes, including the transcription factors AGAMOUS-Like6 and MYB36, was overexpressed in the stem tissues that generated root primordia in PtAIL1-overexpressing plants, whereas their expression was reduced in the RNA interference lines. These results demonstrate that PtAIL1 is a positive regulator of poplar rooting that acts early in the development of adventitious roots.},
	language = {eng},
	number = {4},
	journal = {Plant Physiology},
	author = {Rigal, Adeline and Yordanov, Yordan S. and Perrone, Irene and Karlberg, Anna and Tisserant, Emilie and Bellini, Catherine and Busov, Victor B. and Martin, Francis and Kohler, Annegret and Bhalerao, Rishikesh P. and Legué, Valérie},
	month = dec,
	year = {2012},
	pmid = {23077242},
	pmcid = {PMC3510126},
	keywords = {Gene Expression Regulation, Developmental, Gene Expression Regulation, Plant, Genes, Homeobox, Plant Proteins, Plant Roots, Plants, Genetically Modified, Populus, RNA Interference, RNA, Messenger, Transcription Factors, Transcriptome},
	pages = {1996--2006},
}

Adventitious rooting is an essential but sometimes rate-limiting step in the clonal multiplication of elite tree germplasm, because the ability to form roots declines rapidly with age in mature adult plant tissues. In spite of the importance of adventitious rooting, the mechanism behind this developmental process remains poorly understood. We have described the transcriptional profiles that are associated with the developmental stages of adventitious root formation in the model tree poplar (Populus trichocarpa). Transcriptome analyses indicate a highly specific temporal induction of the AINTEGUMENTA LIKE1 (PtAIL1) transcription factor of the AP2 family during adventitious root formation. Transgenic poplar samples that overexpressed PtAIL1 were able to grow an increased number of adventitious roots, whereas RNA interference mediated the down-expression of PtAIL1 expression, which led to a delay in adventitious root formation. Microarray analysis showed that the expression of 15 genes, including the transcription factors AGAMOUS-Like6 and MYB36, was overexpressed in the stem tissues that generated root primordia in PtAIL1-overexpressing plants, whereas their expression was reduced in the RNA interference lines. These results demonstrate that PtAIL1 is a positive regulator of poplar rooting that acts early in the development of adventitious roots.

@article{baba_activity-dormancy_2011,
	title = {Activity-dormancy transition in the cambial meristem involves stage-specific modulation of auxin response in hybrid aspen},
	volume = {108},
	issn = {0027-8424, 1091-6490},
	url = {http://www.pnas.org/cgi/doi/10.1073/pnas.1011506108},
	doi = {10/d34mx2},
	language = {en},
	number = {8},
	urldate = {2021-06-08},
	journal = {Proceedings of the National Academy of Sciences},
	author = {Baba, K. and Karlberg, A. and Schmidt, J. and Schrader, J. and Hvidsten, T. R. and Bakó, L. and Bhalerao, Rishikesh P.},
	month = feb,
	year = {2011},
	pages = {3418--3423},
}

@article{gendre_conserved_2011,
	title = {Conserved {Arabidopsis} {ECHIDNA} protein mediates trans-{Golgi}-network trafficking and cell elongation},
	volume = {108},
	issn = {0027-8424, 1091-6490},
	url = {http://www.pnas.org/cgi/doi/10.1073/pnas.1018371108},
	doi = {10/b6k65m},
	language = {en},
	number = {19},
	urldate = {2021-06-08},
	journal = {Proceedings of the National Academy of Sciences},
	author = {Gendre, D. and Oh, J. and Boutte, Y. and Best, J. G. and Samuels, L. and Nilsson, R. and Uemura, T. and Marchant, A. and Bennett, M. J. and Grebe, M. and Bhalerao, Rishikesh P.},
	month = may,
	year = {2011},
	pages = {8048--8053},
}

@article{karlberg_short_2011,
	title = {Short {Day}–{Mediated} {Cessation} of {Growth} {Requires} the {Downregulation} of {AINTEGUMENTALIKE1} {Transcription} {Factor} in {Hybrid} {Aspen}},
	volume = {7},
	issn = {1553-7404},
	url = {https://dx.plos.org/10.1371/journal.pgen.1002361},
	doi = {10/dx44wg},
	language = {en},
	number = {11},
	urldate = {2021-06-08},
	journal = {PLoS Genetics},
	author = {Karlberg, Anna and Bakó, Laszlo and Bhalerao, Rishikesh P.},
	editor = {Sederoff, Ronald R.},
	month = nov,
	year = {2011},
	pages = {e1002361},
}

@article{karlberg_analysis_2010,
	title = {Analysis of global changes in gene expression during activity-dormancy cycle in hybrid aspen apex},
	volume = {27},
	doi = {10/frkc7v},
	abstract = {Perennial plants such as the long-lived trees of boreal forest cycle between periods of active growth and dormancy. Transition from active growth to dormancy is induced by short day (SD) signal. Once dormancy is established, prolonged exposure to low temperature is required for breaking dormancy before warm temperatures can induce growth. We have studied global changes in gene expression in the apex of model plant hybrid aspen during the distinct stages of activity-dormancy cycle. Our data shows that all stages of activity-dormancy cycle in the apex are associated with substantial modulation of the transcriptome. Detailed analysis of core cell cycle genes indicates that with the exception of plant specific B-type CDKs, all of the other CDKs are regulated post-transcriptionally during growth cessation. SD signal appears to target the expression of cyclin genes that are down regulated during growth arrest. Several of the cold hardiness related genes e. g. dehydrins are induced during transition to dormancy although temperature is not reduced and the up-regulation of the expression of these genes does not appear to rely on SD mediated induction of classical CBF transcription factors. Our results suggest that transcriptional control plays a key role in modulation of hormones such as ABA and GA that are known to play a central role in various processes during activity-dormancy cycle. Analysis of histone and DNA modification genes indicates that chromatin remodeling could be involved in coordinating global changes in gene expression during activity-dormancy cycle.},
	number = {1},
	journal = {Plant Biotechnology},
	author = {Karlberg, Anna and Englund, Madeleine and Petterle, Anna and Molnar, Gergely and Sjödin, Andreas and Bakó, Laszlo and Bhalerao, Rishikesh P.},
	year = {2010},
	keywords = {Cell cycle, dormancy, hormone, microarray, poplar},
	pages = {1--16},
}

Perennial plants such as the long-lived trees of boreal forest cycle between periods of active growth and dormancy. Transition from active growth to dormancy is induced by short day (SD) signal. Once dormancy is established, prolonged exposure to low temperature is required for breaking dormancy before warm temperatures can induce growth. We have studied global changes in gene expression in the apex of model plant hybrid aspen during the distinct stages of activity-dormancy cycle. Our data shows that all stages of activity-dormancy cycle in the apex are associated with substantial modulation of the transcriptome. Detailed analysis of core cell cycle genes indicates that with the exception of plant specific B-type CDKs, all of the other CDKs are regulated post-transcriptionally during growth cessation. SD signal appears to target the expression of cyclin genes that are down regulated during growth arrest. Several of the cold hardiness related genes e. g. dehydrins are induced during transition to dormancy although temperature is not reduced and the up-regulation of the expression of these genes does not appear to rely on SD mediated induction of classical CBF transcription factors. Our results suggest that transcriptional control plays a key role in modulation of hormones such as ABA and GA that are known to play a central role in various processes during activity-dormancy cycle. Analysis of histone and DNA modification genes indicates that chromatin remodeling could be involved in coordinating global changes in gene expression during activity-dormancy cycle.

@article{resman_components_2010,
	title = {Components {Acting} {Downstream} of {Short} {Day} {Perception} {Regulate} {Differential} {Cessation} of {Cambial} {Activity} and {Associated} {Responses} in {Early} and {Late} {Clones} of {Hybrid} {Poplar}},
	volume = {154},
	issn = {1532-2548},
	url = {https://academic.oup.com/plphys/article/154/3/1294/6111326},
	doi = {10/dhnvbh},
	abstract = {Abstract
            Short days (SDs) in autumn induce growth cessation, bud set, cold acclimation, and dormancy in trees of boreal and temperate forests, and these responses occur earlier in northern than in southern genotypes. Nevertheless, we know little about whether this variation results from differential perception of SDs or differential downstream responses to the SD signal or a combination of the two. We compared global patterns of SD-regulated gene expression in the stems of hybrid poplar (Populus trichocarpa × Populus deltoides) clones that differ in their SD-induced growth cessation in order to address this question. The timing of cessation of cambial cell division caused by SDs differed between the clones and was coincident with the change in the pattern of expression of the auxin-regulated genes. The clones also differed in the timing of their SD-regulated changes in the transcript abundance of genes associated with cold tolerance, starch breakdown, and storage protein accumulation. By analyzing the expression of homologs of FLOWERING LOCUS T, we demonstrated that the clones differed little in their perception of SDs under the growth conditions applied but differed substantially in the downstream responses manifested in the timing and magnitude of gene expression after SD treatment. These results demonstrate the existence of factors that act downstream of SD perception and can contribute to variation in SD-regulated adaptive photoperiodic responses in trees.},
	language = {en},
	number = {3},
	urldate = {2021-06-08},
	journal = {Plant Physiology},
	author = {Resman, Lars and Howe, Glenn and Jonsen, David and Englund, Madeleine and Druart, Nathalie and Schrader, Jarmo and Antti, Henrik and Skinner, Jeff and Sjödin, Andreas and Chen, Tony and Bhalerao, Rishikesh P.},
	month = nov,
	year = {2010},
	pages = {1294--1303},
}

Abstract Short days (SDs) in autumn induce growth cessation, bud set, cold acclimation, and dormancy in trees of boreal and temperate forests, and these responses occur earlier in northern than in southern genotypes. Nevertheless, we know little about whether this variation results from differential perception of SDs or differential downstream responses to the SD signal or a combination of the two. We compared global patterns of SD-regulated gene expression in the stems of hybrid poplar (Populus trichocarpa × Populus deltoides) clones that differ in their SD-induced growth cessation in order to address this question. The timing of cessation of cambial cell division caused by SDs differed between the clones and was coincident with the change in the pattern of expression of the auxin-regulated genes. The clones also differed in the timing of their SD-regulated changes in the transcript abundance of genes associated with cold tolerance, starch breakdown, and storage protein accumulation. By analyzing the expression of homologs of FLOWERING LOCUS T, we demonstrated that the clones differed little in their perception of SDs under the growth conditions applied but differed substantially in the downstream responses manifested in the timing and magnitude of gene expression after SD treatment. These results demonstrate the existence of factors that act downstream of SD perception and can contribute to variation in SD-regulated adaptive photoperiodic responses in trees.

@article{ubeda-tomas_gibberellin_2009,
	title = {Gibberellin {Signaling} in the {Endodermis} {Controls} {Arabidopsis} {Root} {Meristem} {Size}},
	volume = {19},
	issn = {09609822},
	url = {https://linkinghub.elsevier.com/retrieve/pii/S0960982209012962},
	doi = {10/dfm6hq},
	language = {en},
	number = {14},
	urldate = {2021-06-08},
	journal = {Current Biology},
	author = {Ubeda-Tomás, Susana and Federici, Fernán and Casimiro, Ilda and Beemster, Gerrit T.S. and Bhalerao, Rishikesh P. and Swarup, Ranjan and Doerner, Peter and Haseloff, Jim and Bennett, Malcolm J.},
	month = jul,
	year = {2009},
	pages = {1194--1199},
}

@article{gronlund_modular_2009,
	title = {Modular gene expression in {Poplar}: a multilayer network approach},
	volume = {181},
	issn = {0028-646X, 1469-8137},
	shorttitle = {Modular gene expression in {Poplar}},
	url = {https://onlinelibrary.wiley.com/doi/10.1111/j.1469-8137.2008.02668.x},
	doi = {10/fm5ggr},
	language = {en},
	number = {2},
	urldate = {2021-06-10},
	journal = {New Phytologist},
	author = {Grönlund, Andreas and Bhalerao, Rishikesh P. and Karlsson, Jan},
	month = jan,
	year = {2009},
	pages = {315--322},
}

@article{felten_ectomycorrhizal_2009,
	title = {The {Ectomycorrhizal} {Fungus} \textit{{Laccaria} bicolor} {Stimulates} {Lateral} {Root} {Formation} in {Poplar} and {Arabidopsis} through {Auxin} {Transport} and {Signaling}},
	volume = {151},
	issn = {1532-2548},
	url = {https://academic.oup.com/plphys/article/151/4/1991/6109870},
	doi = {10/dsjkhv},
	abstract = {Abstract
            The early phase of the interaction between tree roots and ectomycorrhizal fungi, prior to symbiosis establishment, is accompanied by a stimulation of lateral root (LR) development. We aimed to identify gene networks that regulate LR development during the early signal exchanges between poplar (Populus tremula × Populus alba) and the ectomycorrhizal fungus Laccaria bicolor with a focus on auxin transport and signaling pathways. Our data demonstrated that increased LR development in poplar and Arabidopsis (Arabidopsis thaliana) interacting with L. bicolor is not dependent on the ability of the plant to form ectomycorrhizae. LR stimulation paralleled an increase in auxin accumulation at root apices. Blocking plant polar auxin transport with 1-naphthylphthalamic acid inhibited LR development and auxin accumulation. An oligoarray-based transcript profile of poplar roots exposed to molecules released by L. bicolor revealed the differential expression of 2,945 genes, including several components of polar auxin transport (PtaPIN and PtaAUX genes), auxin conjugation (PtaGH3 genes), and auxin signaling (PtaIAA genes). Transcripts of PtaPIN9, the homolog of Arabidopsis AtPIN2, and several PtaIAAs accumulated specifically during the early interaction phase. Expression of these rapidly induced genes was repressed by 1-naphthylphthalamic acid. Accordingly, LR stimulation upon contact with L. bicolor in Arabidopsis transgenic plants defective in homologs of these genes was decreased or absent. Furthermore, in Arabidopsis pin2, the root apical auxin increase during contact with the fungus was modified. We propose a model in which fungus-induced auxin accumulation at the root apex stimulates LR formation through a mechanism involving PtaPIN9-dependent auxin redistribution together with PtaIAA-based auxin signaling.},
	language = {en},
	number = {4},
	urldate = {2021-06-08},
	journal = {Plant Physiology},
	author = {Felten, Judith and Kohler, Annegret and Morin, Emmanuelle and Bhalerao, Rishikesh P. and Palme, Klaus and Martin, Francis and Ditengou, Franck A. and Legué, Valérie},
	month = dec,
	year = {2009},
	pages = {1991--2005},
}

Abstract The early phase of the interaction between tree roots and ectomycorrhizal fungi, prior to symbiosis establishment, is accompanied by a stimulation of lateral root (LR) development. We aimed to identify gene networks that regulate LR development during the early signal exchanges between poplar (Populus tremula × Populus alba) and the ectomycorrhizal fungus Laccaria bicolor with a focus on auxin transport and signaling pathways. Our data demonstrated that increased LR development in poplar and Arabidopsis (Arabidopsis thaliana) interacting with L. bicolor is not dependent on the ability of the plant to form ectomycorrhizae. LR stimulation paralleled an increase in auxin accumulation at root apices. Blocking plant polar auxin transport with 1-naphthylphthalamic acid inhibited LR development and auxin accumulation. An oligoarray-based transcript profile of poplar roots exposed to molecules released by L. bicolor revealed the differential expression of 2,945 genes, including several components of polar auxin transport (PtaPIN and PtaAUX genes), auxin conjugation (PtaGH3 genes), and auxin signaling (PtaIAA genes). Transcripts of PtaPIN9, the homolog of Arabidopsis AtPIN2, and several PtaIAAs accumulated specifically during the early interaction phase. Expression of these rapidly induced genes was repressed by 1-naphthylphthalamic acid. Accordingly, LR stimulation upon contact with L. bicolor in Arabidopsis transgenic plants defective in homologs of these genes was decreased or absent. Furthermore, in Arabidopsis pin2, the root apical auxin increase during contact with the fungus was modified. We propose a model in which fungus-induced auxin accumulation at the root apex stimulates LR formation through a mechanism involving PtaPIN9-dependent auxin redistribution together with PtaIAA-based auxin signaling.

@article{nieminen_cytokinin_2008,
	title = {Cytokinin signaling regulates cambial development in poplar},
	volume = {105},
	issn = {0027-8424, 1091-6490},
	url = {http://www.pnas.org/cgi/doi/10.1073/pnas.0805617106},
	doi = {10/cv6jmj},
	language = {en},
	number = {50},
	urldate = {2021-06-10},
	journal = {Proceedings of the National Academy of Sciences},
	author = {Nieminen, K. and Immanen, J. and Laxell, M. and Kauppinen, L. and Tarkowski, P. and Dolezal, K. and Tahtiharju, S. and Elo, A. and Decourteix, M. and Ljung, K. and Bhalerao, Rishikesh P. and Keinonen, K. and Albert, V. A. and Helariutta, Y.},
	month = dec,
	year = {2008},
	pages = {20032--20037},
}

@article{nilsson_dissecting_2008,
	title = {Dissecting the {Molecular} {Basis} of the {Regulation} of {Wood} {Formation} by {Auxin} in {Hybrid} {Aspen}},
	volume = {20},
	issn = {1532-298X},
	url = {https://academic.oup.com/plcell/article/20/4/843/6092327},
	doi = {10/c7bg45},
	abstract = {Abstract
            Indole acetic acid (auxin) is a key regulator of wood formation, and an observed overlap between auxin concentration gradient and developing secondary xylem cells has led to the hypothesis that auxin regulates wood formation by acting as a morphogen. We dissected the role of auxin in wood formation by identifying the auxin-responsive transcriptome in wood-forming tissues and investigating alterations in wood formation in transgenic hybrid aspen plants (Populus tremula × Populus tremuloides) with perturbed auxin signaling. We showed that auxin-responsive genes in wood-forming tissues respond dynamically to changes in cellular auxin levels. However, the expression patterns of most of the auxin-responsive genes displayed limited correlation with the auxin concentration across this developmental zone. Perturbing auxin signaling by reducing auxin responsiveness reduced the cambial cell division activity, caused spatial deregulation of cell division of the cambial initials, and led to reductions in not only radial but also axial dimensions of fibers and vessels. We propose that, instead of acting as a morphogen, changes in auxin concentration in developing secondary xylem cells may provide important regulatory cues that modulate the expression of a few key regulators; these, in turn, may control the global gene expression patterns that are essential for normal secondary xylem development.},
	language = {en},
	number = {4},
	urldate = {2021-06-10},
	journal = {The Plant Cell},
	author = {Nilsson, Jeanette and Karlberg, Anna and Antti, Henrik and Lopez-Vernaza, Manuel and Mellerowicz, Ewa and Perrot-Rechenmann, Catherine and Sandberg, Göran and Bhalerao, Rishikesh P.},
	month = may,
	year = {2008},
	pages = {843--855},
}

Abstract Indole acetic acid (auxin) is a key regulator of wood formation, and an observed overlap between auxin concentration gradient and developing secondary xylem cells has led to the hypothesis that auxin regulates wood formation by acting as a morphogen. We dissected the role of auxin in wood formation by identifying the auxin-responsive transcriptome in wood-forming tissues and investigating alterations in wood formation in transgenic hybrid aspen plants (Populus tremula × Populus tremuloides) with perturbed auxin signaling. We showed that auxin-responsive genes in wood-forming tissues respond dynamically to changes in cellular auxin levels. However, the expression patterns of most of the auxin-responsive genes displayed limited correlation with the auxin concentration across this developmental zone. Perturbing auxin signaling by reducing auxin responsiveness reduced the cambial cell division activity, caused spatial deregulation of cell division of the cambial initials, and led to reductions in not only radial but also axial dimensions of fibers and vessels. We propose that, instead of acting as a morphogen, changes in auxin concentration in developing secondary xylem cells may provide important regulatory cues that modulate the expression of a few key regulators; these, in turn, may control the global gene expression patterns that are essential for normal secondary xylem development.

@article{ubeda-tomas_root_2008,
	title = {Root growth in {Arabidopsis} requires gibberellin/{DELLA} signalling in the endodermis},
	volume = {10},
	issn = {1465-7392, 1476-4679},
	url = {http://www.nature.com/articles/ncb1726},
	doi = {10/fj897f},
	language = {en},
	number = {5},
	urldate = {2021-06-10},
	journal = {Nature Cell Biology},
	author = {Ubeda-Tomás, Susana and Swarup, Ranjan and Coates, Juliet and Swarup, Kamal and Laplaze, Laurent and Beemster, Gerrit T.S. and Hedden, Peter and Bhalerao, Rishikesh P. and Bennett, Malcolm J.},
	month = may,
	year = {2008},
	pages = {625--628},
}

@article{ruttink_molecular_2007,
	title = {A {Molecular} {Timetable} for {Apical} {Bud} {Formation} and {Dormancy} {Induction} in {Poplar}},
	volume = {19},
	issn = {1532-298X},
	url = {https://academic.oup.com/plcell/article/19/8/2370/6088927},
	doi = {10/bcfnqh},
	abstract = {Abstract
            The growth of perennial plants in the temperate zone alternates with periods of dormancy that are typically initiated during bud development in autumn. In a systems biology approach to unravel the underlying molecular program of apical bud development in poplar (Populus tremula × Populus alba), combined transcript and metabolite profiling were applied to a high-resolution time course from short-day induction to complete dormancy. Metabolite and gene expression dynamics were used to reconstruct the temporal sequence of events during bud development. Importantly, bud development could be dissected into bud formation, acclimation to dehydration and cold, and dormancy. To each of these processes, specific sets of regulatory and marker genes and metabolites are associated and provide a reference frame for future functional studies. Light, ethylene, and abscisic acid signal transduction pathways consecutively control bud development by setting, modifying, or terminating these processes. Ethylene signal transduction is positioned temporally between light and abscisic acid signals and is putatively activated by transiently low hexose pools. The timing and place of cell proliferation arrest (related to dormancy) and of the accumulation of storage compounds (related to acclimation processes) were established within the bud by electron microscopy. Finally, the identification of a large set of genes commonly expressed during the growth-to-dormancy transitions in poplar apical buds, cambium, or Arabidopsis thaliana seeds suggests parallels in the underlying molecular mechanisms in different plant organs.},
	language = {en},
	number = {8},
	urldate = {2021-06-10},
	journal = {The Plant Cell},
	author = {Ruttink, Tom and Arend, Matthias and Morreel, Kris and Storme, Véronique and Rombauts, Stephane and Fromm, Jörg and Bhalerao, Rishikesh P. and Boerjan, Wout and Rohde, Antje},
	month = oct,
	year = {2007},
	pages = {2370--2390},
}

Abstract The growth of perennial plants in the temperate zone alternates with periods of dormancy that are typically initiated during bud development in autumn. In a systems biology approach to unravel the underlying molecular program of apical bud development in poplar (Populus tremula × Populus alba), combined transcript and metabolite profiling were applied to a high-resolution time course from short-day induction to complete dormancy. Metabolite and gene expression dynamics were used to reconstruct the temporal sequence of events during bud development. Importantly, bud development could be dissected into bud formation, acclimation to dehydration and cold, and dormancy. To each of these processes, specific sets of regulatory and marker genes and metabolites are associated and provide a reference frame for future functional studies. Light, ethylene, and abscisic acid signal transduction pathways consecutively control bud development by setting, modifying, or terminating these processes. Ethylene signal transduction is positioned temporally between light and abscisic acid signals and is putatively activated by transiently low hexose pools. The timing and place of cell proliferation arrest (related to dormancy) and of the accumulation of storage compounds (related to acclimation processes) were established within the bud by electron microscopy. Finally, the identification of a large set of genes commonly expressed during the growth-to-dormancy transitions in poplar apical buds, cambium, or Arabidopsis thaliana seeds suggests parallels in the underlying molecular mechanisms in different plant organs.

@article{druart_environmental_2007,
	title = {Environmental and hormonal regulation of the activity-dormancy cycle in the cambial meristem involves stage-specific modulation of transcriptional and metabolic networks: {Molecular} analysis of cambial activity-dormancy cycle},
	volume = {50},
	issn = {09607412, 1365313X},
	shorttitle = {Environmental and hormonal regulation of the activity-dormancy cycle in the cambial meristem involves stage-specific modulation of transcriptional and metabolic networks},
	url = {http://doi.wiley.com/10.1111/j.1365-313X.2007.03077.x},
	doi = {10/cgt589},
	language = {en},
	number = {4},
	urldate = {2021-06-10},
	journal = {The Plant Journal},
	author = {Druart, Nathalie and Johansson, Annika and Baba, Kyoko and Schrader, Jarmo and Sjödin, Andreas and Bhalerao, Rupali R. and Resman, Lars and Trygg, Johan and Moritz, Thomas and Bhalerao, Rishikesh P.},
	month = apr,
	year = {2007},
	pages = {557--573},
}

@article{swarup_ethylene_2007,
	title = {Ethylene {Upregulates} {Auxin} {Biosynthesis} in \textit{{Arabidopsis}} {Seedlings} to {Enhance} {Inhibition} of {Root} {Cell} {Elongation}},
	volume = {19},
	issn = {1532-298X},
	url = {https://academic.oup.com/plcell/article/19/7/2186/6092109},
	doi = {10/cd3mq3},
	abstract = {Abstract
            Ethylene represents an important regulatory signal for root development. Genetic studies in Arabidopsis thaliana have demonstrated that ethylene inhibition of root growth involves another hormone signal, auxin. This study investigated why auxin was required by ethylene to regulate root growth. We initially observed that ethylene positively controls auxin biosynthesis in the root apex. We subsequently demonstrated that ethylene-regulated root growth is dependent on (1) the transport of auxin from the root apex via the lateral root cap and (2) auxin responses occurring in multiple elongation zone tissues. Detailed growth studies revealed that the ability of the ethylene precursor 1-aminocyclopropane-1-carboxylic acid to inhibit root cell elongation was significantly enhanced in the presence of auxin. We conclude that by upregulating auxin biosynthesis, ethylene facilitates its ability to inhibit root cell expansion.},
	language = {en},
	number = {7},
	urldate = {2021-06-10},
	journal = {The Plant Cell},
	author = {Swarup, Ranjan and Perry, Paula and Hagenbeek, Dik and Van Der Straeten, Dominique and Beemster, Gerrit T.S. and Sandberg, Göran and Bhalerao, Rishikesh P. and Ljung, Karin and Bennett, Malcolm J.},
	month = aug,
	year = {2007},
	pages = {2186--2196},
}

Abstract Ethylene represents an important regulatory signal for root development. Genetic studies in Arabidopsis thaliana have demonstrated that ethylene inhibition of root growth involves another hormone signal, auxin. This study investigated why auxin was required by ethylene to regulate root growth. We initially observed that ethylene positively controls auxin biosynthesis in the root apex. We subsequently demonstrated that ethylene-regulated root growth is dependent on (1) the transport of auxin from the root apex via the lateral root cap and (2) auxin responses occurring in multiple elongation zone tissues. Detailed growth studies revealed that the ability of the ethylene precursor 1-aminocyclopropane-1-carboxylic acid to inhibit root cell elongation was significantly enhanced in the presence of auxin. We conclude that by upregulating auxin biosynthesis, ethylene facilitates its ability to inhibit root cell expansion.

@article{druart_molecular_2006,
	title = {Molecular targets of elevated [{CO2}] in leaves and stems of {Populus} deltoides: implications for future tree growth and carbon sequestration},
	volume = {33},
	issn = {1445-4408},
	shorttitle = {Molecular targets of elevated [{CO2}] in leaves and stems of {Populus} deltoides},
	doi = {10.1071/FP05139},
	abstract = {We report the first comprehensive analysis of the effects of elevated [CO2] on gene expression in source leaf and stem sink tissues in woody plants. We have taken advantage of coppiced Populus deltoides (Bartr.) stands grown for 3 years under three different and constant elevated [CO2] in the agriforest mesocosms of Biosphere 2. Leaf area per tree was doubled by elevated [CO2] but although growth at 800 v. 400 mu mol mol(-1) CO2 resulted in a significant increase in stem biomass, growth was not stimulated at 1200 mu mol mol(-1) CO2. Growth under elevated [CO2] also resulted in significant increases in stem wood density. Analysis of expression data for the 13 490 clones present on POP1 microarrays revealed 95 and 277 [CO2]-responsive clones in leaves and stems respectively, with the response being stronger at 1200 mu mol mol(-1). When these [CO2]-responsive genes were assigned to functional categories, metabolism- related genes were the most responsive to elevated [CO2]. However within this category, expression of genes relating to bioenergetic processes was unchanged in leaves whereas the expression of genes for storage proteins and of those involved in control of wall expansion was enhanced. In contrast to leaves, the genes up-regulated in stems under elevated [CO2] were primarily enzymes responsible for lignin formation and polymerisation or ethylene response factors, also known to induce lignin biosynthesis. Concomitant with this enhancement of lignin biosynthesis in stems, there was a pronounced repression of genes related to cell wall formation and cell growth. These changes in gene expression have clear consequences for long-term carbon sequestration, reducing the carbon-fertilisation effect, and the potential for increased lignification may negatively impact on future wood quality for timber and paper production.},
	language = {English},
	number = {2},
	journal = {Functional Plant Biology},
	author = {Druart, N. and Rodriguez-Buey, M. and Barron-Gafford, G. and Sjodin, A. and Bhalerao, Rishikesh P. and Hurry, V.},
	year = {2006},
	note = {Place: Clayton
Publisher: Csiro Publishing
WOS:000235065100002},
	keywords = {Populus, atmospheric co2, betula-pendula roth, cdna microarray, cell-wall protein, cottonwood, deciduous   forest, elevated CO2, enrichment popface, global change, leaf growth, microarray, pinus-sylvestris, plant-growth, wood   properties},
	pages = {121--131},
}

We report the first comprehensive analysis of the effects of elevated [CO2] on gene expression in source leaf and stem sink tissues in woody plants. We have taken advantage of coppiced Populus deltoides (Bartr.) stands grown for 3 years under three different and constant elevated [CO2] in the agriforest mesocosms of Biosphere 2. Leaf area per tree was doubled by elevated [CO2] but although growth at 800 v. 400 mu mol mol(-1) CO2 resulted in a significant increase in stem biomass, growth was not stimulated at 1200 mu mol mol(-1) CO2. Growth under elevated [CO2] also resulted in significant increases in stem wood density. Analysis of expression data for the 13 490 clones present on POP1 microarrays revealed 95 and 277 [CO2]-responsive clones in leaves and stems respectively, with the response being stronger at 1200 mu mol mol(-1). When these [CO2]-responsive genes were assigned to functional categories, metabolism- related genes were the most responsive to elevated [CO2]. However within this category, expression of genes relating to bioenergetic processes was unchanged in leaves whereas the expression of genes for storage proteins and of those involved in control of wall expansion was enhanced. In contrast to leaves, the genes up-regulated in stems under elevated [CO2] were primarily enzymes responsible for lignin formation and polymerisation or ethylene response factors, also known to induce lignin biosynthesis. Concomitant with this enhancement of lignin biosynthesis in stems, there was a pronounced repression of genes related to cell wall formation and cell growth. These changes in gene expression have clear consequences for long-term carbon sequestration, reducing the carbon-fertilisation effect, and the potential for increased lignification may negatively impact on future wood quality for timber and paper production.

@article{benedict_cbf1-dependent_2006,
	title = {The {CBF1}-dependent low temperature signalling pathway, regulon and increase in freeze tolerance are conserved in {Populus} spp.},
	volume = {29},
	issn = {0140-7791},
	doi = {10.1111/j.1365-3040.2006.01505.x},
	abstract = {The meristematic tissues of temperate woody perennials must acclimate to freezing temperatures to survive the winter and resume growth the following year. To determine whether the C-repeat binding factor (CBF) family of transcription factors contributing to this process in annual herbaceous species also functions in woody perennials, we investigated the changes in phenotype and transcript profile of transgenic Populus constitutively expressing CBF1 from Arabidopsis (AtCBF1). Ectopic expression of AtCBF1 was sufficient to significantly increase the freezing tolerance of non-acclimated leaves and stems relative to wild-type plants. cDNA microarray experiments identified genes up-regulated by ectopic AtCBF1 expression in Populus, demonstrated a strong conservation of the CBF regulon between Populus and Arabidopsis and identified differences between leaf and stem regulons. We studied the induction kinetics and tissue specificity of four CBF paralogues identified from the Populus balsamifera subsp. trichocarpa genome sequence (PtCBFs). All four PtCBFs are cold-inducible in leaves, but only PtCBF1 and PtCBF3 show significant induction in stems. Our results suggest that the central role played by the CBF family of transcriptional activators in cold acclimation of Arabidopsis has been maintained in Populus. However, the differential expression of the PtCBFs and differing clusters of CBF-responsive genes in annual (leaf) and perennial (stem) tissues suggest that the perennial-driven evolution of winter dormancy may have given rise to specific roles for these 'master-switches' in the different annual and perennial tissues of woody species.},
	language = {English},
	number = {7},
	journal = {Plant Cell and Environment},
	author = {Benedict, Catherine and Skinner, Jeffrey S. and Meng, Rengong and Chang, Yongjian and Bhalerao, Rishikesh P. and Huner, Norman P. A. and Finn, Chad E. and Chen, Tony H. H. and Hurry, Vaughan},
	month = jul,
	year = {2006},
	note = {Place: Hoboken
Publisher: Wiley
WOS:000238064400006},
	keywords = {abscisic-acid, arabidopsis-thaliana, birch betula-pendula, cold tolerance, cold-response pathway, induced gene-expression, microarray, peach prunus-persica, seasonal-changes, short photoperiod, silver birch, transcription factors},
	pages = {1259--1272},
}

The meristematic tissues of temperate woody perennials must acclimate to freezing temperatures to survive the winter and resume growth the following year. To determine whether the C-repeat binding factor (CBF) family of transcription factors contributing to this process in annual herbaceous species also functions in woody perennials, we investigated the changes in phenotype and transcript profile of transgenic Populus constitutively expressing CBF1 from Arabidopsis (AtCBF1). Ectopic expression of AtCBF1 was sufficient to significantly increase the freezing tolerance of non-acclimated leaves and stems relative to wild-type plants. cDNA microarray experiments identified genes up-regulated by ectopic AtCBF1 expression in Populus, demonstrated a strong conservation of the CBF regulon between Populus and Arabidopsis and identified differences between leaf and stem regulons. We studied the induction kinetics and tissue specificity of four CBF paralogues identified from the Populus balsamifera subsp. trichocarpa genome sequence (PtCBFs). All four PtCBFs are cold-inducible in leaves, but only PtCBF1 and PtCBF3 show significant induction in stems. Our results suggest that the central role played by the CBF family of transcriptional activators in cold acclimation of Arabidopsis has been maintained in Populus. However, the differential expression of the PtCBFs and differing clusters of CBF-responsive genes in annual (leaf) and perennial (stem) tissues suggest that the perennial-driven evolution of winter dormancy may have given rise to specific roles for these 'master-switches' in the different annual and perennial tissues of woody species.

@article{tuskan_genome_2006,
	title = {The genome of black cottonwood, {Populus} trichocarpa ({Torr}. \& {Gray})},
	volume = {313},
	issn = {0036-8075},
	doi = {10/c7hs34},
	abstract = {We report the draft genome of the black cottonwood tree, Populus trichocarpa. Integration of shotgun sequence assembly with genetic mapping enabled chromosome-scale reconstruction of the genome. More than 45,000 putative protein-coding genes were identified. Analysis of the assembled genome revealed a whole-genome duplication event; about 8000 pairs of duplicated genes from that event survived in the Populus genome. A second, older duplication event is indistinguishably coincident with the divergence of the Populus and Arabidopsis lineages. Nucleotide substitution, tandem gene duplication, and gross chromosomal rearrangement appear to proceed substantially more slowly in Populus than in Arabidopsis. Populus has more protein-coding genes than Arabidopsis, ranging on average from 1.4 to 1.6 putative Populus homologs for each Arabidopsis gene. However, the relative frequency of protein domains in the two genomes is similar. Overrepresented exceptions in Populus include genes associated with lignocellulosic wall biosynthesis, meristem development, disease resistance, and metabolite transport.},
	language = {English},
	number = {5793},
	journal = {Science},
	author = {Tuskan, G. A. and DiFazio, S. and Jansson, S. and Bohlmann, J. and Grigoriev, I. and Hellsten, U. and Putnam, N. and Ralph, S. and Rombauts, S. and Salamov, A. and Schein, J. and Sterck, L. and Aerts, A. and Bhalerao, Rishikesh P. and Bhalerao, R. P. and Blaudez, D. and Boerjan, W. and Brun, A. and Brunner, A. and Busov, V. and Campbell, M. and Carlson, J. and Chalot, M. and Chapman, J. and Chen, G.-L. and Cooper, D. and Coutinho, P. M. and Couturier, J. and Covert, S. and Cronk, Q. and Cunningham, R. and Davis, J. and Degroeve, S. and Dejardin, A. and dePamphilis, C. and Detter, J. and Dirks, B. and Dubchak, I. and Duplessis, S. and Ehlting, J. and Ellis, B. and Gendler, K. and Goodstein, D. and Gribskov, M. and Grimwood, J. and Groover, A. and Gunter, L. and Hamberger, B. and Heinze, B. and Helariutta, Y. and Henrissat, B. and Holligan, D. and Holt, R. and Huang, W. and Islam-Faridi, N. and Jones, S. and Jones-Rhoades, M. and Jorgensen, R. and Joshi, C. and Kangasjarvi, J. and Karlsson, J. and Kelleher, C. and Kirkpatrick, R. and Kirst, M. and Kohler, A. and Kalluri, U. and Larimer, F. and Leebens-Mack, J. and Leple, J.-C. and Locascio, P. and Lou, Y. and Lucas, S. and Martin, F. and Montanini, B. and Napoli, C. and Nelson, D. R. and Nelson, C. and Nieminen, K. and Nilsson, O. and Pereda, V. and Peter, G. and Philippe, R. and Pilate, G. and Poliakov, A. and Razumovskaya, J. and Richardson, P. and Rinaldi, C. and Ritland, K. and Rouze, P. and Ryaboy, D. and Schmutz, J. and Schrader, J. and Segerman, B. and Shin, H. and Siddiqui, A. and Sterky, F. and Terry, A. and Tsai, C.-J. and Uberbacher, E. and Unneberg, P. and Vahala, J. and Wall, K. and Wessler, S. and Yang, G. and Yin, T. and Douglas, C. and Marra, M. and Sandberg, G. and Van de Peer, Y. and Rokhsar, D.},
	month = sep,
	year = {2006},
	note = {Place: Washington
Publisher: Amer Assoc Advancement Science
WOS:000240498900035},
	keywords = {arabidopsis-thaliana, cinnamyl alcohol-dehydrogenase, gene-expression, gravitational induction, hybrid poplar, lignin biosynthesis, phenylpropanoid metabolism, quaking   aspen, resistance genes, transcriptional regulators},
	pages = {1596--1604},
}

We report the draft genome of the black cottonwood tree, Populus trichocarpa. Integration of shotgun sequence assembly with genetic mapping enabled chromosome-scale reconstruction of the genome. More than 45,000 putative protein-coding genes were identified. Analysis of the assembled genome revealed a whole-genome duplication event; about 8000 pairs of duplicated genes from that event survived in the Populus genome. A second, older duplication event is indistinguishably coincident with the divergence of the Populus and Arabidopsis lineages. Nucleotide substitution, tandem gene duplication, and gross chromosomal rearrangement appear to proceed substantially more slowly in Populus than in Arabidopsis. Populus has more protein-coding genes than Arabidopsis, ranging on average from 1.4 to 1.6 putative Populus homologs for each Arabidopsis gene. However, the relative frequency of protein domains in the two genomes is similar. Overrepresented exceptions in Populus include genes associated with lignocellulosic wall biosynthesis, meristem development, disease resistance, and metabolite transport.

@article{wirta_assembly_2005,
	title = {Assembly of a gene sequence tag microarray by reversible biotin-streptavidin capture for transcript analysis of {Arabidopsis} thaliana},
	volume = {5},
	issn = {1472-6750},
	url = {https://doi.org/10.1186/1472-6750-5-5},
	doi = {10.1186/1472-6750-5-5},
	abstract = {Transcriptional profiling using microarrays has developed into a key molecular tool for the elucidation of gene function and gene regulation. Microarray platforms based on either oligonucleotides or purified amplification products have been utilised in parallel to produce large amounts of data. Irrespective of platform examined, the availability of genome sequence or a large number of representative expressed sequence tags (ESTs) is, however, a pre-requisite for the design and selection of specific and high-quality microarray probes. This is of great importance for organisms, such as Arabidopsis thaliana, with a high number of duplicated genes, as cross-hybridisation signals between evolutionary related genes cannot be distinguished from true signals unless the probes are carefully designed to be specific.},
	number = {1},
	urldate = {2021-06-11},
	journal = {BMC Biotechnology},
	author = {Wirta, Valtteri and Holmberg, Anders and Lukacs, Morten and Nilsson, Peter and Hilson, Pierre and Uhlén, Mathias and Bhalerao, Rishikesh P. and Lundeberg, Joakim},
	month = feb,
	year = {2005},
	keywords = {Additional Data File, Auxin Regulation, Auxin Transporter, Multiple Reuse, Photo Multiplier Tube},
	pages = {5},
}

Transcriptional profiling using microarrays has developed into a key molecular tool for the elucidation of gene function and gene regulation. Microarray platforms based on either oligonucleotides or purified amplification products have been utilised in parallel to produce large amounts of data. Irrespective of platform examined, the availability of genome sequence or a large number of representative expressed sequence tags (ESTs) is, however, a pre-requisite for the design and selection of specific and high-quality microarray probes. This is of great importance for organisms, such as Arabidopsis thaliana, with a high number of duplicated genes, as cross-hybridisation signals between evolutionary related genes cannot be distinguished from true signals unless the probes are carefully designed to be specific.

@article{swarup_root_2005,
	title = {Root gravitropism requires lateral root cap and epidermal cells for transport and response to a mobile auxin signal},
	volume = {7},
	copyright = {2005 Nature Publishing Group},
	issn = {1476-4679},
	url = {https://www.nature.com/articles/ncb1316},
	doi = {10.1038/ncb1316},
	abstract = {Re-orientation of Arabidopsis seedlings induces a rapid, asymmetric release of the growth regulator auxin from gravity-sensing columella cells at the root apex. The resulting lateral auxin gradient is hypothesized to drive differential cell expansion in elongation-zone tissues. We mapped those root tissues that function to transport or respond to auxin during a gravitropic response. Targeted expression of the auxin influx facilitator AUX1 demonstrated that root gravitropism requires auxin to be transported via the lateral root cap to all elongating epidermal cells. A three-dimensional model of the root elongation zone predicted that AUX1 causes the majority of auxin to accumulate in the epidermis. Selectively disrupting the auxin responsiveness of expanding epidermal cells by expressing a mutant form of the AUX/IAA17 protein, axr3-1, abolished root gravitropism. We conclude that gravitropic curvature in Arabidopsis roots is primarily driven by the differential expansion of epidermal cells in response to an influx-carrier-dependent auxin gradient.},
	language = {en},
	number = {11},
	urldate = {2021-06-11},
	journal = {Nature Cell Biology},
	author = {Swarup, Ranjan and Kramer, Eric M. and Perry, Paula and Knox, Kirsten and Leyser, H. M. Ottoline and Haseloff, Jim and Beemster, Gerrit T. S. and Bhalerao, Rishikesh P. and Bennett, Malcolm J.},
	month = nov,
	year = {2005},
	note = {Number: 11
Publisher: Nature Publishing Group},
	pages = {1057--1065},
}

Re-orientation of Arabidopsis seedlings induces a rapid, asymmetric release of the growth regulator auxin from gravity-sensing columella cells at the root apex. The resulting lateral auxin gradient is hypothesized to drive differential cell expansion in elongation-zone tissues. We mapped those root tissues that function to transport or respond to auxin during a gravitropic response. Targeted expression of the auxin influx facilitator AUX1 demonstrated that root gravitropism requires auxin to be transported via the lateral root cap to all elongating epidermal cells. A three-dimensional model of the root elongation zone predicted that AUX1 causes the majority of auxin to accumulate in the epidermis. Selectively disrupting the auxin responsiveness of expanding epidermal cells by expressing a mutant form of the AUX/IAA17 protein, axr3-1, abolished root gravitropism. We conclude that gravitropic curvature in Arabidopsis roots is primarily driven by the differential expansion of epidermal cells in response to an influx-carrier-dependent auxin gradient.

@article{sterky_populus_2004,
	title = {A {Populus} {EST} resource for plant functional genomics},
	volume = {101},
	copyright = {Copyright © 2004, The National Academy of Sciences},
	issn = {0027-8424, 1091-6490},
	url = {https://www.pnas.org/content/101/38/13951},
	doi = {10/brt6bx},
	abstract = {Trees present a life form of paramount importance for terrestrial ecosystems and human societies because of their ecological structure and physiological function and provision of energy and industrial materials. The genus Populus is the internationally accepted model for molecular tree biology. We have analyzed 102,019 Populus ESTs that clustered into 11,885 clusters and 12,759 singletons. We also provide {\textgreater}4,000 assembled full clone sequences to serve as a basis for the upcoming annotation of the Populus genome sequence. A public web-based EST database (populusdb) provides digital expression profiles for 18 tissues that comprise the majority of differentiated organs. The coding content of Populus and Arabidopsis genomes shows very high similarity, indicating that differences between these annual and perennial angiosperm life forms result primarily from differences in gene regulation. The high similarity between Populus and Arabidopsis will allow studies of Populus to directly benefit from the detailed functional genomic information generated for Arabidopsis, enabling detailed insights into tree development and adaptation. These data will also valuable for functional genomic efforts in Arabidopsis.},
	language = {en},
	number = {38},
	urldate = {2021-06-15},
	journal = {Proceedings of the National Academy of Sciences},
	author = {Sterky, Fredrik and Bhalerao, Rupali R. and Unneberg, Per and Segerman, Bo and Nilsson, Peter and Brunner, Amy M. and Charbonnel-Campaa, Laurence and Lindvall, Jenny Jonsson and Tandre, Karolina and Strauss, Steven H. and Sundberg, Björn and Gustafsson, Petter and Uhlén, Mathias and Bhalerao, Rishikesh P. and Nilsson, Ove and Sandberg, Göran and Karlsson, Jan and Lundeberg, Joakim and Jansson, Stefan},
	month = sep,
	year = {2004},
	pmid = {15353603},
	note = {Publisher: National Academy of Sciences
Section: Biological Sciences},
	pages = {13951--13956},
}

Trees present a life form of paramount importance for terrestrial ecosystems and human societies because of their ecological structure and physiological function and provision of energy and industrial materials. The genus Populus is the internationally accepted model for molecular tree biology. We have analyzed 102,019 Populus ESTs that clustered into 11,885 clusters and 12,759 singletons. We also provide \textgreater4,000 assembled full clone sequences to serve as a basis for the upcoming annotation of the Populus genome sequence. A public web-based EST database (populusdb) provides digital expression profiles for 18 tissues that comprise the majority of differentiated organs. The coding content of Populus and Arabidopsis genomes shows very high similarity, indicating that differences between these annual and perennial angiosperm life forms result primarily from differences in gene regulation. The high similarity between Populus and Arabidopsis will allow studies of Populus to directly benefit from the detailed functional genomic information generated for Arabidopsis, enabling detailed insights into tree development and adaptation. These data will also valuable for functional genomic efforts in Arabidopsis.

@article{andersson_transcriptional_2004,
	title = {A transcriptional timetable of autumn senescence},
	volume = {5},
	issn = {1474-760X},
	doi = {10/dw5fcc},
	abstract = {Background: We have developed genomic tools to allow the genus Populus ( aspens and cottonwoods) to be exploited as a full-featured model for investigating fundamental aspects of tree biology. We have undertaken large-scale expressed sequence tag ( EST) sequencing programs and created Populus microarrays with significant gene coverage. One of the important aspects of plant biology that cannot be studied in annual plants is the gene activity involved in the induction of autumn leaf senescence. Results: On the basis of 36,354 Populus ESTs, obtained from seven cDNA libraries, we have created a DNA microarray consisting of 13,490 clones, spotted in duplicate. Of these clones, 12,376 (92\%) were confirmed by resequencing and all sequences were annotated and functionally classified. Here we have used the microarray to study transcript abundance in leaves of a free-growing aspen tree ( Populus tremula) in northern Sweden during natural autumn senescence. Of the 13,490 spotted clones, 3,792 represented genes with significant expression in all leaf samples from the seven studied dates. Conclusions: We observed a major shift in gene expression, coinciding with massive chlorophyll degradation, that reflected a shift from photosynthetic competence to energy generation by mitochondrial respiration, oxidation of fatty acids and nutrient mobilization. Autumn senescence had much in common with senescence in annual plants; for example many proteases were induced. We also found evidence for increased transcriptional activity before the appearance of visible signs of senescence, presumably preparing the leaf for degradation of its components.},
	language = {English},
	number = {4},
	journal = {Genome Biology},
	author = {Andersson, A. and Keskitalo, J. and Sjodin, A. and Bhalerao, Rishikesh P. and Sterky, F. and Wissel, K. and Tandre, K. and Aspeborg, H. and Moyle, R. and Ohmiya, Y. and Bhalerao, R. and Brunner, A. and Gustafsson, P. and Karlsson, J. and Lundeberg, J. and Nilsson, O. and Sandberg, G. and Strauss, S. and Sundberg, B. and Uhlen, M. and Jansson, S. and Nilsson, P.},
	year = {2004},
	note = {Place: London
Publisher: Bmc
WOS:000220584700010},
	keywords = {aspen, biology, cytosolic glutamine-synthetase, gene-expression, genomics, leaf senescence, leaves, plants, programmed cell-death, proteins},
	pages = {R24},
}

Background: We have developed genomic tools to allow the genus Populus ( aspens and cottonwoods) to be exploited as a full-featured model for investigating fundamental aspects of tree biology. We have undertaken large-scale expressed sequence tag ( EST) sequencing programs and created Populus microarrays with significant gene coverage. One of the important aspects of plant biology that cannot be studied in annual plants is the gene activity involved in the induction of autumn leaf senescence. Results: On the basis of 36,354 Populus ESTs, obtained from seven cDNA libraries, we have created a DNA microarray consisting of 13,490 clones, spotted in duplicate. Of these clones, 12,376 (92%) were confirmed by resequencing and all sequences were annotated and functionally classified. Here we have used the microarray to study transcript abundance in leaves of a free-growing aspen tree ( Populus tremula) in northern Sweden during natural autumn senescence. Of the 13,490 spotted clones, 3,792 represented genes with significant expression in all leaf samples from the seven studied dates. Conclusions: We observed a major shift in gene expression, coinciding with massive chlorophyll degradation, that reflected a shift from photosynthetic competence to energy generation by mitochondrial respiration, oxidation of fatty acids and nutrient mobilization. Autumn senescence had much in common with senescence in annual plants; for example many proteases were induced. We also found evidence for increased transcriptional activity before the appearance of visible signs of senescence, presumably preparing the leaf for degradation of its components.

@article{schrader_cambial_2004,
	title = {Cambial meristem dormancy in trees involves extensive remodelling of the transcriptome},
	volume = {40},
	issn = {1365-313X},
	url = {https://onlinelibrary.wiley.com/doi/abs/10.1111/j.1365-313X.2004.02199.x},
	doi = {10/bfwz2r},
	abstract = {The establishment of the dormant state in meristems involves considerable physiological and metabolic alterations necessary for surviving unfavourable growth conditions. However, a global molecular analysis of dormancy in meristems has been hampered by the difficulty in isolating meristem cells. We used cryosectioning to isolate purified cambial meristem cells from the woody plant Populus tremula during active growth and dormancy. These samples were used to generate meristem-specific cDNA libraries and for cDNA microarray experiments to define the global transcriptional changes underlying cambial dormancy. The results indicate a significant reduction in the complexity of the cambial transcriptome in the dormant state. Although cell division is terminated in the dormant cambium, the cell cycle machinery appears to be maintained in a skeletal state as suggested by the continued presence of transcripts for several cell cycle regulators. The downregulation of PttPIN1 and PttPIN2 transcripts explains the reduced basipetal polar auxin transport during dormancy. The induction of a member of the SINA family of ubiquitin ligases implicated in auxin signalling indicates a potential mechanism for modulation of auxin sensitivity during cambial dormancy. The metabolic alterations during dormancy are mirrored in the induction of genes involved in starch breakdown and the glyoxysomal cycle. Interestingly, the induction of RGA1 like gene suggests modification of gibberellin signalling in cambial dormancy. The induction of genes such as poplar orthologues of FIE and HAP2 indicates a potential role for these global regulators of transcription in orchestrating extensive changes in gene expression during dormancy.},
	language = {en},
	number = {2},
	urldate = {2021-06-15},
	journal = {The Plant Journal},
	author = {Schrader, Jarmo and Moyle, Richard and Bhalerao, Rupali and Hertzberg, Magnus and Lundeberg, Joakim and Nilsson, Peter and Bhalerao, Rishikesh P.},
	year = {2004},
	note = {\_eprint: https://onlinelibrary.wiley.com/doi/pdf/10.1111/j.1365-313X.2004.02199.x},
	keywords = {Populus tremula, cambium, dormancy, meristem, microarray, wood formation},
	pages = {173--187},
}

The establishment of the dormant state in meristems involves considerable physiological and metabolic alterations necessary for surviving unfavourable growth conditions. However, a global molecular analysis of dormancy in meristems has been hampered by the difficulty in isolating meristem cells. We used cryosectioning to isolate purified cambial meristem cells from the woody plant Populus tremula during active growth and dormancy. These samples were used to generate meristem-specific cDNA libraries and for cDNA microarray experiments to define the global transcriptional changes underlying cambial dormancy. The results indicate a significant reduction in the complexity of the cambial transcriptome in the dormant state. Although cell division is terminated in the dormant cambium, the cell cycle machinery appears to be maintained in a skeletal state as suggested by the continued presence of transcripts for several cell cycle regulators. The downregulation of PttPIN1 and PttPIN2 transcripts explains the reduced basipetal polar auxin transport during dormancy. The induction of a member of the SINA family of ubiquitin ligases implicated in auxin signalling indicates a potential mechanism for modulation of auxin sensitivity during cambial dormancy. The metabolic alterations during dormancy are mirrored in the induction of genes involved in starch breakdown and the glyoxysomal cycle. Interestingly, the induction of RGA1 like gene suggests modification of gibberellin signalling in cambial dormancy. The induction of genes such as poplar orthologues of FIE and HAP2 indicates a potential role for these global regulators of transcription in orchestrating extensive changes in gene expression during dormancy.

@article{espinosa-ruiz_differential_2004,
	title = {Differential stage-specific regulation of cyclin-dependent kinases during cambial dormancy in hybrid aspen},
	volume = {38},
	issn = {1365-313X},
	url = {https://onlinelibrary.wiley.com/doi/abs/10.1111/j.1365-313X.2004.02070.x},
	doi = {10/d4fk2f},
	abstract = {The cambium of woody plants cycles between active and dormant states. Dormancy can be subdivided into eco- and endodormant stages. Ecodormant trees resume growth upon exposure to growth-promotive signals, while the establishment of endodormant state results in loss of the ability to respond to these signals. In this paper, we analysed the regulation of cyclin-dependent kinases (CDKs) to understand the differential response of cell division machinery to growth-promotive signals during the distinct stages of dormancy in hybrid aspen. We show that 4 weeks of short-day (SD) treatment causes termination of the cambial cell division and establishment of the ecodormant state. This coincides with a steady decline in the histone H1 kinase activity of the PSTAIRE-type poplar CDKA (PttCDKA) and the PPTTLRE-type PttCDKB kinase complexes. However, neither the transcript nor the polypeptide levels of PttCDKA and PttCDKB are reduced during ecodormancy. In contrast, 6 weeks of SD treatment establishes endodormancy, which is marked by the reduction and disappearance of the PttCDKA and PttCDKB protein levels and the PttCDKB transcript levels. The transition to endodormancy is preceded by an elevated E2F (adenosine E2 promoter binding factor) phosphorylation activity of the PttCDKA kinase that reduces the DNA-binding activity of E2F in vitro. The transition to endodormancy is followed by a reduction of retinoblastoma (Rb) phosphorylation activity of PttCDKA protein complexes. Both phosphorylation events could contribute to block the G1 to S phase transition upon the establishment of endodormancy. Our results indicate that eco- and endodormant stages of cambial dormancy involve a stage-specific regulation of the cell cycle effectors at multiple levels.},
	language = {en},
	number = {4},
	urldate = {2021-06-15},
	journal = {The Plant Journal},
	author = {Espinosa-Ruiz, Ana and Saxena, Sangeeta and Schmidt, Julien and Mellerowicz, Ewa and Miskolczi, Pál and Bakó, László and Bhalerao, Rishikesh P.},
	year = {2004},
	note = {\_eprint: https://onlinelibrary.wiley.com/doi/pdf/10.1111/j.1365-313X.2004.02070.x},
	keywords = {CDK regulation, cambial dormancy, cell cycle, ecodormancy, endodormancy, hybrid aspen},
	pages = {603--615},
}

The cambium of woody plants cycles between active and dormant states. Dormancy can be subdivided into eco- and endodormant stages. Ecodormant trees resume growth upon exposure to growth-promotive signals, while the establishment of endodormant state results in loss of the ability to respond to these signals. In this paper, we analysed the regulation of cyclin-dependent kinases (CDKs) to understand the differential response of cell division machinery to growth-promotive signals during the distinct stages of dormancy in hybrid aspen. We show that 4 weeks of short-day (SD) treatment causes termination of the cambial cell division and establishment of the ecodormant state. This coincides with a steady decline in the histone H1 kinase activity of the PSTAIRE-type poplar CDKA (PttCDKA) and the PPTTLRE-type PttCDKB kinase complexes. However, neither the transcript nor the polypeptide levels of PttCDKA and PttCDKB are reduced during ecodormancy. In contrast, 6 weeks of SD treatment establishes endodormancy, which is marked by the reduction and disappearance of the PttCDKA and PttCDKB protein levels and the PttCDKB transcript levels. The transition to endodormancy is preceded by an elevated E2F (adenosine E2 promoter binding factor) phosphorylation activity of the PttCDKA kinase that reduces the DNA-binding activity of E2F in vitro. The transition to endodormancy is followed by a reduction of retinoblastoma (Rb) phosphorylation activity of PttCDKA protein complexes. Both phosphorylation events could contribute to block the G1 to S phase transition upon the establishment of endodormancy. Our results indicate that eco- and endodormant stages of cambial dormancy involve a stage-specific regulation of the cell cycle effectors at multiple levels.

@article{karpinska_myb_2004,
	title = {{MYB} transcription factors are differentially expressed and regulated during secondary vascular tissue development in hybrid aspen},
	volume = {56},
	issn = {1573-5028},
	url = {https://doi.org/10.1007/s11103-004-3354-5},
	doi = {10/bg9dms},
	abstract = {More than 120,000 poplar ESTs have been sequenced from 20 different cDNA libraries by the Swedish Centre for Tree Functional Genomics. We screened this EST collection for MYB transcription factors involved in secondary vascular tissue formation, and genes assigned as PttMYB3Ra, PttMYB4a and PttMYB21a were selected for further characterisation. Three MYB genes showed different expression patterns in various organs, tissues and stem sub-sections representing different developmental stages of vascular tissue formation. Furthermore, the analysis showed that PttMYB21a expression was much higher in secondary cell wall formation zone of xylem and phloem fibers than in other developmental zones. Transgenic hybrid aspen plants, expressing the 3′-part of the PttMYB21a gene in antisense orientation were generated to assess the function of PttMYB21a gene in vascular tissue formation and lignification. All transgenic lines showed reduced growth and had fewer internodes compared to the wild-type. The analysis of selected lines showed that acid soluble lignin present in the bark was higher in transgenic lines as compared to wild-type plants. Moreover a higher transcript level of caffeoyl-CoA 3-O-methyltransferase [CCoAOMT]; EC 2.1.1.104) was found in the phloem of the transgenic plants, suggesting that PttMYB21a might function as a transcriptional repressor.},
	language = {en},
	number = {2},
	urldate = {2021-06-15},
	journal = {Plant Molecular Biology},
	author = {Karpinska, Barbara and Karlsson, Marlene and Srivastava, Manoj and Stenberg, Anneli and Schrader, Jarmo and Sterky, Fredrik and Bhalerao, Rishikesh P. and Wingsle, Gunnar},
	month = sep,
	year = {2004},
	pages = {255--270},
}

More than 120,000 poplar ESTs have been sequenced from 20 different cDNA libraries by the Swedish Centre for Tree Functional Genomics. We screened this EST collection for MYB transcription factors involved in secondary vascular tissue formation, and genes assigned as PttMYB3Ra, PttMYB4a and PttMYB21a were selected for further characterisation. Three MYB genes showed different expression patterns in various organs, tissues and stem sub-sections representing different developmental stages of vascular tissue formation. Furthermore, the analysis showed that PttMYB21a expression was much higher in secondary cell wall formation zone of xylem and phloem fibers than in other developmental zones. Transgenic hybrid aspen plants, expressing the 3′-part of the PttMYB21a gene in antisense orientation were generated to assess the function of PttMYB21a gene in vascular tissue formation and lignification. All transgenic lines showed reduced growth and had fewer internodes compared to the wild-type. The analysis of selected lines showed that acid soluble lignin present in the bark was higher in transgenic lines as compared to wild-type plants. Moreover a higher transcript level of caffeoyl-CoA 3-O-methyltransferase [CCoAOMT]; EC 2.1.1.104) was found in the phloem of the transgenic plants, suggesting that PttMYB21a might function as a transcriptional repressor.

@article{baba_organellar_2004,
	title = {Organellar gene transcription and early seedling development are affected in the {rpoT};2 mutant of {Arabidopsis}},
	volume = {38},
	issn = {1365-313X},
	url = {https://onlinelibrary.wiley.com/doi/abs/10.1111/j.1365-313X.2004.02022.x},
	doi = {10/dtrc6f},
	abstract = {An Arabidopsis mutant that exhibited reduced root length was isolated from a population of activation-tagged T-DNA insertion lines in a screen for aberrant root growth. This mutant also exhibited reduced hypocotyl length as well as a delay in greening and altered leaf shape. Molecular genetic analysis of the mutant indicated a single T-DNA insertion in the gene RpoT;2 encoding a homolog of the phage-type RNA polymerase (RNAP), that is targeted to both mitochondria and plastids. A second T-DNA-tagged allele also showed a similar phenotype. The mutation in RpoT;2 affected the light-induced accumulation of several plastid mRNAs and proteins and resulted in a lower photosynthetic efficiency. In contrast to the alterations in the plastid gene expression, no major effect of the rpoT;2 mutation on the accumulation of examined mitochondrial gene transcripts and proteins was observed. The rpoT;2 mutant exhibited tissue-specific alterations in the transcript levels of two other organelle-directed nuclear-encoded RNAPs, RpoT;1 and RpoT;3. This suggests the existence of cross-talk between the regulatory pathways of the three RNAPs through organelle to nucleus communication. These data provide an important information on a role of RpoT;2 in plastid gene expression and early plant development.},
	language = {en},
	number = {1},
	urldate = {2021-06-15},
	journal = {The Plant Journal},
	author = {Baba, Kyoko and Schmidt, Julien and Espinosa-Ruiz, Ana and Villarejo, Arsenio and Shiina, Takashi and Gardeström, Per and Sane, Aniruddha P. and Bhalerao, Rishikesh P.},
	year = {2004},
	note = {\_eprint: https://onlinelibrary.wiley.com/doi/pdf/10.1111/j.1365-313X.2004.02022.x},
	keywords = {NEP, PEP, mitochondria, organelle-nucleus signaling, plastid, transcription},
	pages = {38--48},
}

An Arabidopsis mutant that exhibited reduced root length was isolated from a population of activation-tagged T-DNA insertion lines in a screen for aberrant root growth. This mutant also exhibited reduced hypocotyl length as well as a delay in greening and altered leaf shape. Molecular genetic analysis of the mutant indicated a single T-DNA insertion in the gene RpoT;2 encoding a homolog of the phage-type RNA polymerase (RNAP), that is targeted to both mitochondria and plastids. A second T-DNA-tagged allele also showed a similar phenotype. The mutation in RpoT;2 affected the light-induced accumulation of several plastid mRNAs and proteins and resulted in a lower photosynthetic efficiency. In contrast to the alterations in the plastid gene expression, no major effect of the rpoT;2 mutation on the accumulation of examined mitochondrial gene transcripts and proteins was observed. The rpoT;2 mutant exhibited tissue-specific alterations in the transcript levels of two other organelle-directed nuclear-encoded RNAPs, RpoT;1 and RpoT;3. This suggests the existence of cross-talk between the regulatory pathways of the three RNAPs through organelle to nucleus communication. These data provide an important information on a role of RpoT;2 in plastid gene expression and early plant development.

@article{hilson_versatile_2004,
	title = {Versatile {Gene}-{Specific} {Sequence} {Tags} for {Arabidopsis} {Functional} {Genomics}: {Transcript} {Profiling} and {Reverse} {Genetics} {Applications}},
	volume = {14},
	issn = {1088-9051, 1549-5469},
	shorttitle = {Versatile {Gene}-{Specific} {Sequence} {Tags} for {Arabidopsis} {Functional} {Genomics}},
	url = {https://genome.cshlp.org/content/14/10b/2176},
	doi = {10/brkpzf},
	abstract = {Microarray transcript profiling and RNA interference are two new technologies crucial for large-scale gene function studies in multicellular eukaryotes. Both rely on sequence-specific hybridization between complementary nucleic acid strands, inciting us to create a collection of gene-specific sequence tags (GSTs) representing at least 21,500 Arabidopsis genes and which are compatible with both approaches. The GSTs were carefully selected to ensure that each of them shared no significant similarity with any other region in the Arabidopsis genome. They were synthesized by PCR amplification from genomic DNA. Spotted microarrays fabricated from the GSTs show good dynamic range, specificity, and sensitivity in transcript profiling experiments. The GSTs have also been transferred to bacterial plasmid vectors via recombinational cloning protocols. These cloned GSTs constitute the ideal starting point for a variety of functional approaches, including reverse genetics. We have subcloned GSTs on a large scale into vectors designed for gene silencing in plant cells. We show that in planta expression of GST hairpin RNA results in the expected phenotypes in silenced Arabidopsis lines. These versatile GST resources provide novel and powerful tools for functional genomics.},
	language = {en},
	number = {10b},
	urldate = {2021-06-30},
	journal = {Genome Research},
	author = {Hilson, Pierre and Allemeersch, Joke and Altmann, Thomas and Aubourg, Sébastien and Avon, Alexandra and Beynon, Jim and Bhalerao, Rishikesh P. and Bitton, Frédérique and Caboche, Michel and Cannoot, Bernard and Chardakov, Vasil and Cognet-Holliger, Cécile and Colot, Vincent and Crowe, Mark and Darimont, Caroline and Durinck, Steffen and Eickhoff, Holger and Longevialle, Andéol Falcon de and Farmer, Edward E. and Grant, Murray and Kuiper, Martin T. R. and Lehrach, Hans and Léon, Céline and Leyva, Antonio and Lundeberg, Joakim and Lurin, Claire and Moreau, Yves and Nietfeld, Wilfried and Paz-Ares, Javier and Reymond, Philippe and Rouzé, Pierre and Sandberg, Goran and Segura, Maria Dolores and Serizet, Carine and Tabrett, Alexandra and Taconnat, Ludivine and Thareau, Vincent and Hummelen, Paul Van and Vercruysse, Steven and Vuylsteke, Marnik and Weingartner, Magdalena and Weisbeek, Peter J. and Wirta, Valtteri and Wittink, Floyd R. A. and Zabeau, Marc and Small, Ian},
	month = oct,
	year = {2004},
	pmid = {15489341},
	note = {Company: Cold Spring Harbor Laboratory Press
Distributor: Cold Spring Harbor Laboratory Press
Institution: Cold Spring Harbor Laboratory Press
Label: Cold Spring Harbor Laboratory Press
Publisher: Cold Spring Harbor Lab},
	pages = {2176--2189},
}

Microarray transcript profiling and RNA interference are two new technologies crucial for large-scale gene function studies in multicellular eukaryotes. Both rely on sequence-specific hybridization between complementary nucleic acid strands, inciting us to create a collection of gene-specific sequence tags (GSTs) representing at least 21,500 Arabidopsis genes and which are compatible with both approaches. The GSTs were carefully selected to ensure that each of them shared no significant similarity with any other region in the Arabidopsis genome. They were synthesized by PCR amplification from genomic DNA. Spotted microarrays fabricated from the GSTs show good dynamic range, specificity, and sensitivity in transcript profiling experiments. The GSTs have also been transferred to bacterial plasmid vectors via recombinational cloning protocols. These cloned GSTs constitute the ideal starting point for a variety of functional approaches, including reverse genetics. We have subcloned GSTs on a large scale into vectors designed for gene silencing in plant cells. We show that in planta expression of GST hairpin RNA results in the expected phenotypes in silenced Arabidopsis lines. These versatile GST resources provide novel and powerful tools for functional genomics.

@article{bhalerao_gene_2003,
	title = {Gene {Expression} in {Autumn} {Leaves}},
	volume = {131},
	issn = {0032-0889},
	url = {https://doi.org/10.1104/pp.012732},
	doi = {10.1104/pp.012732},
	abstract = {Two cDNA libraries were prepared, one from leaves of a field-grown aspen (Populus tremula) tree, harvested just before any visible sign of leaf senescence in the autumn, and one from young but fully expanded leaves of greenhouse-grown aspen (Populus tremula × tremuloides). Expressed sequence tags (ESTs; 5,128 and 4,841, respectively) were obtained from the two libraries. A semiautomatic method of annotation and functional classification of the ESTs, according to a modified Munich Institute of Protein Sequences classification scheme, was developed, utilizing information from three different databases. The patterns of gene expression in the two libraries were strikingly different. In the autumn leaf library, ESTs encoding metallothionein, early light-inducible proteins, and cysteine proteases were most abundant. Clones encoding other proteases and proteins involved in respiration and breakdown of lipids and pigments, as well as stress-related genes, were also well represented. We identified homologs to many known senescence-associated genes, as well as seven different genes encoding cysteine proteases, two encoding aspartic proteases, five encoding metallothioneins, and 35 additional genes that were up-regulated in autumn leaves. We also indirectly estimated the rate of plastid protein synthesis in the autumn leaves to be less that 10\% of that in young leaves.},
	number = {2},
	urldate = {2024-06-28},
	journal = {Plant Physiology},
	author = {Bhalerao, Rupali and Keskitalo, Johanna and Sterky, Fredrik and Erlandsson, Rikard and Björkbacka, Harry and Birve, Simon Jonsson and Karlsson, Jan and Gardeström, Per and Gustafsson, Petter and Lundeberg, Joakim and Jansson, Stefan},
	month = feb,
	year = {2003},
	pages = {430--442},
}

Two cDNA libraries were prepared, one from leaves of a field-grown aspen (Populus tremula) tree, harvested just before any visible sign of leaf senescence in the autumn, and one from young but fully expanded leaves of greenhouse-grown aspen (Populus tremula × tremuloides). Expressed sequence tags (ESTs; 5,128 and 4,841, respectively) were obtained from the two libraries. A semiautomatic method of annotation and functional classification of the ESTs, according to a modified Munich Institute of Protein Sequences classification scheme, was developed, utilizing information from three different databases. The patterns of gene expression in the two libraries were strikingly different. In the autumn leaf library, ESTs encoding metallothionein, early light-inducible proteins, and cysteine proteases were most abundant. Clones encoding other proteases and proteins involved in respiration and breakdown of lipids and pigments, as well as stress-related genes, were also well represented. We identified homologs to many known senescence-associated genes, as well as seven different genes encoding cysteine proteases, two encoding aspartic proteases, five encoding metallothioneins, and 35 additional genes that were up-regulated in autumn leaves. We also indirectly estimated the rate of plastid protein synthesis in the autumn leaves to be less that 10% of that in young leaves.

@article{bhalerao_out_2003,
	title = {Out of the woods: forest biotechnology enters the genomic era},
	volume = {14},
	issn = {0958-1669},
	shorttitle = {Out of the woods},
	url = {https://www.sciencedirect.com/science/article/pii/S0958166903000296},
	doi = {10/fp8hj9},
	abstract = {Trees represent a unique life form of upmost importance for mankind, as these organisms have developed a perennial lifestyle that produces the majority of terrestrial biomass. The difference between trees and annual plants is one of the main arguments behind the effort to sequence the entire genome of the poplar tree. This initiative is being backed up with a full-scale functional genomics effort on trees that will set a completely new agenda for forest research.},
	language = {en},
	number = {2},
	urldate = {2021-07-05},
	journal = {Current Opinion in Biotechnology},
	author = {Bhalerao, Rishikesh and Nilsson, Ove and Sandberg, Goran},
	month = apr,
	year = {2003},
	pages = {206--213},
}

Trees represent a unique life form of upmost importance for mankind, as these organisms have developed a perennial lifestyle that produces the majority of terrestrial biomass. The difference between trees and annual plants is one of the main arguments behind the effort to sequence the entire genome of the poplar tree. This initiative is being backed up with a full-scale functional genomics effort on trees that will set a completely new agenda for forest research.

@article{marchant_aux1_2002,
	title = {{AUX1} {Promotes} {Lateral} {Root} {Formation} by {Facilitating} {Indole}-3-{Acetic} {Acid} {Distribution} between {Sink} and {Source} {Tissues} in the {Arabidopsis} {Seedling}},
	volume = {14},
	issn = {1040-4651},
	url = {https://doi.org/10.1105/tpc.010354},
	doi = {10/btp7mv},
	abstract = {Arabidopsis root architecture is regulated by shoot-derived signals such as nitrate and auxin. We report that mutations in the putative auxin influx carrier AUX1 modify root architecture as a result of the disruption in hormone transport between indole-3-acetic acid (IAA) source and sink tissues. Gas chromatography–selected reaction monitoring–mass spectrometry measurements revealed that the aux1 mutant exhibited altered IAA distribution in young leaf and root tissues, the major IAA source and sink organs, respectively, in the developing seedling. Expression studies using the auxin-inducible reporter IAA2::uidA revealed that AUX1 facilitates IAA loading into the leaf vascular transport system. AUX1 also facilitates IAA unloading in the primary root apex and developing lateral root primordium. Exogenous application of the synthetic auxin 1-naphthylacetic acid is able to rescue the aux1 lateral root phenotype, implying that root auxin levels are suboptimal for lateral root primordium initiation in the mutant.},
	number = {3},
	urldate = {2021-10-19},
	journal = {The Plant Cell},
	author = {Marchant, Alan and Bhalerao, Rishikesh and Casimiro, Ilda and Eklöf, Jan and Casero, Pedro J. and Bennett, Malcolm and Sandberg, Goran},
	month = mar,
	year = {2002},
	pages = {589--597},
}

Arabidopsis root architecture is regulated by shoot-derived signals such as nitrate and auxin. We report that mutations in the putative auxin influx carrier AUX1 modify root architecture as a result of the disruption in hormone transport between indole-3-acetic acid (IAA) source and sink tissues. Gas chromatography–selected reaction monitoring–mass spectrometry measurements revealed that the aux1 mutant exhibited altered IAA distribution in young leaf and root tissues, the major IAA source and sink organs, respectively, in the developing seedling. Expression studies using the auxin-inducible reporter IAA2::uidA revealed that AUX1 facilitates IAA loading into the leaf vascular transport system. AUX1 also facilitates IAA unloading in the primary root apex and developing lateral root primordium. Exogenous application of the synthetic auxin 1-naphthylacetic acid is able to rescue the aux1 lateral root phenotype, implying that root auxin levels are suboptimal for lateral root primordium initiation in the mutant.

@article{moyle_environmental_2002,
	title = {Environmental and auxin regulation of wood formation involves members of the {Aux}/{IAA} gene family in hybrid aspen},
	volume = {31},
	issn = {1365-313X},
	url = {https://onlinelibrary.wiley.com/doi/abs/10.1046/j.1365-313X.2002.01386.x},
	doi = {10/fw3n8w},
	abstract = {Indole acetic acid (IAA/auxin) profoundly affects wood formation but the molecular mechanism of auxin action in this process remains poorly understood. We have cloned cDNAs for eight members of the Aux/IAA gene family from hybrid aspen (Populus tremula L. × Populus tremuloides Michx.) that encode potential mediators of the auxin signal transduction pathway. These genes designated as PttIAA1-PttIAA8 are auxin inducible but differ in their requirement of de novo protein synthesis for auxin induction. The auxin induction of the PttIAA genes is also developmentally controlled as evidenced by the loss of their auxin inducibility during leaf maturation. The PttIAA genes are differentially expressed in the cell types of a developmental gradient comprising the wood-forming tissues. Interestingly, the expression of the PttIAA genes is downregulated during transition of the active cambium into dormancy, a process in which meristematic cells of the cambium lose their sensitivity to auxin. Auxin-regulated developmental reprogramming of wood formation during the induction of tension wood is accompanied by changes in the expression of PttIAA genes. The distinct tissue-specific expression patterns of the auxin inducible PttIAA genes in the cambial region together with the change in expression during dormancy transition and tension wood formation suggest a role for these genes in mediating cambial responses to auxin and xylem development.},
	language = {en},
	number = {6},
	urldate = {2021-10-19},
	journal = {The Plant Journal},
	author = {Moyle, Richard and Schrader, Jarmo and Stenberg, Anneli and Olsson, Olof and Saxena, Sangeeta and Sandberg, Göran and Bhalerao, Rishikesh P},
	year = {2002},
	note = {\_eprint: https://onlinelibrary.wiley.com/doi/pdf/10.1046/j.1365-313X.2002.01386.x},
	keywords = {Aux, IAA proteins, auxin, development, dormancy, tension wood, wood formation},
	pages = {675--685},
}

Indole acetic acid (IAA/auxin) profoundly affects wood formation but the molecular mechanism of auxin action in this process remains poorly understood. We have cloned cDNAs for eight members of the Aux/IAA gene family from hybrid aspen (Populus tremula L. × Populus tremuloides Michx.) that encode potential mediators of the auxin signal transduction pathway. These genes designated as PttIAA1-PttIAA8 are auxin inducible but differ in their requirement of de novo protein synthesis for auxin induction. The auxin induction of the PttIAA genes is also developmentally controlled as evidenced by the loss of their auxin inducibility during leaf maturation. The PttIAA genes are differentially expressed in the cell types of a developmental gradient comprising the wood-forming tissues. Interestingly, the expression of the PttIAA genes is downregulated during transition of the active cambium into dormancy, a process in which meristematic cells of the cambium lose their sensitivity to auxin. Auxin-regulated developmental reprogramming of wood formation during the induction of tension wood is accompanied by changes in the expression of PttIAA genes. The distinct tissue-specific expression patterns of the auxin inducible PttIAA genes in the cambial region together with the change in expression during dormancy transition and tension wood formation suggest a role for these genes in mediating cambial responses to auxin and xylem development.

@article{bhalerao_shoot-derived_2002,
	title = {Shoot-derived auxin is essential for early lateral root emergence in {Arabidopsis} seedlings},
	volume = {29},
	issn = {1365-313X},
	url = {https://onlinelibrary.wiley.com/doi/abs/10.1046/j.0960-7412.2001.01217.x},
	doi = {10/cjt66p},
	abstract = {Lateral root formation is profoundly affected by auxins. Here we present data which indicate that light influences the formation of indole-3-acetic acid (IAA) in germinating Arabidopsis seedlings. IAA transported from the developing leaves to the root system is detectable as a short-lived pulse in the roots and is required for the emergence of the lateral root primordia (LRP) during early seedling development. LRP emergence is inhibited by the removal of apical tissues prior to detection of the IAA pulse in the root, but this treatment has minimal effects on LRP initiation. Our results identify the first developing true leaves as the most likely source for the IAA required for the first emergence of the LRP, as removal of cotyledons has only a minor effect on LRP emergence in contrast to removal of the leaves. A basipetal IAA concentration gradient with high levels of IAA in the root tip appears to control LRP initiation, in contrast to their emergence. A significant increase in the ability of the root system to synthesize IAA is observed 10 days after germination, and this in turn is reflected in the reduced dependence of the lateral root emergence on aerial tissue-derived auxin at this stage. We propose a model for lateral root formation during early seedling development that can be divided into two phases: (i) an LRP initiation phase dependent on a root tip-localized IAA source, and (ii) an LRP emergence phase dependent on leaf-derived IAA up to 10 days after germination.},
	language = {en},
	number = {3},
	urldate = {2021-10-19},
	journal = {The Plant Journal},
	author = {Bhalerao, Rishikesh P. and Eklöf, Jan and Ljung, Karin and Marchant, Alan and Bennett, Malcolm and Sandberg, Göran},
	year = {2002},
	note = {\_eprint: https://onlinelibrary.wiley.com/doi/pdf/10.1046/j.0960-7412.2001.01217.x},
	keywords = {Arabidopsis thaliana, IAA, auxin, lateral root},
	pages = {325--332},
}

Lateral root formation is profoundly affected by auxins. Here we present data which indicate that light influences the formation of indole-3-acetic acid (IAA) in germinating Arabidopsis seedlings. IAA transported from the developing leaves to the root system is detectable as a short-lived pulse in the roots and is required for the emergence of the lateral root primordia (LRP) during early seedling development. LRP emergence is inhibited by the removal of apical tissues prior to detection of the IAA pulse in the root, but this treatment has minimal effects on LRP initiation. Our results identify the first developing true leaves as the most likely source for the IAA required for the first emergence of the LRP, as removal of cotyledons has only a minor effect on LRP emergence in contrast to removal of the leaves. A basipetal IAA concentration gradient with high levels of IAA in the root tip appears to control LRP initiation, in contrast to their emergence. A significant increase in the ability of the root system to synthesize IAA is observed 10 days after germination, and this in turn is reflected in the reduced dependence of the lateral root emergence on aerial tissue-derived auxin at this stage. We propose a model for lateral root formation during early seedling development that can be divided into two phases: (i) an LRP initiation phase dependent on a root tip-localized IAA source, and (ii) an LRP emergence phase dependent on leaf-derived IAA up to 10 days after germination.

@article{hertzberg_transcriptional_2001,
	title = {A transcriptional roadmap to wood formation},
	volume = {98},
	copyright = {Copyright © 2001, The National Academy of Sciences},
	issn = {0027-8424, 1091-6490},
	url = {https://www.pnas.org/content/98/25/14732},
	doi = {10/ckrdsz},
	abstract = {The large vascular meristem of poplar trees with its highly organized secondary xylem enables the boundaries between different developmental zones to be easily distinguished. This property of wood-forming tissues allowed us to determine a unique tissue-specific transcript profile for a well defined developmental gradient. RNA was prepared from different developmental stages of xylogenesis for DNA microarray analysis by using a hybrid aspen unigene set consisting of 2,995 expressed sequence tags. The analysis revealed that the genes encoding lignin and cellulose biosynthetic enzymes, as well as a number of transcription factors and other potential regulators of xylogenesis, are under strict developmental stage-specific transcriptional regulation.},
	language = {en},
	number = {25},
	urldate = {2021-11-02},
	journal = {Proceedings of the National Academy of Sciences},
	author = {Hertzberg, Magnus and Aspeborg, Henrik and Schrader, Jarmo and Andersson, Anders and Erlandsson, Rikard and Blomqvist, Kristina and Bhalerao, Rupali and Uhlén, Mathias and Teeri, Tuula T. and Lundeberg, Joakim and Sundberg, Björn and Nilsson, Peter and Sandberg, Göran},
	month = dec,
	year = {2001},
	pmid = {11724959},
	note = {Publisher: National Academy of Sciences
Section: Biological Sciences},
	pages = {14732--14737},
}

The large vascular meristem of poplar trees with its highly organized secondary xylem enables the boundaries between different developmental zones to be easily distinguished. This property of wood-forming tissues allowed us to determine a unique tissue-specific transcript profile for a well defined developmental gradient. RNA was prepared from different developmental stages of xylogenesis for DNA microarray analysis by using a hybrid aspen unigene set consisting of 2,995 expressed sequence tags. The analysis revealed that the genes encoding lignin and cellulose biosynthetic enzymes, as well as a number of transcription factors and other potential regulators of xylogenesis, are under strict developmental stage-specific transcriptional regulation.

@article{casimiro_auxin_2001,
	title = {Auxin {Transport} {Promotes} {Arabidopsis} {Lateral} {Root} {Initiation}},
	volume = {13},
	issn = {1040-4651},
	url = {https://doi.org/10.1105/tpc.13.4.843},
	doi = {10.1105/tpc.13.4.843},
	abstract = {Lateral root development in Arabidopsis provides a model for the study of hormonal signals that regulate postembryonic organogenesis in higher plants. Lateral roots originate from pairs of pericycle cells, in several cell files positioned opposite the xylem pole, that initiate a series of asymmetric, transverse divisions. The auxin transport inhibitor N-1-naphthylphthalamic acid (NPA) arrests lateral root development by blocking the first transverse division(s). We investigated the basis of NPA action by using a cell-specific reporter to demonstrate that xylem pole pericycle cells retain their identity in the presence of the auxin transport inhibitor. However, NPA causes indoleacetic acid (IAA) to accumulate in the root apex while reducing levels in basal tissues critical for lateral root initiation. This pattern of IAA redistribution is consistent with NPA blocking basipetal IAA movement from the root tip. Characterization of lateral root development in the shoot meristemless1 mutant demonstrates that root basipetal and leaf acropetal auxin transport activities are required during the initiation and emergence phases, respectively, of lateral root development.},
	number = {4},
	urldate = {2021-11-02},
	journal = {The Plant Cell},
	author = {Casimiro, Ilda and Marchant, Alan and Bhalerao, Rishikesh P. and Beeckman, Tom and Dhooge, Sandra and Swarup, Ranjan and Graham, Neil and Inzé, Dirk and Sandberg, Goran and Casero, Pedro J. and Bennett, Malcolm},
	month = apr,
	year = {2001},
	pages = {843--852},
}

Lateral root development in Arabidopsis provides a model for the study of hormonal signals that regulate postembryonic organogenesis in higher plants. Lateral roots originate from pairs of pericycle cells, in several cell files positioned opposite the xylem pole, that initiate a series of asymmetric, transverse divisions. The auxin transport inhibitor N-1-naphthylphthalamic acid (NPA) arrests lateral root development by blocking the first transverse division(s). We investigated the basis of NPA action by using a cell-specific reporter to demonstrate that xylem pole pericycle cells retain their identity in the presence of the auxin transport inhibitor. However, NPA causes indoleacetic acid (IAA) to accumulate in the root apex while reducing levels in basal tissues critical for lateral root initiation. This pattern of IAA redistribution is consistent with NPA blocking basipetal IAA movement from the root tip. Characterization of lateral root development in the shoot meristemless1 mutant demonstrates that root basipetal and leaf acropetal auxin transport activities are required during the initiation and emergence phases, respectively, of lateral root development.

@article{ljung_sites_2001,
	title = {Sites and homeostatic control of auxin biosynthesis in {Arabidopsis} during vegetative growth},
	volume = {28},
	issn = {1365-313X},
	url = {https://onlinelibrary.wiley.com/doi/abs/10.1046/j.1365-313X.2001.01173.x},
	doi = {10.1046/j.1365-313X.2001.01173.x},
	abstract = {The distribution and biosynthesis of indole-3-acetic acid (IAA) was investigated during early plant development in Arabidopsis. The youngest leaves analysed, less than 0.5 mm in length, contained 250 pg mg−1 of IAA and also exhibited the highest relative capacity to synthesize this hormone. A decrease of nearly one hundred-fold in IAA content occurred as the young leaves expanded to their full size, and this was accompanied by a clear shift in both pool size and IAA synthesis capacity. The correlation between high IAA content and intense cell division was further verified in tobacco leaves, where a detailed analysis revealed that dividing mesophyll tissue contained ten-fold higher IAA levels than tissue growing solely by elongation. We demonstrated that all parts of the young Arabidopsis plant can potentially contribute to the auxin needed for growth and development, as not only young leaves, but also all other parts of the plant such as cotyledons, expanding leaves and root tissues have the capacity to synthesize IAA de novo. We also observed that naphthylphthalamic acid (NPA) treatment induced tissue-dependent feedback inhibition of IAA biosynthesis in expanding leaves and cotyledons, but intriguingly not in young leaves or in the root system. This observation supports the hypothesis that there is a sophisticated tissue-specific regulatory mechanism for auxin biosynthesis. Finally, a strict requirement for maintaining the pool sizes of IAA was revealed as reductions in leaf expansion followed both decreases and increases in the IAA levels in developing leaves. This indicates that leaves are not only important sources for IAA synthesis, but that normal leaf expansion depends on rigorous control of IAA homeostasis.},
	language = {en},
	number = {4},
	urldate = {2021-11-02},
	journal = {The Plant Journal},
	author = {Ljung, Karin and Bhalerao, Rishikesh P. and Sandberg, Göran},
	year = {2001},
	note = {\_eprint: https://onlinelibrary.wiley.com/doi/pdf/10.1046/j.1365-313X.2001.01173.x},
	keywords = {auxin, distribution and biosynthesis, feedback inhibition, indole-3-acetic acid, leaf expansion, naphthylphthalamic acid},
	pages = {465--474},
}

The distribution and biosynthesis of indole-3-acetic acid (IAA) was investigated during early plant development in Arabidopsis. The youngest leaves analysed, less than 0.5 mm in length, contained 250 pg mg−1 of IAA and also exhibited the highest relative capacity to synthesize this hormone. A decrease of nearly one hundred-fold in IAA content occurred as the young leaves expanded to their full size, and this was accompanied by a clear shift in both pool size and IAA synthesis capacity. The correlation between high IAA content and intense cell division was further verified in tobacco leaves, where a detailed analysis revealed that dividing mesophyll tissue contained ten-fold higher IAA levels than tissue growing solely by elongation. We demonstrated that all parts of the young Arabidopsis plant can potentially contribute to the auxin needed for growth and development, as not only young leaves, but also all other parts of the plant such as cotyledons, expanding leaves and root tissues have the capacity to synthesize IAA de novo. We also observed that naphthylphthalamic acid (NPA) treatment induced tissue-dependent feedback inhibition of IAA biosynthesis in expanding leaves and cotyledons, but intriguingly not in young leaves or in the root system. This observation supports the hypothesis that there is a sophisticated tissue-specific regulatory mechanism for auxin biosynthesis. Finally, a strict requirement for maintaining the pool sizes of IAA was revealed as reductions in leaf expansion followed both decreases and increases in the IAA levels in developing leaves. This indicates that leaves are not only important sources for IAA synthesis, but that normal leaf expansion depends on rigorous control of IAA homeostasis.

@article{yamaguchi_activation_2000,
	title = {Activation of {CDK}-activating kinase is dependent on interaction with {H}-type cyclins in plants},
	volume = {24},
	issn = {1365-313X},
	url = {https://onlinelibrary.wiley.com/doi/abs/10.1046/j.1365-313x.2000.00846.x},
	doi = {10/cxkrs9},
	abstract = {cDNAs encoding cyclin H homologs were isolated from poplar (Populus tremulax tremuloides) and rice (Oryza sativa) plants, and were designated Pt;cycH;1 and Os;cycH;1, respectively. The deduced amino-acid sequences showed 40–60\% similarity to human cyclin H and Schizosaccharomyces pombe Mcs2, with higher similarity in the cyclin box region. While Pt;cycH;1 and Os;cycH;1 were expressed in all tissues examined, the transcripts accumulated abundantly in dividing cells. Expression of Os;cycH;1 was abundant in the S-phase in partially synchronized suspension cells, and was induced by submergence in internodes of deepwater rice. A yeast two-hybrid assay demonstrated that both Pt;CycH;1 and Os;CycH;1 were able to interact with rice R2 kinase, which is structurally and functionally similar to cyclin-dependent kinase (CDK)-activating kinase (CAK) of vertebrates. Moreover, an in vitro pull-down assay showed that Os;CycH;1 specifically bound to R2 but not to other rice CDKs. When R2 was expressed in budding yeast CAK mutant, the suppression activity in terms of temperature-sensitivity was enhanced by co-expression with Os;cycH;1. Furthermore, in vitro kinase assay indicated that the kinase activities of R2 on CDKs and the carboxy-terminal domain (CTD) of the largest subunit of RNA polymerase II were markedly elevated by binding to Os;CycH;1. Our results suggest that cyclin H is a regulatory subunit of CAK, which positively controls CDK- and CTD-kinase activities in plant cells.},
	language = {en},
	number = {1},
	urldate = {2021-11-08},
	journal = {The Plant Journal},
	author = {Yamaguchi, Masatoshi and Fabian, Tanja and Sauter, Margret and Bhalerao, Rishikesh P. and Schrader, Jarmo and Sandberg, Göran and Umeda, Masaaki and Uchimiya, Hirofumi},
	year = {2000},
	note = {\_eprint: https://onlinelibrary.wiley.com/doi/pdf/10.1046/j.1365-313x.2000.00846.x},
	keywords = {CDK-activating kinase, cell cycle, cyclin H, cyclin-dependent protein kinase, poplar, rice},
	pages = {11--20},
}

cDNAs encoding cyclin H homologs were isolated from poplar (Populus tremulax tremuloides) and rice (Oryza sativa) plants, and were designated Pt;cycH;1 and Os;cycH;1, respectively. The deduced amino-acid sequences showed 40–60% similarity to human cyclin H and Schizosaccharomyces pombe Mcs2, with higher similarity in the cyclin box region. While Pt;cycH;1 and Os;cycH;1 were expressed in all tissues examined, the transcripts accumulated abundantly in dividing cells. Expression of Os;cycH;1 was abundant in the S-phase in partially synchronized suspension cells, and was induced by submergence in internodes of deepwater rice. A yeast two-hybrid assay demonstrated that both Pt;CycH;1 and Os;CycH;1 were able to interact with rice R2 kinase, which is structurally and functionally similar to cyclin-dependent kinase (CDK)-activating kinase (CAK) of vertebrates. Moreover, an in vitro pull-down assay showed that Os;CycH;1 specifically bound to R2 but not to other rice CDKs. When R2 was expressed in budding yeast CAK mutant, the suppression activity in terms of temperature-sensitivity was enhanced by co-expression with Os;cycH;1. Furthermore, in vitro kinase assay indicated that the kinase activities of R2 on CDKs and the carboxy-terminal domain (CTD) of the largest subunit of RNA polymerase II were markedly elevated by binding to Os;CycH;1. Our results suggest that cyclin H is a regulatory subunit of CAK, which positively controls CDK- and CTD-kinase activities in plant cells.

@article{kleinow_functional_2000,
	title = {Functional identification of an {Arabidopsis} {Snf4} ortholog by screening for heterologous multicopy suppressors of snf4 deficiency in yeast},
	volume = {23},
	issn = {1365-313X},
	url = {https://onlinelibrary.wiley.com/doi/abs/10.1046/j.1365-313x.2000.00809.x},
	doi = {10/btmg6n},
	abstract = {Yeast Snf4 is a prototype of activating γ-subunits of conserved Snf1/AMPK-related protein kinases (SnRKs) controlling glucose and stress signaling in eukaryotes. The catalytic subunits of Arabidopsis SnRKs, AKIN10 and AKIN11, interact with Snf4 and suppress the snf1 and snf4 mutations in yeast. By expression of an Arabidopsis cDNA library in yeast, heterologous multicopy snf4 suppressors were isolated. In addition to AKIN10 and AKIN11, the deficiency of yeast snf4 mutant to grown on non-fermentable carbon source was suppressed by Arabidopsis Myb30, CAAT-binding factor Hap3b, casein kinase I, zinc-finger factors AZF2 and ZAT10, as well as orthologs of hexose/UDP-hexose transporters, calmodulin, SMC1-cohesin and Snf4. Here we describe the characterization of AtSNF4, a functional Arabidopsis Snf4 ortholog, that interacts with yeast Snf1 and specifically binds to the C-terminal regulatory domain of Arabidopsis SnRKs AKIN10 and AKIN11.},
	language = {en},
	number = {1},
	urldate = {2021-11-08},
	journal = {The Plant Journal},
	author = {Kleinow, Tatjana and Bhalerao, Rishikesh and Breuer, Frank and Umeda, Masaaki and Salchert, Klaus and Koncz, Csaba},
	year = {2000},
	note = {\_eprint: https://onlinelibrary.wiley.com/doi/pdf/10.1046/j.1365-313x.2000.00809.x},
	keywords = {Snf1-related protein kinases, glucose signaling, protein interaction, suppressors of snf4, yeast two-hybrid system},
	pages = {115--122},
}

Yeast Snf4 is a prototype of activating γ-subunits of conserved Snf1/AMPK-related protein kinases (SnRKs) controlling glucose and stress signaling in eukaryotes. The catalytic subunits of Arabidopsis SnRKs, AKIN10 and AKIN11, interact with Snf4 and suppress the snf1 and snf4 mutations in yeast. By expression of an Arabidopsis cDNA library in yeast, heterologous multicopy snf4 suppressors were isolated. In addition to AKIN10 and AKIN11, the deficiency of yeast snf4 mutant to grown on non-fermentable carbon source was suppressed by Arabidopsis Myb30, CAAT-binding factor Hap3b, casein kinase I, zinc-finger factors AZF2 and ZAT10, as well as orthologs of hexose/UDP-hexose transporters, calmodulin, SMC1-cohesin and Snf4. Here we describe the characterization of AtSNF4, a functional Arabidopsis Snf4 ortholog, that interacts with yeast Snf1 and specifically binds to the C-terminal regulatory domain of Arabidopsis SnRKs AKIN10 and AKIN11.

@article{barlier_sur2_2000,
	title = {The {SUR2} gene of {Arabidopsis} thaliana encodes the cytochrome {P450} {CYP83B1}, a modulator of auxin homeostasis},
	volume = {97},
	copyright = {Copyright © 2000, The National Academy of Sciences},
	issn = {0027-8424, 1091-6490},
	url = {https://www.pnas.org/content/97/26/14819},
	doi = {10/c36wb6},
	abstract = {Genetic screens have been performed to identify mutants with altered auxin homeostasis in Arabidopsis. A tagged allele of the auxin-overproducing mutant sur2 was identified within a transposon mutagenized population. The SUR2 gene was cloned and shown to encode the CYP83B1 protein, which belongs to the large family of the P450-dependent monooxygenases. SUR2 expression is up-regulated in sur1 mutants and induced by exogenous auxin in the wild type. Analysis of indole-3-acetic acid (IAA) synthesis and metabolism in sur2 plants indicates that the mutation causes a conditional increase in the pool size of IAA through up-regulation of IAA synthesis.},
	language = {en},
	number = {26},
	urldate = {2021-11-08},
	journal = {Proceedings of the National Academy of Sciences},
	author = {Barlier, Isabelle and Kowalczyk, Mariusz and Marchant, Alan and Ljung, Karin and Bhalerao, Rishikesh and Bennett, Malcolm and Sandberg, Goeran and Bellini, Catherine},
	month = dec,
	year = {2000},
	pmid = {11114200},
	note = {Publisher: National Academy of Sciences
Section: Biological Sciences},
	keywords = {metabolism},
	pages = {14819--14824},
}

Genetic screens have been performed to identify mutants with altered auxin homeostasis in Arabidopsis. A tagged allele of the auxin-overproducing mutant sur2 was identified within a transposon mutagenized population. The SUR2 gene was cloned and shown to encode the CYP83B1 protein, which belongs to the large family of the P450-dependent monooxygenases. SUR2 expression is up-regulated in sur1 mutants and induced by exogenous auxin in the wild type. Analysis of indole-3-acetic acid (IAA) synthesis and metabolism in sur2 plants indicates that the mutation causes a conditional increase in the pool size of IAA through up-regulation of IAA synthesis.

@article{bhalerao_regulatory_1999,
	title = {Regulatory interaction of {PRL1} {WD} protein with {Arabidopsis} {SNF1}-like protein kinases},
	volume = {96},
	url = {https://www.ncbi.nlm.nih.gov/sites/ppmc/articles/PMC21862/},
	doi = {10/fpvx8m},
	abstract = {Mutation of the PRL1 gene, encoding a regulatory WD protein, results in glucose hypersensitivity and derepression of glucose-regulated genes in Arabidopsis. The yeast SNF1 protein kinase, a key regulator of glucose signaling, and Arabidopsis SNF1 homologs ...},
	language = {en},
	number = {9},
	urldate = {2021-11-08},
	journal = {Proceedings of the National Academy of Sciences of the United States of America},
	author = {Bhalerao, Rishikesh P. and Salchert, Klaus and Bakó, László and Ökrész, László and Szabados, László and Muranaka, Toshiya and Machida, Yasunori and Schell, Jeff and Koncz, Csaba},
	month = apr,
	year = {1999},
	pmid = {10220464},
	note = {Publisher: National Academy of Sciences},
	pages = {5322},
}

Mutation of the PRL1 gene, encoding a regulatory WD protein, results in glucose hypersensitivity and derepression of glucose-regulated genes in Arabidopsis. The yeast SNF1 protein kinase, a key regulator of glucose signaling, and Arabidopsis SNF1 homologs ...