Schmid, Markus - Regulation of Plant Growth & Development by the Environment

@incollection{riechmann_isolation_2023,
	address = {New York, NY},
	title = {Isolation of {Nuclei} {Tagged} in {Specific} {Cell} {Types} ({INTACT}) in {Arabidopsis}},
	volume = {2686},
	isbn = {978-1-07-163298-7 978-1-07-163299-4},
	url = {https://link.springer.com/10.1007/978-1-0716-3299-4_16},
	abstract = {Many functionally distinct plant tissues have relatively low numbers of cells that are embedded within complex tissues. For example, the shoot apical meristem (SAM) consists of a small population of pluripotent stem cells surrounded by developing leaves and/or flowers at the growing tip of the plant. It is technically challenging to collect enough high-quality SAM samples for molecular analyses. Isolation of Nuclei Tagged in specific Cell Types (INTACT) is an easily reproducible method that allows the enrichment of biotin-tagged cell-type-specific nuclei from the total nuclei pool using biotin-streptavidin affinity purification. Here, we provide a detailed INTACT protocol for isolating nuclei from the Arabidopsis SAM. One can also adapt this protocol to isolate nuclei from other tissues and cell types for investigating tissue/cell-type-specific transcriptome and epigenome and their changes during developmental programs at a high spatiotemporal resolution. Furthermore, due to its low cost and simple procedures, INTACT can be conducted in any standard molecular laboratory.},
	language = {en},
	urldate = {2023-08-14},
	booktitle = {Flower {Development}},
	author = {Benstein, Ruben M. and Schmid, Markus and You, Yuan},
	editor = {Riechmann, José Luis and Ferrándiz, Cristina},
	month = jan,
	year = {2023},
	doi = {10.1007/978-1-0716-3299-4_16},
	note = {Series Title: Methods in Molecular Biology},
	pages = {313--328},
}

Many functionally distinct plant tissues have relatively low numbers of cells that are embedded within complex tissues. For example, the shoot apical meristem (SAM) consists of a small population of pluripotent stem cells surrounded by developing leaves and/or flowers at the growing tip of the plant. It is technically challenging to collect enough high-quality SAM samples for molecular analyses. Isolation of Nuclei Tagged in specific Cell Types (INTACT) is an easily reproducible method that allows the enrichment of biotin-tagged cell-type-specific nuclei from the total nuclei pool using biotin-streptavidin affinity purification. Here, we provide a detailed INTACT protocol for isolating nuclei from the Arabidopsis SAM. One can also adapt this protocol to isolate nuclei from other tissues and cell types for investigating tissue/cell-type-specific transcriptome and epigenome and their changes during developmental programs at a high spatiotemporal resolution. Furthermore, due to its low cost and simple procedures, INTACT can be conducted in any standard molecular laboratory.

@article{andre_flowering_2022,
	title = {{FLOWERING} {LOCUS} {T} paralogs control the annual growth cycle in {Populus} trees},
	volume = {32},
	issn = {0960-9822},
	url = {https://www.cell.com/current-biology/abstract/S0960-9822(22)00782-5},
	doi = {10.1016/j.cub.2022.05.023},
	abstract = {In temperate and boreal regions, perennials adapt their annual growth cycle to the change of seasons. These adaptations ensure survival in harsh environmental conditions, allowing growth at different latitudes and altitudes, and are therefore tightly regulated. Populus tree species cease growth and form terminal buds in autumn when photoperiod falls below a certain threshold.1 This is followed by establishment of dormancy and cold hardiness over the winter. At the center of the photoperiodic pathway in Populus is the gene FLOWERING LOCUS T2 (FT2), which is expressed during summer and harbors significant SNPs in its locus associated with timing of bud set.1, 2, 3, 4 The paralogous gene FT1, on the other hand, is hyper-induced in chilling buds during winter.3,5 Even though its function is so far unknown, it has been suggested to be involved in the regulation of flowering and the release of winter dormancy.3,5 In this study, we employ CRISPR-Cas9-mediated gene editing to individually study the function of the FT-like genes in Populus trees. We show that while FT2 is required for vegetative growth during spring and summer and regulates the entry into dormancy, expression of FT1 is absolutely required for bud flush in spring. Gene expression profiling suggests that this function of FT1 is linked to the release of winter dormancy rather than to the regulation of bud flush per se. These data show how FT duplication and sub-functionalization have allowed Populus trees to regulate two completely different and major developmental control points during the yearly growth cycle.},
	language = {English},
	number = {13},
	urldate = {2022-08-12},
	journal = {Current Biology},
	author = {André, Domenique and Marcon, Alice and Lee, Keh Chien and Goretti, Daniela and Zhang, Bo and Delhomme, Nicolas and Schmid, Markus and Nilsson, Ove},
	month = jul,
	year = {2022},
	pmid = {35660141},
	note = {Publisher: Elsevier},
	keywords = {FLOWERING LOCUS T, Populus, annual growth cycle, bud flush, dormancy, paralogs},
	pages = {2988--2996.e4},
}

In temperate and boreal regions, perennials adapt their annual growth cycle to the change of seasons. These adaptations ensure survival in harsh environmental conditions, allowing growth at different latitudes and altitudes, and are therefore tightly regulated. Populus tree species cease growth and form terminal buds in autumn when photoperiod falls below a certain threshold.1 This is followed by establishment of dormancy and cold hardiness over the winter. At the center of the photoperiodic pathway in Populus is the gene FLOWERING LOCUS T2 (FT2), which is expressed during summer and harbors significant SNPs in its locus associated with timing of bud set.1, 2, 3, 4 The paralogous gene FT1, on the other hand, is hyper-induced in chilling buds during winter.3,5 Even though its function is so far unknown, it has been suggested to be involved in the regulation of flowering and the release of winter dormancy.3,5 In this study, we employ CRISPR-Cas9-mediated gene editing to individually study the function of the FT-like genes in Populus trees. We show that while FT2 is required for vegetative growth during spring and summer and regulates the entry into dormancy, expression of FT1 is absolutely required for bud flush in spring. Gene expression profiling suggests that this function of FT1 is linked to the release of winter dormancy rather than to the regulation of bud flush per se. These data show how FT duplication and sub-functionalization have allowed Populus trees to regulate two completely different and major developmental control points during the yearly growth cycle.

@article{zacharaki_impaired_2022,
	title = {Impaired {KIN10} function restores developmental defects in the {Arabidopsis} trehalose 6-phosphate synthase1 (tps1) mutant},
	volume = {235},
	issn = {1469-8137},
	url = {https://onlinelibrary.wiley.com/doi/abs/10.1111/nph.18104},
	doi = {10.1111/nph.18104},
	abstract = {Sensing carbohydrate availability is essential for plants to coordinate their growth and development. In Arabidopsis thaliana, TREHALOSE 6-PHOSPHATE SYNTHASE 1 (TPS1) and its product, trehalose 6-phosphate (T6P), are important for the metabolic control of development. tps1 mutants are embryo-lethal and unable to flower when embryogenesis is rescued. T6P regulates development in part through inhibition of SUCROSE NON-FERMENTING1 RELATED KINASE1 (SnRK1). Here, we explored the role of SnRK1 in T6P-mediated plant growth and development using a combination of a mutant suppressor screen and genetic, cellular and transcriptomic approaches. We report nonsynonymous amino acid substitutions in the catalytic KIN10 and regulatory SNF4 subunits of SnRK1 that can restore both embryogenesis and flowering of tps1 mutant plants. The identified SNF4 point mutations disrupt the interaction with the catalytic subunit KIN10. Contrary to the common view that the two A. thaliana SnRK1 catalytic subunits act redundantly, we found that loss-of-function mutations in KIN11 are unable to restore embryogenesis and flowering, highlighting the important role of KIN10 in T6P signalling.},
	language = {en},
	number = {1},
	urldate = {2022-06-09},
	journal = {New Phytologist},
	author = {Zacharaki, Vasiliki and Ponnu, Jathish and Crepin, Nathalie and Langenecker, Tobias and Hagmann, Jörg and Skorzinski, Noemi and Musialak-Lange, Magdalena and Wahl, Vanessa and Rolland, Filip and Schmid, Markus},
	year = {2022},
	keywords = {Arabidopsis thaliana, SnRK1 complex, T6P pathway, TPS1, embryogenesis, flowering time},
	pages = {220--233},
}

Sensing carbohydrate availability is essential for plants to coordinate their growth and development. In Arabidopsis thaliana, TREHALOSE 6-PHOSPHATE SYNTHASE 1 (TPS1) and its product, trehalose 6-phosphate (T6P), are important for the metabolic control of development. tps1 mutants are embryo-lethal and unable to flower when embryogenesis is rescued. T6P regulates development in part through inhibition of SUCROSE NON-FERMENTING1 RELATED KINASE1 (SnRK1). Here, we explored the role of SnRK1 in T6P-mediated plant growth and development using a combination of a mutant suppressor screen and genetic, cellular and transcriptomic approaches. We report nonsynonymous amino acid substitutions in the catalytic KIN10 and regulatory SNF4 subunits of SnRK1 that can restore both embryogenesis and flowering of tps1 mutant plants. The identified SNF4 point mutations disrupt the interaction with the catalytic subunit KIN10. Contrary to the common view that the two A. thaliana SnRK1 catalytic subunits act redundantly, we found that loss-of-function mutations in KIN11 are unable to restore embryogenesis and flowering, highlighting the important role of KIN10 in T6P signalling.

@article{mateos_picln_2022,
	title = {{PICLN} modulates alternative splicing and light/temperature responses in plants},
	issn = {0032-0889},
	url = {https://doi.org/10.1093/plphys/kiac527},
	doi = {10.1093/plphys/kiac527},
	abstract = {Plants undergo transcriptome reprogramming to adapt to daily and seasonal fluctuations in light and temperature conditions. While most efforts have focused on the role of master transcription factors, the importance of splicing factors modulating these processes is now emerging. Efficient pre-mRNA splicing depends on proper spliceosome assembly, which in plants and animals requires the methylosome complex. Ion Chloride nucleotide-sensitive protein (PICLN) is part of the methylosome complex in both humans and Arabidopsis (Arabidopsis thaliana), and we show here that the human PICLN ortholog rescues phenotypes of Arabidopsis picln mutants. Altered photomorphogenic and photoperiodic responses in Arabidopsis picln mutants are associated with changes in pre-mRNA splicing that partially overlap with those in PROTEIN-ARGININE METHYL TRANSFERASE5 (prmt5) mutants. Mammalian PICLN also acts in concert with the Survival Motor Neuron (SMN) complex component GEMIN2 to modulate the late steps of UsnRNP assembly, and many alternative splicing events regulated by PICLN but not PRMT5, the main protein of the methylosome, are controlled by Arabidopsis GEMIN2. As with GEMIN2 and SM PROTEIN E1/PORCUPINE (SME1/PCP), low temperature, which increases PICLN expression, aggravates morphological and molecular defects of picln mutants. Taken together, these results establish a key role for PICLN in the regulation of pre-mRNA splicing and in mediating plant adaptation to daily and seasonal fluctuations in environmental conditions.},
	urldate = {2022-12-02},
	journal = {Plant Physiology},
	author = {Mateos, Julieta L and Sanchez, Sabrina E and Legris, Martina and Esteve-Bruna, David and Torchio, Jeanette C and Petrillo, Ezequiel and Goretti, Daniela and Blanco-Touriñán, Noel and Seymour, Danelle K and Schmid, Markus and Weigel, Detlef and Alabadí, David and Yanovsky, Marcelo J},
	month = nov,
	year = {2022},
	pages = {kiac527},
}

Plants undergo transcriptome reprogramming to adapt to daily and seasonal fluctuations in light and temperature conditions. While most efforts have focused on the role of master transcription factors, the importance of splicing factors modulating these processes is now emerging. Efficient pre-mRNA splicing depends on proper spliceosome assembly, which in plants and animals requires the methylosome complex. Ion Chloride nucleotide-sensitive protein (PICLN) is part of the methylosome complex in both humans and Arabidopsis (Arabidopsis thaliana), and we show here that the human PICLN ortholog rescues phenotypes of Arabidopsis picln mutants. Altered photomorphogenic and photoperiodic responses in Arabidopsis picln mutants are associated with changes in pre-mRNA splicing that partially overlap with those in PROTEIN-ARGININE METHYL TRANSFERASE5 (prmt5) mutants. Mammalian PICLN also acts in concert with the Survival Motor Neuron (SMN) complex component GEMIN2 to modulate the late steps of UsnRNP assembly, and many alternative splicing events regulated by PICLN but not PRMT5, the main protein of the methylosome, are controlled by Arabidopsis GEMIN2. As with GEMIN2 and SM PROTEIN E1/PORCUPINE (SME1/PCP), low temperature, which increases PICLN expression, aggravates morphological and molecular defects of picln mutants. Taken together, these results establish a key role for PICLN in the regulation of pre-mRNA splicing and in mediating plant adaptation to daily and seasonal fluctuations in environmental conditions.

@article{pandey_epigenetic_2021,
	title = {Epigenetic {Regulation} of {Temperature} {Responses} – {Past} {Successes} and {Future} {Challenges}},
	volume = {72},
	issn = {0022-0957, 1460-2431},
	url = {https://academic.oup.com/jxb/advance-article/doi/10.1093/jxb/erab248/6288481},
	doi = {10.1093/jxb/erab248},
	abstract = {Abstract
            In contrast to animals, plants cannot avoid unfavorable temperature conditions. Instead, plants have evolved intricate signaling pathways that enable them to perceive and respond to temperature. General acclimation processes that prepare the plant to respond to stressful heat and cold, usually occur throughout the whole plant. More specific temperature responses, however, are limited to certain tissues or cell types. While global responses are amenable to epigenomic analyses, responses which are highly localized are more problematic as the chromatin in question is not easily accessible. Here we review the current knowledge of the epigenetic regulation of FLOWERING LOCUS C and FLOWERING LOCUS T as examples of temperature-responsive flowering time regulators that are expressed broadly throughout the plants and in specific cell types, respectively. While undoubtably extremely successful, we reason that future analyses would benefit from higher spatiotemporal resolution. We conclude by reviewing methods and successful applications of tissue- and cell type-specific epigenomic analyses and provide a brief outlook into the future, single-cell epigenomics.},
	language = {en},
	number = {21},
	urldate = {2021-06-03},
	journal = {Journal of Experimental Botany},
	author = {Pandey, Saurabh Prakash and Benstein, Ruben M and Wang, Yanwei and Schmid, Markus},
	month = may,
	year = {2021},
	pages = {7482--7497},
}

Abstract In contrast to animals, plants cannot avoid unfavorable temperature conditions. Instead, plants have evolved intricate signaling pathways that enable them to perceive and respond to temperature. General acclimation processes that prepare the plant to respond to stressful heat and cold, usually occur throughout the whole plant. More specific temperature responses, however, are limited to certain tissues or cell types. While global responses are amenable to epigenomic analyses, responses which are highly localized are more problematic as the chromatin in question is not easily accessible. Here we review the current knowledge of the epigenetic regulation of FLOWERING LOCUS C and FLOWERING LOCUS T as examples of temperature-responsive flowering time regulators that are expressed broadly throughout the plants and in specific cell types, respectively. While undoubtably extremely successful, we reason that future analyses would benefit from higher spatiotemporal resolution. We conclude by reviewing methods and successful applications of tissue- and cell type-specific epigenomic analyses and provide a brief outlook into the future, single-cell epigenomics.

@article{dikaya_insights_2021,
	title = {Insights into the role of alternative splicing in plant temperature response},
	volume = {72},
	issn = {0022-0957},
	url = {https://doi.org/10.1093/jxb/erab234},
	doi = {10/gkhp7j},
	abstract = {Alternative splicing occurs in all eukaryotic organisms. Since the first description of multiexon genes and the splicing machinery, the field has expanded rapidly, especially in animals and yeast. However, our knowledge about splicing in plants is still quite fragmented. Though eukaryotes show some similarity in the composition and dynamics of their splicing machinery, observations of unique plant traits are only starting to emerge. For instance, plant alternative splicing is closely linked to their ability to perceive various environmental stimuli. Due to their sessile lifestyle, temperature is a central source of information, allowing plants to adjust their development to match current growth conditions. Hence, seasonal temperature fluctuations and day–night cycles can strongly influence plant morphology across developmental stages. Here we discuss available data on temperature-dependent alternative splicing in plants. Given its fragmented state, it is not always possible to fit specific observations into a coherent picture, yet it is sufficient to estimate the complexity of this field and the need for further research. Better understanding of alternative splicing as a part of plant temperature response and adaptation may also prove to be a powerful tool for both fundamental and applied sciences.},
	number = {21},
	urldate = {2022-02-04},
	journal = {Journal of Experimental Botany},
	author = {Dikaya, Varvara and El Arbi, Nabila and Rojas-Murcia, Nelson and Nardeli, Sarah Muniz and Goretti, Daniela and Schmid, Markus},
	month = nov,
	year = {2021},
	pages = {7384--7403},
}

Alternative splicing occurs in all eukaryotic organisms. Since the first description of multiexon genes and the splicing machinery, the field has expanded rapidly, especially in animals and yeast. However, our knowledge about splicing in plants is still quite fragmented. Though eukaryotes show some similarity in the composition and dynamics of their splicing machinery, observations of unique plant traits are only starting to emerge. For instance, plant alternative splicing is closely linked to their ability to perceive various environmental stimuli. Due to their sessile lifestyle, temperature is a central source of information, allowing plants to adjust their development to match current growth conditions. Hence, seasonal temperature fluctuations and day–night cycles can strongly influence plant morphology across developmental stages. Here we discuss available data on temperature-dependent alternative splicing in plants. Given its fragmented state, it is not always possible to fit specific observations into a coherent picture, yet it is sufficient to estimate the complexity of this field and the need for further research. Better understanding of alternative splicing as a part of plant temperature response and adaptation may also prove to be a powerful tool for both fundamental and applied sciences.

@article{muralidhara_perturbations_2021,
	title = {Perturbations in plant energy homeostasis prime lateral root initiation via {SnRK1}-{bZIP63}-{ARF19} signaling},
	volume = {118},
	copyright = {© 2021 . https://www.pnas.org/site/aboutpnas/licenses.xhtmlPublished under the PNAS license.},
	issn = {0027-8424, 1091-6490},
	url = {https://www.pnas.org/content/118/37/e2106961118},
	doi = {10/gmvnsg},
	abstract = {Plants adjust their energy metabolism to continuous environmental fluctuations, resulting in a tremendous plasticity in their architecture. The regulatory circuits involved, however, remain largely unresolved. In Arabidopsis, moderate perturbations in photosynthetic activity, administered by short-term low light exposure or unexpected darkness, lead to increased lateral root (LR) initiation. Consistent with expression of low-energy markers, these treatments alter energy homeostasis and reduce sugar availability in roots. Here, we demonstrate that the LR response requires the metabolic stress sensor kinase Snf1-RELATED-KINASE1 (SnRK1), which phosphorylates the transcription factor BASIC LEUCINE ZIPPER63 (bZIP63) that directly binds and activates the promoter of AUXIN RESPONSE FACTOR19 (ARF19), a key regulator of LR initiation. Consistently, starvation-induced ARF19 transcription is impaired in bzip63 mutants. This study highlights a positive developmental function of SnRK1. During energy limitation, LRs are initiated and primed for outgrowth upon recovery. Hence, this study provides mechanistic insights into how energy shapes the agronomically important root system.},
	language = {en},
	number = {37},
	urldate = {2021-11-12},
	journal = {Proceedings of the National Academy of Sciences},
	author = {Muralidhara, Prathibha and Weiste, Christoph and Collani, Silvio and Krischke, Markus and Kreisz, Philipp and Draken, Jan and Feil, Regina and Mair, Andrea and Teige, Markus and Müller, Martin J. and Schmid, Markus and Becker, Dirk and Lunn, John E. and Rolland, Filip and Hanson, Johannes and Dröge-Laser, Wolfgang},
	month = sep,
	year = {2021},
	keywords = {ARF19, SnRK1, bZIP63, lateral root, metabolic homeostasis},
}

Plants adjust their energy metabolism to continuous environmental fluctuations, resulting in a tremendous plasticity in their architecture. The regulatory circuits involved, however, remain largely unresolved. In Arabidopsis, moderate perturbations in photosynthetic activity, administered by short-term low light exposure or unexpected darkness, lead to increased lateral root (LR) initiation. Consistent with expression of low-energy markers, these treatments alter energy homeostasis and reduce sugar availability in roots. Here, we demonstrate that the LR response requires the metabolic stress sensor kinase Snf1-RELATED-KINASE1 (SnRK1), which phosphorylates the transcription factor BASIC LEUCINE ZIPPER63 (bZIP63) that directly binds and activates the promoter of AUXIN RESPONSE FACTOR19 (ARF19), a key regulator of LR initiation. Consistently, starvation-induced ARF19 transcription is impaired in bzip63 mutants. This study highlights a positive developmental function of SnRK1. During energy limitation, LRs are initiated and primed for outgrowth upon recovery. Hence, this study provides mechanistic insights into how energy shapes the agronomically important root system.

@article{yang_mirna_2021,
	title = {{miRNA} {Mediated} {Regulation} and {Interaction} between {Plants} and {Pathogens}},
	volume = {22},
	issn = {1422-0067},
	url = {https://www.mdpi.com/1422-0067/22/6/2913},
	doi = {10/gjjv65},
	abstract = {Plants have evolved diverse molecular mechanisms that enable them to respond to a wide range of pathogens. It has become clear that microRNAs, a class of short single-stranded RNA molecules that regulate gene expression at the transcriptional or post-translational level, play a crucial role in coordinating plant-pathogen interactions. Specifically, miRNAs have been shown to be involved in the regulation of phytohormone signals, reactive oxygen species, and NBS-LRR gene expression, thereby modulating the arms race between hosts and pathogens. Adding another level of complexity, it has recently been shown that specific lncRNAs (ceRNAs) can act as decoys that interact with and modulate the activity of miRNAs. Here we review recent findings regarding the roles of miRNA in plant defense, with a focus on the regulatory modes of miRNAs and their possible applications in breeding pathogen-resistance plants including crops and trees. Special emphasis is placed on discussing the role of miRNA in the arms race between hosts and pathogens, and the interaction between disease-related miRNAs and lncRNAs.},
	language = {en},
	number = {6},
	urldate = {2021-06-03},
	journal = {International Journal of Molecular Sciences},
	author = {Yang, Xiaoqian and Zhang, Lichun and Yang, Yuzhang and Schmid, Markus and Wang, Yanwei},
	month = mar,
	year = {2021},
	pages = {2913},
}

Plants have evolved diverse molecular mechanisms that enable them to respond to a wide range of pathogens. It has become clear that microRNAs, a class of short single-stranded RNA molecules that regulate gene expression at the transcriptional or post-translational level, play a crucial role in coordinating plant-pathogen interactions. Specifically, miRNAs have been shown to be involved in the regulation of phytohormone signals, reactive oxygen species, and NBS-LRR gene expression, thereby modulating the arms race between hosts and pathogens. Adding another level of complexity, it has recently been shown that specific lncRNAs (ceRNAs) can act as decoys that interact with and modulate the activity of miRNAs. Here we review recent findings regarding the roles of miRNA in plant defense, with a focus on the regulatory modes of miRNAs and their possible applications in breeding pathogen-resistance plants including crops and trees. Special emphasis is placed on discussing the role of miRNA in the arms race between hosts and pathogens, and the interaction between disease-related miRNAs and lncRNAs.

@article{lee_gibberellin_2020,
	title = {A gibberellin methyltransferase modulates the timing of floral transition at the {Arabidopsis} shoot meristem},
	volume = {170},
	issn = {0031-9317, 1399-3054},
	url = {https://onlinelibrary.wiley.com/doi/10.1111/ppl.13146},
	doi = {10.1111/ppl.13146},
	language = {en},
	number = {4},
	urldate = {2021-06-07},
	journal = {Physiologia Plantarum},
	author = {Lee, Joanne E. and Goretti, Daniela and Neumann, Manuela and Schmid, Markus and You, Yuan},
	month = dec,
	year = {2020},
	pages = {474--487},
}

@article{brunoni_conifers_2020,
	title = {Conifers exhibit a characteristic inactivation of auxin to maintain tissue homeostasis},
	volume = {226},
	issn = {0028-646X, 1469-8137},
	url = {https://onlinelibrary.wiley.com/doi/10.1111/nph.16463},
	doi = {10.1111/nph.16463},
	language = {en},
	number = {6},
	urldate = {2021-06-07},
	journal = {New Phytologist},
	author = {Brunoni, Federica and Collani, Silvio and Casanova‐Sáez, Rubén and Šimura, Jan and Karady, Michal and Schmid, Markus and Ljung, Karin and Bellini, Catherine},
	month = jun,
	year = {2020},
	pages = {1753--1765},
}

@article{goretti_terminal_2020,
	title = {{TERMINAL} {FLOWER1} {Functions} as a {Mobile} {Transcriptional} {Cofactor} in the {Shoot} {Apical} {Meristem}},
	volume = {182},
	issn = {0032-0889, 1532-2548},
	url = {https://academic.oup.com/plphys/article/182/4/2081-2095/6116513},
	doi = {10/ghqb3x},
	language = {en},
	number = {4},
	urldate = {2021-06-07},
	journal = {Plant Physiology},
	author = {Goretti, Daniela and Silvestre, Marina and Collani, Silvio and Langenecker, Tobias and Méndez, Carla and Madueño, Francisco and Schmid, Markus},
	month = apr,
	year = {2020},
	pages = {2081--2095},
}

@article{ponnu_trehalose_2020,
	title = {The trehalose 6‐phosphate pathway impacts vegetative phase change in \textit{{Arabidopsis} thaliana}},
	volume = {104},
	issn = {0960-7412, 1365-313X},
	url = {https://onlinelibrary.wiley.com/doi/10.1111/tpj.14965},
	doi = {10.1111/tpj.14965},
	language = {en},
	number = {3},
	urldate = {2021-06-07},
	journal = {The Plant Journal},
	author = {Ponnu, Jathish and Schlereth, Armin and Zacharaki, Vasiliki and Działo, Magdalena A. and Abel, Christin and Feil, Regina and Schmid, Markus and Wahl, Vanessa},
	month = nov,
	year = {2020},
	pages = {768--780},
}

@article{brunoni_bacterial_2019,
	title = {A bacterial assay for rapid screening of {IAA} catabolic enzymes},
	volume = {15},
	issn = {1746-4811},
	url = {https://plantmethods.biomedcentral.com/articles/10.1186/s13007-019-0509-6},
	doi = {10.1186/s13007-019-0509-6},
	abstract = {Abstract
            
              Background
              
                Plants rely on concentration gradients of the native auxin, indole-3-acetic acid (IAA), to modulate plant growth and development. Both metabolic and transport processes participate in the dynamic regulation of IAA homeostasis. Free IAA levels can be reduced by inactivation mechanisms, such as conjugation and degradation. IAA can be conjugated via ester linkage to glucose, or via amide linkage to amino acids, and degraded via oxidation. Members of the UDP glucosyl transferase (UGT) family catalyze the conversion of IAA to indole-3-acetyl-1-glucosyl ester (IAGlc); by contrast, IAA is irreversibly converted to indole-3-acetyl-
                l
                -aspartic acid (IAAsp) and indole-3-acetyl glutamic acid (IAGlu) by Group II of the GRETCHEN HAGEN3 (GH3) family of acyl amido synthetases. Dioxygenase for auxin oxidation (DAO) irreversibly oxidizes IAA to oxindole-3-acetic acid (oxIAA) and, in turn, oxIAA can be further glucosylated to oxindole-3-acetyl-1-glucosyl ester (oxIAGlc) by UGTs. These metabolic pathways have been identified based on mutant analyses, in vitro activity measurements, and
                in planta
                feeding assays. In vitro assays for studying protein activity are based on producing Arabidopsis enzymes in a recombinant form in bacteria or yeast followed by recombinant protein purification. However, the need to extract and purify the recombinant proteins represents a major obstacle when performing in vitro assays.
              
            
            
              Results
              In this work we report a rapid, reproducible and cheap method to screen the enzymatic activity of recombinant proteins that are known to inactivate IAA. The enzymatic reactions are carried out directly in bacteria that produce the recombinant protein. The enzymatic products can be measured by direct injection of a small supernatant fraction from the bacterial culture on ultrahigh-performance liquid chromatography coupled to electrospray ionization tandem spectrometry (UHPLC–ESI-MS/MS). Experimental procedures were optimized for testing the activity of different classes of IAA-modifying enzymes without the need to purify recombinant protein.
            
            
              Conclusions
              This new method represents an alternative to existing in vitro assays. It can be applied to the analysis of IAA metabolites that are produced upon supplementation of substrate to engineered bacterial cultures and can be used for a rapid screening of orthologous candidate genes from non-model species.},
	language = {en},
	number = {1},
	urldate = {2021-06-07},
	journal = {Plant Methods},
	author = {Brunoni, Federica and Collani, Silvio and Šimura, Jan and Schmid, Markus and Bellini, Catherine and Ljung, Karin},
	month = dec,
	year = {2019},
	pages = {126},
}

Abstract Background Plants rely on concentration gradients of the native auxin, indole-3-acetic acid (IAA), to modulate plant growth and development. Both metabolic and transport processes participate in the dynamic regulation of IAA homeostasis. Free IAA levels can be reduced by inactivation mechanisms, such as conjugation and degradation. IAA can be conjugated via ester linkage to glucose, or via amide linkage to amino acids, and degraded via oxidation. Members of the UDP glucosyl transferase (UGT) family catalyze the conversion of IAA to indole-3-acetyl-1-glucosyl ester (IAGlc); by contrast, IAA is irreversibly converted to indole-3-acetyl- l -aspartic acid (IAAsp) and indole-3-acetyl glutamic acid (IAGlu) by Group II of the GRETCHEN HAGEN3 (GH3) family of acyl amido synthetases. Dioxygenase for auxin oxidation (DAO) irreversibly oxidizes IAA to oxindole-3-acetic acid (oxIAA) and, in turn, oxIAA can be further glucosylated to oxindole-3-acetyl-1-glucosyl ester (oxIAGlc) by UGTs. These metabolic pathways have been identified based on mutant analyses, in vitro activity measurements, and in planta feeding assays. In vitro assays for studying protein activity are based on producing Arabidopsis enzymes in a recombinant form in bacteria or yeast followed by recombinant protein purification. However, the need to extract and purify the recombinant proteins represents a major obstacle when performing in vitro assays. Results In this work we report a rapid, reproducible and cheap method to screen the enzymatic activity of recombinant proteins that are known to inactivate IAA. The enzymatic reactions are carried out directly in bacteria that produce the recombinant protein. The enzymatic products can be measured by direct injection of a small supernatant fraction from the bacterial culture on ultrahigh-performance liquid chromatography coupled to electrospray ionization tandem spectrometry (UHPLC–ESI-MS/MS). Experimental procedures were optimized for testing the activity of different classes of IAA-modifying enzymes without the need to purify recombinant protein. Conclusions This new method represents an alternative to existing in vitro assays. It can be applied to the analysis of IAA metabolites that are produced upon supplementation of substrate to engineered bacterial cultures and can be used for a rapid screening of orthologous candidate genes from non-model species.

@article{lee_crispr-based_2019,
	title = {{CRISPR}-based tools for targeted transcriptional and epigenetic regulation in plants},
	volume = {14},
	issn = {1932-6203},
	url = {https://dx.plos.org/10.1371/journal.pone.0222778},
	doi = {10.1371/journal.pone.0222778},
	language = {en},
	number = {9},
	urldate = {2021-06-07},
	journal = {PLOS ONE},
	author = {Lee, Joanne E. and Neumann, Manuela and Duro, Daniel Iglesias and Schmid, Markus},
	editor = {Candela, Hector},
	month = sep,
	year = {2019},
	pages = {e0222778},
}

@article{collani_ft_2019,
	title = {{FT} {Modulates} {Genome}-{Wide} {DNA}-{Binding} of the {bZIP} {Transcription} {Factor} {FD}},
	volume = {180},
	issn = {0032-0889, 1532-2548},
	url = {https://academic.oup.com/plphys/article/180/1/367-380/6117581},
	doi = {10/gjdxbs},
	language = {en},
	number = {1},
	urldate = {2021-06-07},
	journal = {Plant Physiology},
	author = {Collani, Silvio and Neumann, Manuela and Yant, Levi and Schmid, Markus},
	month = may,
	year = {2019},
	pages = {367--380},
}

@article{you_phloem_2019,
	title = {Phloem {Companion} {Cell}-{Specific} {Transcriptomic} and {Epigenomic} {Analyses} {Identify} {MRF1}, a {Regulator} of {Flowering}},
	volume = {31},
	issn = {1040-4651, 1532-298X},
	url = {https://academic.oup.com/plcell/article/31/2/325-345/5985421},
	doi = {10/gjdw33},
	language = {en},
	number = {2},
	urldate = {2021-06-07},
	journal = {The Plant Cell},
	author = {You, Yuan and Sawikowska, Aneta and Lee, Joanne E. and Benstein, Ruben M. and Neumann, Manuela and Krajewski, Paweł and Schmid, Markus},
	month = feb,
	year = {2019},
	pages = {325--345},
}

@article{speth_arabidopsis_2018,
	title = {Arabidopsis {RNA} processing factor {SERRATE} regulates the transcription of intronless genes},
	volume = {7},
	issn = {2050-084X},
	url = {https://elifesciences.org/articles/37078},
	doi = {10/gd7w68},
	abstract = {Intron splicing increases proteome complexity, promotes RNA stability, and enhances transcription. However, introns and the concomitant need for splicing extend the time required for gene expression and can cause an undesirable delay in the activation of genes. Here, we show that the plant microRNA processing factor SERRATE (SE) plays an unexpected and pivotal role in the regulation of intronless genes. Arabidopsis SE associated with more than 1000, mainly intronless, genes in a transcription-dependent manner. Chromatin-bound SE liaised with paused and elongating polymerase II complexes and promoted their association with intronless target genes. Our results indicate that stress-responsive genes contain no or few introns, which negatively affects their expression strength, but that some genes circumvent this limitation via a novel SE-dependent transcriptional activation mechanism. Transcriptome analysis of a Drosophila mutant defective in ARS2, the metazoan homologue of SE, suggests that SE/ARS2 function in regulating intronless genes might be conserved across kingdoms.},
	language = {en},
	urldate = {2021-06-07},
	journal = {eLife},
	author = {Speth, Corinna and Szabo, Emese Xochitl and Martinho, Claudia and Collani, Silvio and zur Oven-Krockhaus, Sven and Richter, Sandra and Droste-Borel, Irina and Macek, Boris and Stierhof, York-Dieter and Schmid, Markus and Liu, Chang and Laubinger, Sascha},
	month = aug,
	year = {2018},
	pages = {e37078},
}

Intron splicing increases proteome complexity, promotes RNA stability, and enhances transcription. However, introns and the concomitant need for splicing extend the time required for gene expression and can cause an undesirable delay in the activation of genes. Here, we show that the plant microRNA processing factor SERRATE (SE) plays an unexpected and pivotal role in the regulation of intronless genes. Arabidopsis SE associated with more than 1000, mainly intronless, genes in a transcription-dependent manner. Chromatin-bound SE liaised with paused and elongating polymerase II complexes and promoted their association with intronless target genes. Our results indicate that stress-responsive genes contain no or few introns, which negatively affects their expression strength, but that some genes circumvent this limitation via a novel SE-dependent transcriptional activation mechanism. Transcriptome analysis of a Drosophila mutant defective in ARS2, the metazoan homologue of SE, suggests that SE/ARS2 function in regulating intronless genes might be conserved across kingdoms.

@article{capovilla_porcupine_2018,
	title = {{PORCUPINE} regulates development in response to temperature through alternative splicing},
	volume = {4},
	issn = {2055-0278},
	url = {http://www.nature.com/articles/s41477-018-0176-z},
	doi = {10/gd9hnk},
	language = {en},
	number = {8},
	urldate = {2021-06-07},
	journal = {Nature Plants},
	author = {Capovilla, Giovanna and Delhomme, Nicolas and Collani, Silvio and Shutava, Iryna and Bezrukov, Ilja and Symeonidi, Efthymia and de Francisco Amorim, Marcella and Laubinger, Sascha and Schmid, Markus},
	month = aug,
	year = {2018},
	pages = {534--539},
}

@incollection{gietl_ricinosomes_2018,
	title = {Ricinosomes and {Aleurain}-{Containing} {Vacuoles} ({ACVs}): {Protease}-{Storing} {Organelles}},
	isbn = {978-1-119-31299-4},
	shorttitle = {Ricinosomes and {Aleurain}-{Containing} {Vacuoles} ({ACVs})},
	url = {https://onlinelibrary.wiley.com/doi/abs/10.1002/9781119312994.apr0039},
	abstract = {The sections in this article are},
	language = {en},
	urldate = {2021-10-22},
	booktitle = {Annual {Plant} {Reviews} online},
	publisher = {American Cancer Society},
	author = {Gietl, Christine and Schmid, Markus and Simpson, David},
	year = {2018},
	doi = {10.1002/9781119312994.apr0039},
	note = {Section: 5
\_eprint: https://onlinelibrary.wiley.com/doi/pdf/10.1002/9781119312994.apr0039},
	keywords = {Aleurone cell, aleurain-containing vacuoles, cotyledons, cysteine endopeptidase, endosperm, programmed cell death, ricinosomes},
	pages = {96--118},
}

The sections in this article are

@article{shanks_role_2018,
	title = {Role of \textit{{BASIC} {PENTACYSTEINE}} transcription factors in a subset of cytokinin signaling responses},
	volume = {95},
	issn = {09607412},
	url = {http://doi.wiley.com/10.1111/tpj.13962},
	doi = {10/gdqkns},
	language = {en},
	number = {3},
	urldate = {2021-06-07},
	journal = {The Plant Journal},
	author = {Shanks, Carly M. and Hecker, Andreas and Cheng, Chia-Yi and Brand, Luise and Collani, Silvio and Schmid, Markus and Schaller, G. Eric and Wanke, Dierk and Harter, Klaus and Kieber, Joseph J.},
	month = aug,
	year = {2018},
	pages = {458--473},
}

@article{prat_wrky23_2018,
	title = {{WRKY23} is a component of the transcriptional network mediating auxin feedback on {PIN} polarity},
	volume = {14},
	issn = {1553-7404},
	url = {https://dx.plos.org/10.1371/journal.pgen.1007177},
	doi = {10.1371/journal.pgen.1007177},
	language = {en},
	number = {1},
	urldate = {2021-06-07},
	journal = {PLOS Genetics},
	author = {Prát, Tomáš and Hajný, Jakub and Grunewald, Wim and Vasileva, Mina and Molnár, Gergely and Tejos, Ricardo and Schmid, Markus and Sauer, Michael and Friml, Jiří},
	editor = {Strader, Lucia},
	month = jan,
	year = {2018},
	pages = {e1007177},
}

@article{conn_circrna_2017,
	title = {A {circRNA} from {SEPALLATA3} regulates splicing of its cognate {mRNA} through {R}-loop formation},
	volume = {3},
	issn = {2055-0278},
	url = {http://www.nature.com/articles/nplants201753},
	doi = {10.1038/nplants.2017.53},
	language = {en},
	number = {5},
	urldate = {2021-06-07},
	journal = {Nature Plants},
	author = {Conn, Vanessa M. and Hugouvieux, Véronique and Nayak, Aditya and Conos, Stephanie A. and Capovilla, Giovanna and Cildir, Gökhan and Jourdain, Agnès and Tergaonkar, Vinay and Schmid, Markus and Zubieta, Chloe and Conn, Simon J.},
	month = may,
	year = {2017},
	pages = {17053},
}

@article{capovilla_contribution_2017,
	title = {Contribution of major {FLM} isoforms to temperature-dependent flowering in {Arabidopsis} thaliana},
	volume = {68},
	issn = {0022-0957, 1460-2431},
	url = {https://academic.oup.com/jxb/article/68/18/5117/4210925},
	doi = {10/gcjrww},
	language = {en},
	number = {18},
	urldate = {2021-06-07},
	journal = {Journal of Experimental Botany},
	author = {Capovilla, Giovanna and Symeonidi, Efthymia and Wu, Rui and Schmid, Markus},
	month = nov,
	year = {2017},
	pages = {5117--5127},
}

@article{engelhorn_dynamics_2017,
	title = {Dynamics of {H3K4me3} {Chromatin} {Marks} {Prevails} over {H3K27me3} for {Gene} {Regulation} during {Flower} {Morphogenesis} in {Arabidopsis} thaliana},
	volume = {1},
	copyright = {http://creativecommons.org/licenses/by/3.0/},
	url = {https://www.mdpi.com/2075-4655/1/2/8},
	doi = {10.3390/epigenomes1020008},
	abstract = {Plant life-long organogenesis involves sequential, time and tissue specific expression of developmental genes. This requires activities of Polycomb Group (PcG) and trithorax Group complexes (trxG), respectively responsible for repressive Histone 3 trimethylation at lysine 27 (H3K27me3) and activation-related Histone 3 trimethylation at lysine 4 (H3K4me3). However, the genome-wide dynamics in histone modifications that occur during developmental processes have remained elusive. Here, we report the distributions of H3K27me3 and H3K4me3 along with expression changes, in a developmental series including Arabidopsis thaliana leaf and three stages of flower development. We found that chromatin mark levels are highly dynamic over the time series on nearly half of all Arabidopsis genes. Moreover, during early flower morphogenesis, changes in H3K4me3 prevail over changes in H3K27me3 and quantitatively correlate with expression changes, while H3K27me3 changes occur later. Notably, we found that H3K4me3 increase during the early activation of PcG target genes while H3K27me3 level remain relatively constant at the locus. Our results reveal that H3K4me3 predicts changes in gene expression better than H3K27me3, unveil unexpected chromatin mechanisms at gene activation and underline the relevance of tissue-specific temporal epigenomics.},
	language = {en},
	number = {2},
	urldate = {2021-10-22},
	journal = {Epigenomes},
	author = {Engelhorn, Julia and Blanvillain, Robert and Kröner, Christian and Parrinello, Hugues and Rohmer, Marine and Posé, David and Ott, Felix and Schmid, Markus and Carles, Cristel C.},
	month = sep,
	year = {2017},
	note = {Number: 2
Publisher: Multidisciplinary Digital Publishing Institute},
	keywords = {ChIP-seq, RNA-seq, chromatin and expression dynamics, differentiation, reproductive development},
	pages = {8},
}

Plant life-long organogenesis involves sequential, time and tissue specific expression of developmental genes. This requires activities of Polycomb Group (PcG) and trithorax Group complexes (trxG), respectively responsible for repressive Histone 3 trimethylation at lysine 27 (H3K27me3) and activation-related Histone 3 trimethylation at lysine 4 (H3K4me3). However, the genome-wide dynamics in histone modifications that occur during developmental processes have remained elusive. Here, we report the distributions of H3K27me3 and H3K4me3 along with expression changes, in a developmental series including Arabidopsis thaliana leaf and three stages of flower development. We found that chromatin mark levels are highly dynamic over the time series on nearly half of all Arabidopsis genes. Moreover, during early flower morphogenesis, changes in H3K4me3 prevail over changes in H3K27me3 and quantitatively correlate with expression changes, while H3K27me3 changes occur later. Notably, we found that H3K4me3 increase during the early activation of PcG target genes while H3K27me3 level remain relatively constant at the locus. Our results reveal that H3K4me3 predicts changes in gene expression better than H3K27me3, unveil unexpected chromatin mechanisms at gene activation and underline the relevance of tissue-specific temporal epigenomics.

@article{you_temporal_2017,
	title = {Temporal dynamics of gene expression and histone marks at the {Arabidopsis} shoot meristem during flowering},
	volume = {8},
	issn = {2041-1723},
	url = {http://www.nature.com/articles/ncomms15120},
	doi = {10.1038/ncomms15120},
	language = {en},
	number = {1},
	urldate = {2021-06-07},
	journal = {Nature Communications},
	author = {You, Yuan and Sawikowska, Aneta and Neumann, Manuela and Posé, David and Capovilla, Giovanna and Langenecker, Tobias and Neher, Richard A. and Krajewski, Paweł and Schmid, Markus},
	month = aug,
	year = {2017},
	pages = {15120},
}

@article{sayou_sam_2016,
	title = {A {SAM} oligomerization domain shapes the genomic binding landscape of the {LEAFY} transcription factor},
	volume = {7},
	issn = {2041-1723},
	url = {http://www.nature.com/articles/ncomms11222},
	doi = {10/f3tdv9},
	language = {en},
	number = {1},
	urldate = {2021-06-07},
	journal = {Nature Communications},
	author = {Sayou, Camille and Nanao, Max H. and Jamin, Marc and Posé, David and Thévenon, Emmanuel and Grégoire, Laura and Tichtinsky, Gabrielle and Denay, Grégoire and Ott, Felix and Peirats Llobet, Marta and Schmid, Markus and Dumas, Renaud and Parcy, François},
	month = sep,
	year = {2016},
	pages = {11222},
}

@article{pfeiffer_integration_2016,
	title = {Integration of light and metabolic signals for stem cell activation at the shoot apical meristem},
	volume = {5},
	issn = {2050-084X},
	url = {https://elifesciences.org/articles/17023},
	doi = {10/f3r4bk},
	abstract = {A major feature of embryogenesis is the specification of stem cell systems, but in contrast to the situation in most animals, plant stem cells remain quiescent until the postembryonic phase of development. Here, we dissect how light and metabolic signals are integrated to overcome stem cell dormancy at the shoot apical meristem. We show on the one hand that light is able to activate expression of the stem cell inducer WUSCHEL independently of photosynthesis and that this likely involves inter-regional cytokinin signaling. Metabolic signals, on the other hand, are transduced to the meristem through activation of the TARGET OF RAPAMYCIN (TOR) kinase. Surprisingly, TOR is also required for light signal dependent stem cell activation. Thus, the TOR kinase acts as a central integrator of light and metabolic signals and a key regulator of stem cell activation at the shoot apex.
          , 
            Plants are able to grow and develop throughout their lives thanks to groups of stem cells at the tips of their shoots and roots, which can constantly divide to produce new cells. Energy captured from sunlight during a process called photosynthesis is the main source of energy for most plants. Therefore, the amount and quality of light in the environment has a big influence on how plants grow and develop. An enzyme called TOR kinase can sense energy levels in animal cells and regulate many processes including growth and cell division. Plants also have a TOR kinase, but it is less clear if it plays the same role in plants, and whether it can respond to light.
            Plant stem cells only start to divide after the seed germinates. In shoots, a protein called WUSCHEL is required to maintain stem cells in an active state. Here, Pfeiffer et al. studied how shoot stem cells are activated in response to environmental signals in a plant known as Arabidopsis. The experiments show that light is able to activate the production of WUSCHEL independently of photosynthesis via a signal pathway that depends on TOR kinase. The stem cells do not directly sense light; instead other cells detect the light and relay the information to the stem cells with the help of a hormone called cytokinin.
            Further experiments show that information about energy levels in cells is relayed via another signal pathway that also involves the TOR kinase. Therefore, Pfeiffer et al.’s findings suggest that the activation of TOR by light allows plant cells to anticipate how much energy will be available and efficiently tune their growth and development to cope with the environmental conditions. Future challenges are to understand how TOR kinase is regulated by light signals and how this enzyme is able to act on WUSCHEL to trigger stem cell division.},
	language = {en},
	urldate = {2021-06-07},
	journal = {eLife},
	author = {Pfeiffer, Anne and Janocha, Denis and Dong, Yihan and Medzihradszky, Anna and Schöne, Stefanie and Daum, Gabor and Suzaki, Takuya and Forner, Joachim and Langenecker, Tobias and Rempel, Eugen and Schmid, Markus and Wirtz, Markus and Hell, Rüdiger and Lohmann, Jan U},
	month = jul,
	year = {2016},
	pages = {e17023},
}

A major feature of embryogenesis is the specification of stem cell systems, but in contrast to the situation in most animals, plant stem cells remain quiescent until the postembryonic phase of development. Here, we dissect how light and metabolic signals are integrated to overcome stem cell dormancy at the shoot apical meristem. We show on the one hand that light is able to activate expression of the stem cell inducer WUSCHEL independently of photosynthesis and that this likely involves inter-regional cytokinin signaling. Metabolic signals, on the other hand, are transduced to the meristem through activation of the TARGET OF RAPAMYCIN (TOR) kinase. Surprisingly, TOR is also required for light signal dependent stem cell activation. Thus, the TOR kinase acts as a central integrator of light and metabolic signals and a key regulator of stem cell activation at the shoot apex. , Plants are able to grow and develop throughout their lives thanks to groups of stem cells at the tips of their shoots and roots, which can constantly divide to produce new cells. Energy captured from sunlight during a process called photosynthesis is the main source of energy for most plants. Therefore, the amount and quality of light in the environment has a big influence on how plants grow and develop. An enzyme called TOR kinase can sense energy levels in animal cells and regulate many processes including growth and cell division. Plants also have a TOR kinase, but it is less clear if it plays the same role in plants, and whether it can respond to light. Plant stem cells only start to divide after the seed germinates. In shoots, a protein called WUSCHEL is required to maintain stem cells in an active state. Here, Pfeiffer et al. studied how shoot stem cells are activated in response to environmental signals in a plant known as Arabidopsis. The experiments show that light is able to activate the production of WUSCHEL independently of photosynthesis via a signal pathway that depends on TOR kinase. The stem cells do not directly sense light; instead other cells detect the light and relay the information to the stem cells with the help of a hormone called cytokinin. Further experiments show that information about energy levels in cells is relayed via another signal pathway that also involves the TOR kinase. Therefore, Pfeiffer et al.’s findings suggest that the activation of TOR by light allows plant cells to anticipate how much energy will be available and efficiently tune their growth and development to cope with the environmental conditions. Future challenges are to understand how TOR kinase is regulated by light signals and how this enzyme is able to act on WUSCHEL to trigger stem cell division.

@article{leal_valentim_quantitative_2015,
	title = {A quantitative and dynamic model of the {Arabidopsis} flowering time gene regulatory network},
	volume = {10},
	issn = {1932-6203 (Electronic) 1932-6203 (Linking)},
	url = {https://www.ncbi.nlm.nih.gov/pubmed/25719734},
	doi = {10.1371/journal.pone.0116973},
	abstract = {Various environmental signals integrate into a network of floral regulatory genes leading to the final decision on when to flower. Although a wealth of qualitative knowledge is available on how flowering time genes regulate each other, only a few studies incorporated this knowledge into predictive models. Such models are invaluable as they enable to investigate how various types of inputs are combined to give a quantitative readout. To investigate the effect of gene expression disturbances on flowering time, we developed a dynamic model for the regulation of flowering time in Arabidopsis thaliana. Model parameters were estimated based on expression time-courses for relevant genes, and a consistent set of flowering times for plants of various genetic backgrounds. Validation was performed by predicting changes in expression level in mutant backgrounds and comparing these predictions with independent expression data, and by comparison of predicted and experimental flowering times for several double mutants. Remarkably, the model predicts that a disturbance in a particular gene has not necessarily the largest impact on directly connected genes. For example, the model predicts that SUPPRESSOR OF OVEREXPRESSION OF CONSTANS (SOC1) mutation has a larger impact on APETALA1 (AP1), which is not directly regulated by SOC1, compared to its effect on LEAFY (LFY) which is under direct control of SOC1. This was confirmed by expression data. Another model prediction involves the importance of cooperativity in the regulation of APETALA1 (AP1) by LFY, a prediction supported by experimental evidence. Concluding, our model for flowering time gene regulation enables to address how different quantitative inputs are combined into one quantitative output, flowering time.},
	language = {eng},
	number = {2},
	journal = {PLoS One},
	author = {Leal Valentim, F. and Mourik, Sv and Pose, D. and Kim, M. C. and Schmid, M. and van Ham, R. C. and Busscher, M. and Sanchez-Perez, G. F. and Molenaar, J. and Angenent, G. C. and Immink, R. G. and van Dijk, A. D.},
	year = {2015},
	note = {Edition: 2015/02/27},
	keywords = {*Gene Expression Regulation, Plant, *Gene Regulatory Networks, Arabidopsis, Arabidopsis Proteins, Arabidopsis Proteins/genetics/metabolism, Arabidopsis/*genetics/growth \& development, Flowers, Flowers/*genetics/growth \& development, Gene Expression Regulation, Plant, Gene Regulatory Networks, MADS Domain Proteins, MADS Domain Proteins/genetics/metabolism, Models, Genetic, Transcription Factors, Transcription Factors/genetics/metabolism},
	pages = {e0116973},
}

Various environmental signals integrate into a network of floral regulatory genes leading to the final decision on when to flower. Although a wealth of qualitative knowledge is available on how flowering time genes regulate each other, only a few studies incorporated this knowledge into predictive models. Such models are invaluable as they enable to investigate how various types of inputs are combined to give a quantitative readout. To investigate the effect of gene expression disturbances on flowering time, we developed a dynamic model for the regulation of flowering time in Arabidopsis thaliana. Model parameters were estimated based on expression time-courses for relevant genes, and a consistent set of flowering times for plants of various genetic backgrounds. Validation was performed by predicting changes in expression level in mutant backgrounds and comparing these predictions with independent expression data, and by comparison of predicted and experimental flowering times for several double mutants. Remarkably, the model predicts that a disturbance in a particular gene has not necessarily the largest impact on directly connected genes. For example, the model predicts that SUPPRESSOR OF OVEREXPRESSION OF CONSTANS (SOC1) mutation has a larger impact on APETALA1 (AP1), which is not directly regulated by SOC1, compared to its effect on LEAFY (LFY) which is under direct control of SOC1. This was confirmed by expression data. Another model prediction involves the importance of cooperativity in the regulation of APETALA1 (AP1) by LFY, a prediction supported by experimental evidence. Concluding, our model for flowering time gene regulation enables to address how different quantitative inputs are combined into one quantitative output, flowering time.

@article{capovilla_control_2015,
	title = {Control of flowering by ambient temperature},
	volume = {66},
	issn = {1460-2431 (Electronic) 0022-0957 (Linking)},
	url = {https://www.ncbi.nlm.nih.gov/pubmed/25326628},
	doi = {10.1093/jxb/eru416},
	abstract = {The timing of flowering is a crucial decision in the life cycle of plants since favourable conditions are needed to maximize reproductive success and, hence, the survival of the species. It is therefore not surprising that plants constantly monitor endogenous and environmental signals, such as day length (photoperiod) and temperature, to adjust the timing of the floral transition. Temperature in particular has been shown to have a tremendous effect on the timing of flowering: the effect of prolonged periods of cold, called the vernalization response, has been extensively studied and the underlying epigenetic mechanisms are reasonably well understood in Arabidopsis thaliana. In contrast, the effect of moderate changes in ambient growth temperature on the progression of flowering, the thermosensory pathway, is only starting to be understood on the molecular level. Several genes and molecular mechanisms underlying the thermosensory pathway have already been identified and characterized in detail. At a time when global temperature is rising due to climate change, this knowledge will be pivotal to ensure crop production in the future.},
	language = {eng},
	number = {1},
	journal = {J Exp Bot},
	author = {Capovilla, G. and Schmid, M. and Pose, D.},
	month = jan,
	year = {2015},
	note = {Edition: 2014/10/19},
	keywords = {*Plant Development/genetics, *Temperature, Ambient temperature, Arabidopsis, Arabidopsis thaliana, Arabidopsis/genetics/growth \& development, Epigenesis, Genetic, Flowers, Flowers/genetics/*growth \& development, MADS, Mads, Plant Development, Temperature, flowering time, miRNA, thermosensory pathway.},
	pages = {59--69},
}

The timing of flowering is a crucial decision in the life cycle of plants since favourable conditions are needed to maximize reproductive success and, hence, the survival of the species. It is therefore not surprising that plants constantly monitor endogenous and environmental signals, such as day length (photoperiod) and temperature, to adjust the timing of the floral transition. Temperature in particular has been shown to have a tremendous effect on the timing of flowering: the effect of prolonged periods of cold, called the vernalization response, has been extensively studied and the underlying epigenetic mechanisms are reasonably well understood in Arabidopsis thaliana. In contrast, the effect of moderate changes in ambient growth temperature on the progression of flowering, the thermosensory pathway, is only starting to be understood on the molecular level. Several genes and molecular mechanisms underlying the thermosensory pathway have already been identified and characterized in detail. At a time when global temperature is rising due to climate change, this knowledge will be pivotal to ensure crop production in the future.

@article{galvao_gibberellic_2015,
	title = {Gibberellic acid signaling is required for ambient temperature-mediated induction of flowering in {Arabidopsis} thaliana},
	volume = {84},
	issn = {1365-313X (Electronic) 0960-7412 (Linking)},
	url = {https://www.ncbi.nlm.nih.gov/pubmed/26466761},
	doi = {10.1111/tpj.13051},
	abstract = {Distinct molecular mechanisms integrate changes in ambient temperature into the genetic pathways that govern flowering time in Arabidopsis thaliana. Temperature-dependent eviction of the histone variant H2A.Z from nucleosomes has been suggested to facilitate the expression of FT by PIF4 at elevated ambient temperatures. Here we show that, in addition to PIF4, PIF3 and PIF5, but not PIF1 and PIF6, can promote flowering when expressed specifically in phloem companion cells (PCC), where they can induce FT and its close paralog, TSF. However, despite their strong potential to promote flowering, genetic analyses suggest that the PIF genes seem to have only a minor role in adjusting flowering in response to photoperiod or high ambient temperature. In addition, loss of PIF function only partially suppressed the early flowering phenotype and FT expression of the arp6 mutant, which is defective in H2A.Z deposition. In contrast, the chemical inhibition of gibberellic acid (GA) biosynthesis resulted in a strong attenuation of early flowering and FT expression in arp6. Furthermore, GA was able to induce flowering at low temperature (15 degrees C) independently of FT, TSF, and the PIF genes, probably directly at the shoot apical meristem. Together, our results suggest that the timing of the floral transition in response to ambient temperature is more complex than previously thought and that GA signaling might play a crucial role in this process.},
	language = {en},
	number = {5},
	urldate = {2021-06-07},
	journal = {Plant J},
	author = {Galvao, V. C. and Collani, S. and Horrer, D. and Schmid, M.},
	month = dec,
	year = {2015},
	note = {Edition: 2015/10/16},
	keywords = {Arabidopsis Proteins/genetics/metabolism/physiology, Arabidopsis thaliana, Arabidopsis/genetics/*growth \& development/metabolism, Arp6, Basic Helix-Loop-Helix Transcription Factors/genetics/metabolism/physiology, Flm, Flowers/genetics/growth \& development/metabolism, Ft, Gibberellins/*metabolism/pharmacology, H2a.Z, Histones/metabolism, Microfilament Proteins/genetics/metabolism/physiology, Nucleosomes/metabolism, Phosphatidylethanolamine Binding Protein/genetics/metabolism/physiology, Photoperiod, Pif, Plant Growth Regulators/*metabolism/pharmacology, Signal Transduction, Svp, Temperature, ambient temperature, flowering, gibberellin},
	pages = {949--62},
}

Distinct molecular mechanisms integrate changes in ambient temperature into the genetic pathways that govern flowering time in Arabidopsis thaliana. Temperature-dependent eviction of the histone variant H2A.Z from nucleosomes has been suggested to facilitate the expression of FT by PIF4 at elevated ambient temperatures. Here we show that, in addition to PIF4, PIF3 and PIF5, but not PIF1 and PIF6, can promote flowering when expressed specifically in phloem companion cells (PCC), where they can induce FT and its close paralog, TSF. However, despite their strong potential to promote flowering, genetic analyses suggest that the PIF genes seem to have only a minor role in adjusting flowering in response to photoperiod or high ambient temperature. In addition, loss of PIF function only partially suppressed the early flowering phenotype and FT expression of the arp6 mutant, which is defective in H2A.Z deposition. In contrast, the chemical inhibition of gibberellic acid (GA) biosynthesis resulted in a strong attenuation of early flowering and FT expression in arp6. Furthermore, GA was able to induce flowering at low temperature (15 degrees C) independently of FT, TSF, and the PIF genes, probably directly at the shoot apical meristem. Together, our results suggest that the timing of the floral transition in response to ambient temperature is more complex than previously thought and that GA signaling might play a crucial role in this process.

@article{lutz_modulation_2015,
	title = {Modulation of {Ambient} {Temperature}-{Dependent} {Flowering} in {Arabidopsis} thaliana by {Natural} {Variation} of {FLOWERING} {LOCUS} {M}},
	volume = {11},
	issn = {1553-7404},
	url = {https://journals.plos.org/plosgenetics/article?id=10.1371/journal.pgen.1005588},
	doi = {10.1371/journal.pgen.1005588},
	abstract = {Plants integrate seasonal cues such as temperature and day length to optimally adjust their flowering time to the environment. Compared to the control of flowering before and after winter by the vernalization and day length pathways, mechanisms that delay or promote flowering during a transient cool or warm period, especially during spring, are less well understood. Due to global warming, understanding this ambient temperature pathway has gained increasing importance. In Arabidopsis thaliana, FLOWERING LOCUS M (FLM) is a critical flowering regulator of the ambient temperature pathway. FLM is alternatively spliced in a temperature-dependent manner and the two predominant splice variants, FLM-ß and FLM-δ, can repress and activate flowering in the genetic background of the A. thaliana reference accession Columbia-0. The relevance of this regulatory mechanism for the environmental adaptation across the entire range of the species is, however, unknown. Here, we identify insertion polymorphisms in the first intron of FLM as causative for accelerated flowering in many natural A. thaliana accessions, especially in cool (15°C) temperatures. We present evidence for a potential adaptive role of this structural variation and link it specifically to changes in the abundance of FLM-ß. Our results may allow predicting flowering in response to ambient temperatures in the Brassicaceae.},
	language = {en},
	number = {10},
	urldate = {2021-10-22},
	journal = {PLOS Genetics},
	author = {Lutz, Ulrich and Posé, David and Pfeifer, Matthias and Gundlach, Heidrun and Hagmann, Jörg and Wang, Congmao and Weigel, Detlef and Mayer, Klaus F. X. and Schmid, Markus and Schwechheimer, Claus},
	year = {2015},
	note = {Publisher: Public Library of Science},
	keywords = {Arabidopsis thaliana, Flowering plants, Gene expression, Genetic loci, Genomics, Introns, Plant genomics, Polymerase chain reaction},
	pages = {e1005588},
}

Plants integrate seasonal cues such as temperature and day length to optimally adjust their flowering time to the environment. Compared to the control of flowering before and after winter by the vernalization and day length pathways, mechanisms that delay or promote flowering during a transient cool or warm period, especially during spring, are less well understood. Due to global warming, understanding this ambient temperature pathway has gained increasing importance. In Arabidopsis thaliana, FLOWERING LOCUS M (FLM) is a critical flowering regulator of the ambient temperature pathway. FLM is alternatively spliced in a temperature-dependent manner and the two predominant splice variants, FLM-ß and FLM-δ, can repress and activate flowering in the genetic background of the A. thaliana reference accession Columbia-0. The relevance of this regulatory mechanism for the environmental adaptation across the entire range of the species is, however, unknown. Here, we identify insertion polymorphisms in the first intron of FLM as causative for accelerated flowering in many natural A. thaliana accessions, especially in cool (15°C) temperatures. We present evidence for a potential adaptive role of this structural variation and link it specifically to changes in the abundance of FLM-ß. Our results may allow predicting flowering in response to ambient temperatures in the Brassicaceae.

@article{slane_profiling_2015,
	title = {Profiling of embryonic nuclear vs. cellular {RNA} in {Arabidopsis} thaliana},
	volume = {4},
	issn = {2213-5960},
	doi = {10.1016/j.gdata.2015.03.015},
	abstract = {In Arabidopsis, various cell type-specific whole-genome expression analyses have been conducted. However, the vast majority of these were performed with cellular RNA from root tissues or other easily accessible cell types [1]. Nuclear RNA was neglected for a long time as not being representative for transcriptomic studies. In recent years, however, there have been reports describing the validity of nuclear RNA for these types of studies [2,3]. Here we describe the generation, quality assessment and analysis of nuclear transcriptomic data from Arabidopsis embryos published by Slane et al. (2014) [4]. Comparison of nuclear with cellular gene expression demonstrated the usefulness of nuclear transcriptomics.},
	language = {eng},
	journal = {Genomics Data},
	author = {Slane, Daniel and Kong, Jixiang and Schmid, Markus and Jürgens, Gerd and Bayer, Martin},
	month = jun,
	year = {2015},
	pmid = {26484189},
	pmcid = {PMC4536148},
	keywords = {Arabidopsis thaliana, Gene expression, Microarray, Nuclear and cellular transcriptome, Pro-embryo and suspensor transcriptome},
	pages = {96--98},
}

In Arabidopsis, various cell type-specific whole-genome expression analyses have been conducted. However, the vast majority of these were performed with cellular RNA from root tissues or other easily accessible cell types [1]. Nuclear RNA was neglected for a long time as not being representative for transcriptomic studies. In recent years, however, there have been reports describing the validity of nuclear RNA for these types of studies [2,3]. Here we describe the generation, quality assessment and analysis of nuclear transcriptomic data from Arabidopsis embryos published by Slane et al. (2014) [4]. Comparison of nuclear with cellular gene expression demonstrated the usefulness of nuclear transcriptomics.

@article{capovilla_role_2015,
	title = {Role of alternative pre-{mRNA} splicing in temperature signaling},
	volume = {27},
	issn = {1879-0356 (Electronic) 1369-5266 (Linking)},
	url = {https://www.ncbi.nlm.nih.gov/pubmed/26190743},
	doi = {10/f3ndbf},
	abstract = {Developmental plasticity enables plants to respond rapidly to changing environmental conditions, such as temperature fluctuations. Understanding how plants measure temperature and integrate this information into developmental programs at the molecular level will be essential to breed thermo-tolerant crop varieties. Recent studies identified alternative splicing (AS) as a possible 'molecular thermometer', allowing plants to quickly adjust the abundance of functional transcripts to environmental perturbations. In this review, recent advances regarding the effects of temperature-responsive AS on plant development will be discussed, with emphasis on the circadian clock and flowering time control. The challenge for the near future will be to understand the molecular mechanisms by which temperature can influence AS regulation.},
	language = {en},
	urldate = {2021-06-07},
	journal = {Curr Opin Plant Biol},
	author = {Capovilla, G. and Pajoro, A. and Immink, R. G. and Schmid, M.},
	month = oct,
	year = {2015},
	note = {Edition: 2015/07/21},
	keywords = {*Alternative Splicing, *Gene Expression Regulation, Plant, *Genes, Regulator, *Plant Development, Circadian Clocks, Flowers/genetics/growth \& development, Plant Proteins/*genetics/metabolism, Temperature},
	pages = {97--103},
}

Developmental plasticity enables plants to respond rapidly to changing environmental conditions, such as temperature fluctuations. Understanding how plants measure temperature and integrate this information into developmental programs at the molecular level will be essential to breed thermo-tolerant crop varieties. Recent studies identified alternative splicing (AS) as a possible 'molecular thermometer', allowing plants to quickly adjust the abundance of functional transcripts to environmental perturbations. In this review, recent advances regarding the effects of temperature-responsive AS on plant development will be discussed, with emphasis on the circadian clock and flowering time control. The challenge for the near future will be to understand the molecular mechanisms by which temperature can influence AS regulation.

@article{slane_cell_2014,
	title = {Cell type-specific transcriptome analysis in the early {Arabidopsis} thaliana embryo},
	volume = {141},
	issn = {1477-9129},
	doi = {10/f6s68v},
	abstract = {In multicellular organisms, cellular differences in gene activity are a prerequisite for differentiation and establishment of cell types. In order to study transcriptome profiles, specific cell types have to be isolated from a given tissue or even the whole organism. However, whole-transcriptome analysis of early embryos in flowering plants has been hampered by their size and inaccessibility. Here, we describe the purification of nuclear RNA from early stage Arabidopsis thaliana embryos using fluorescence-activated nuclear sorting (FANS) to generate expression profiles of early stages of the whole embryo, the proembryo and the suspensor. We validated our datasets of differentially expressed candidate genes by promoter-reporter gene fusions and in situ hybridization. Our study revealed that different classes of genes with respect to biological processes and molecular functions are preferentially expressed either in the proembryo or in the suspensor. This method can be used especially for tissues with a limited cell population and inaccessible tissue types. Furthermore, we provide a valuable resource for research on Arabidopsis early embryogenesis.},
	language = {eng},
	number = {24},
	journal = {Development (Cambridge, England)},
	author = {Slane, Daniel and Kong, Jixiang and Berendzen, Kenneth W. and Kilian, Joachim and Henschen, Agnes and Kolb, Martina and Schmid, Markus and Harter, Klaus and Mayer, Ulrike and De Smet, Ive and Bayer, Martin and Jürgens, Gerd},
	month = dec,
	year = {2014},
	pmid = {25411212},
	keywords = {Arabidopsis, Cell Nucleus, Cloning, Molecular, Fluorescence-activated nuclear sorting, Gene Expression Profiling, Genotype, In Situ Hybridization, Microarray Analysis, Microscopy, Fluorescence, Proembryo, RNA, Nuclear, Real-Time Polymerase Chain Reaction, Seeds, Suspensor, Transcriptome analysis},
	pages = {4831--4840},
}

In multicellular organisms, cellular differences in gene activity are a prerequisite for differentiation and establishment of cell types. In order to study transcriptome profiles, specific cell types have to be isolated from a given tissue or even the whole organism. However, whole-transcriptome analysis of early embryos in flowering plants has been hampered by their size and inaccessibility. Here, we describe the purification of nuclear RNA from early stage Arabidopsis thaliana embryos using fluorescence-activated nuclear sorting (FANS) to generate expression profiles of early stages of the whole embryo, the proembryo and the suspensor. We validated our datasets of differentially expressed candidate genes by promoter-reporter gene fusions and in situ hybridization. Our study revealed that different classes of genes with respect to biological processes and molecular functions are preferentially expressed either in the proembryo or in the suspensor. This method can be used especially for tissues with a limited cell population and inaccessible tissue types. Furthermore, we provide a valuable resource for research on Arabidopsis early embryogenesis.

@article{zhurov_reciprocal_2014,
	title = {Reciprocal responses in the interaction between {Arabidopsis} and the cell-content-feeding chelicerate herbivore spider mite},
	volume = {164},
	issn = {1532-2548},
	doi = {10/f5m96t},
	abstract = {Most molecular-genetic studies of plant defense responses to arthropod herbivores have focused on insects. However, plant-feeding mites are also pests of diverse plants, and mites induce different patterns of damage to plant tissues than do well-studied insects (e.g. lepidopteran larvae or aphids). The two-spotted spider mite (Tetranychus urticae) is among the most significant mite pests in agriculture, feeding on a staggering number of plant hosts. To understand the interactions between spider mite and a plant at the molecular level, we examined reciprocal genome-wide responses of mites and its host Arabidopsis (Arabidopsis thaliana). Despite differences in feeding guilds, we found that transcriptional responses of Arabidopsis to mite herbivory resembled those observed for lepidopteran herbivores. Mutant analysis of induced plant defense pathways showed functionally that only a subset of induced programs, including jasmonic acid signaling and biosynthesis of indole glucosinolates, are central to Arabidopsis's defense to mite herbivory. On the herbivore side, indole glucosinolates dramatically increased mite mortality and development times. We identified an indole glucosinolate dose-dependent increase in the number of differentially expressed mite genes belonging to pathways associated with detoxification of xenobiotics. This demonstrates that spider mite is sensitive to Arabidopsis defenses that have also been associated with the deterrence of insect herbivores that are very distantly related to chelicerates. Our findings provide molecular insights into the nature of, and response to, herbivory for a representative of a major class of arthropod herbivores.},
	language = {eng},
	number = {1},
	journal = {Plant Physiology},
	author = {Zhurov, Vladimir and Navarro, Marie and Bruinsma, Kristie A. and Arbona, Vicent and Santamaria, M. Estrella and Cazaux, Marc and Wybouw, Nicky and Osborne, Edward J. and Ens, Cherise and Rioja, Cristina and Vermeirssen, Vanessa and Rubio-Somoza, Ignacio and Krishna, Priti and Diaz, Isabel and Schmid, Markus and Gómez-Cadenas, Aurelio and Van de Peer, Yves and Grbic, Miodrag and Clark, Richard M. and Van Leeuwen, Thomas and Grbic, Vojislava},
	month = jan,
	year = {2014},
	pmid = {24285850},
	pmcid = {PMC3875816},
	keywords = {Animals, Arabidopsis, Cyclopentanes, Female, Gene Expression Profiling, Gene Expression Regulation, Plant, Genetic Variation, Glucosinolates, Herbivory, Host-Parasite Interactions, Larva, Mutation, Oxylipins, Plant Growth Regulators, Signal Transduction, Tetranychidae},
	pages = {384--399},
}

Most molecular-genetic studies of plant defense responses to arthropod herbivores have focused on insects. However, plant-feeding mites are also pests of diverse plants, and mites induce different patterns of damage to plant tissues than do well-studied insects (e.g. lepidopteran larvae or aphids). The two-spotted spider mite (Tetranychus urticae) is among the most significant mite pests in agriculture, feeding on a staggering number of plant hosts. To understand the interactions between spider mite and a plant at the molecular level, we examined reciprocal genome-wide responses of mites and its host Arabidopsis (Arabidopsis thaliana). Despite differences in feeding guilds, we found that transcriptional responses of Arabidopsis to mite herbivory resembled those observed for lepidopteran herbivores. Mutant analysis of induced plant defense pathways showed functionally that only a subset of induced programs, including jasmonic acid signaling and biosynthesis of indole glucosinolates, are central to Arabidopsis's defense to mite herbivory. On the herbivore side, indole glucosinolates dramatically increased mite mortality and development times. We identified an indole glucosinolate dose-dependent increase in the number of differentially expressed mite genes belonging to pathways associated with detoxification of xenobiotics. This demonstrates that spider mite is sensitive to Arabidopsis defenses that have also been associated with the deterrence of insect herbivores that are very distantly related to chelicerates. Our findings provide molecular insights into the nature of, and response to, herbivory for a representative of a major class of arthropod herbivores.

@incollection{galvao_regulation_2014,
	title = {Regulation of {Flowering} by {Endogenous} {Signals}},
	volume = {72},
	isbn = {978-0-12-417162-6},
	abstract = {The transition from vegetative to reproductive development, or floral transition, is a crucial event in the life cycle of plants. Work carried out over the last decades has shown how environmental signals, such as seasonal changes in the day length and temperature, are perceived and accurately integrated into genetically defined pathways to properly time the induction of flowering. In addition to seasonal fluctuations, plants must cope with a vast array of often stressful conditions that greatly affect metabolism and physiology. In this context, plant hormones and sugars have emerged as important endogenous signalling molecules mediating the transition to the reproductive phase. In this chapter we report the recent advances in understanding the molecular basis underlying the transition to flowering in response to these endogenous signals.},
	booktitle = {Advances in {Botanical} {Research}},
	author = {Galvão, Vinicius and Schmid, Markus},
	month = dec,
	year = {2014},
	doi = {10.1016/B978-0-12-417162-6.00003-1},
	note = {Journal Abbreviation: Advances in Botanical Research},
	pages = {63--102},
}

The transition from vegetative to reproductive development, or floral transition, is a crucial event in the life cycle of plants. Work carried out over the last decades has shown how environmental signals, such as seasonal changes in the day length and temperature, are perceived and accurately integrated into genetically defined pathways to properly time the induction of flowering. In addition to seasonal fluctuations, plants must cope with a vast array of often stressful conditions that greatly affect metabolism and physiology. In this context, plant hormones and sugars have emerged as important endogenous signalling molecules mediating the transition to the reproductive phase. In this chapter we report the recent advances in understanding the molecular basis underlying the transition to flowering in response to these endogenous signals.

@article{wahl_regulation_2013,
	title = {Regulation of flowering by trehalose-6-phosphate signaling in {Arabidopsis} thaliana},
	volume = {339},
	issn = {1095-9203},
	doi = {10/f4kxph},
	abstract = {The timing of the induction of flowering determines to a large extent the reproductive success of plants. Plants integrate diverse environmental and endogenous signals to ensure the timely transition from vegetative growth to flowering. Carbohydrates are thought to play a crucial role in the regulation of flowering, and trehalose-6-phosphate (T6P) has been suggested to function as a proxy for carbohydrate status in plants. The loss of TREHALOSE-6-PHOSPHATE SYNTHASE 1 (TPS1) causes Arabidopsis thaliana to flower extremely late, even under otherwise inductive environmental conditions. This suggests that TPS1 is required for the timely initiation of flowering. We show that the T6P pathway affects flowering both in the leaves and at the shoot meristem, and integrate TPS1 into the existing genetic framework of flowering-time control.},
	language = {eng},
	number = {6120},
	journal = {Science (New York, N.Y.)},
	author = {Wahl, Vanessa and Ponnu, Jathish and Schlereth, Armin and Arrivault, Stéphanie and Langenecker, Tobias and Franke, Annika and Feil, Regina and Lunn, John E. and Stitt, Mark and Schmid, Markus},
	month = feb,
	year = {2013},
	pmid = {23393265},
	keywords = {Arabidopsis, Arabidopsis Proteins, Circadian Rhythm, Flowers, Gene Expression Regulation, Plant, Glucosyltransferases, Meristem, MicroRNAs, Phosphatidylethanolamine Binding Protein, Photoperiod, Plant Leaves, Plant Shoots, Signal Transduction, Sugar Phosphates, Trehalose},
	pages = {704--707},
}

The timing of the induction of flowering determines to a large extent the reproductive success of plants. Plants integrate diverse environmental and endogenous signals to ensure the timely transition from vegetative growth to flowering. Carbohydrates are thought to play a crucial role in the regulation of flowering, and trehalose-6-phosphate (T6P) has been suggested to function as a proxy for carbohydrate status in plants. The loss of TREHALOSE-6-PHOSPHATE SYNTHASE 1 (TPS1) causes Arabidopsis thaliana to flower extremely late, even under otherwise inductive environmental conditions. This suggests that TPS1 is required for the timely initiation of flowering. We show that the T6P pathway affects flowering both in the leaves and at the shoot meristem, and integrate TPS1 into the existing genetic framework of flowering-time control.

@article{lee_regulation_2013,
	title = {Regulation of temperature-responsive flowering by {MADS}-box transcription factor repressors},
	volume = {342},
	issn = {1095-9203},
	doi = {10/f5fmt6},
	abstract = {Changes in ambient temperature affect flowering time in plants; understanding this phenomenon will be crucial for buffering agricultural systems from the effects of climate change. Here, we show that levels of FLM-β, an alternatively spliced form of the flowering repressor FLOWERING LOCUS M, increase at lower temperatures, repressing flowering. FLM-β interacts with SHORT VEGETATIVE PHASE (SVP); SVP is degraded at high temperatures, reducing the abundance of the SVP-FLM-β repressor complex and, thus, allowing the plant to flower. The svp and flm mutants show temperature-insensitive flowering in different temperature ranges. Control of SVP-FLM-β repressor complex abundance via transcriptional and splicing regulation of FLM and posttranslational regulation of SVP protein stability provides an efficient, rapid mechanism for plants to respond to ambient temperature changes.},
	language = {eng},
	number = {6158},
	journal = {Science (New York, N.Y.)},
	author = {Lee, Jeong Hwan and Ryu, Hak-Seung and Chung, Kyung Sook and Posé, David and Kim, Soonkap and Schmid, Markus and Ahn, Ji Hoon},
	month = nov,
	year = {2013},
	pmid = {24030492},
	keywords = {Alternative Splicing, Arabidopsis, Arabidopsis Proteins, Flowers, Gene Expression Regulation, Plant, MADS Domain Proteins, Molecular Sequence Data, Mutation, Repressor Proteins, Temperature, Transcription Factors},
	pages = {628--632},
}

Changes in ambient temperature affect flowering time in plants; understanding this phenomenon will be crucial for buffering agricultural systems from the effects of climate change. Here, we show that levels of FLM-β, an alternatively spliced form of the flowering repressor FLOWERING LOCUS M, increase at lower temperatures, repressing flowering. FLM-β interacts with SHORT VEGETATIVE PHASE (SVP); SVP is degraded at high temperatures, reducing the abundance of the SVP-FLM-β repressor complex and, thus, allowing the plant to flower. The svp and flm mutants show temperature-insensitive flowering in different temperature ranges. Control of SVP-FLM-β repressor complex abundance via transcriptional and splicing regulation of FLM and posttranslational regulation of SVP protein stability provides an efficient, rapid mechanism for plants to respond to ambient temperature changes.

@article{pose_temperature-dependent_2013,
	title = {Temperature-dependent regulation of flowering by antagonistic {FLM} variants},
	volume = {503},
	issn = {1476-4687},
	doi = {10/f5h734},
	abstract = {The appropriate timing of flowering is crucial for plant reproductive success. It is therefore not surprising that intricate genetic networks have evolved to perceive and integrate both endogenous and environmental signals, such as carbohydrate and hormonal status, photoperiod and temperature. In contrast to our detailed understanding of the vernalization pathway, little is known about how flowering time is controlled in response to changes in the ambient growth temperature. In Arabidopsis thaliana, the MADS-box transcription factor genes FLOWERING LOCUS M (FLM) and SHORT VEGETATIVE PHASE (SVP) have key roles in this process. FLM is subject to temperature-dependent alternative splicing. Here we report that the two main FLM protein splice variants, FLM-β and FLM-δ, compete for interaction with the floral repressor SVP. The SVP-FLM-β complex is predominately formed at low temperatures and prevents precocious flowering. By contrast, the competing SVP-FLM-δ complex is impaired in DNA binding and acts as a dominant-negative activator of flowering at higher temperatures. Our results show a new mechanism that controls the timing of the floral transition in response to changes in ambient temperature. A better understanding of how temperature controls the molecular mechanisms of flowering will be important to cope with current changes in global climate.},
	language = {eng},
	number = {7476},
	journal = {Nature},
	author = {Posé, David and Verhage, Leonie and Ott, Felix and Yant, Levi and Mathieu, Johannes and Angenent, Gerco C. and Immink, Richard G. H. and Schmid, Markus},
	month = nov,
	year = {2013},
	pmid = {24067612},
	keywords = {Alternative Splicing, Arabidopsis, Arabidopsis Proteins, DNA-Binding Proteins, Flowers, Gene Expression Regulation, Plant, MADS Domain Proteins, Plants, Genetically Modified, Protein Binding, Protein Isoforms, Temperature, Time Factors, Transcription Factors},
	pages = {414--417},
}

The appropriate timing of flowering is crucial for plant reproductive success. It is therefore not surprising that intricate genetic networks have evolved to perceive and integrate both endogenous and environmental signals, such as carbohydrate and hormonal status, photoperiod and temperature. In contrast to our detailed understanding of the vernalization pathway, little is known about how flowering time is controlled in response to changes in the ambient growth temperature. In Arabidopsis thaliana, the MADS-box transcription factor genes FLOWERING LOCUS M (FLM) and SHORT VEGETATIVE PHASE (SVP) have key roles in this process. FLM is subject to temperature-dependent alternative splicing. Here we report that the two main FLM protein splice variants, FLM-β and FLM-δ, compete for interaction with the floral repressor SVP. The SVP-FLM-β complex is predominately formed at low temperatures and prevents precocious flowering. By contrast, the competing SVP-FLM-δ complex is impaired in DNA binding and acts as a dominant-negative activator of flowering at higher temperatures. Our results show a new mechanism that controls the timing of the floral transition in response to changes in ambient temperature. A better understanding of how temperature controls the molecular mechanisms of flowering will be important to cope with current changes in global climate.

@article{immink_characterization_2012,
	title = {Characterization of {SOC1}'s central role in flowering by the identification of its upstream and downstream regulators},
	volume = {160},
	issn = {1532-2548},
	doi = {10/f36vk3},
	abstract = {The transition from vegetative to reproductive development is one of the most important phase changes in the plant life cycle. This step is controlled by various environmental signals that are integrated at the molecular level by so-called floral integrators. One such floral integrator in Arabidopsis (Arabidopsis thaliana) is the MADS domain transcription factor SUPPRESSOR OF OVEREXPRESSION OF CONSTANS1 (SOC1). Despite extensive genetic studies, little is known about the transcriptional control of SOC1, and we are just starting to explore the network of genes under the direct control of SOC1 transcription factor complexes. Here, we show that several MADS domain proteins, including SOC1 heterodimers, are able to bind SOC1 regulatory sequences. Genome-wide target gene analysis by ChIP-seq confirmed the binding of SOC1 to its own locus and shows that it also binds to a plethora of flowering-time regulatory and floral homeotic genes. In turn, the encoded floral homeotic MADS domain proteins appear to bind SOC1 regulatory sequences. Subsequent in planta analyses revealed SOC1 repression by several floral homeotic MADS domain proteins, and we show that, mechanistically, this depends on the presence of the SOC1 protein. Together, our data show that SOC1 constitutes a major hub in the regulatory networks underlying floral timing and flower development and that these networks are composed of many positive and negative autoregulatory and feedback loops. The latter seems to be crucial for the generation of a robust flower-inducing signal, followed shortly after by repression of the SOC1 floral integrator.},
	language = {eng},
	number = {1},
	journal = {Plant Physiology},
	author = {Immink, Richard G. H. and Posé, David and Ferrario, Silvia and Ott, Felix and Kaufmann, Kerstin and Valentim, Felipe Leal and de Folter, Stefan and van der Wal, Froukje and van Dijk, Aalt D. J. and Schmid, Markus and Angenent, Gerco C.},
	month = sep,
	year = {2012},
	pmid = {22791302},
	pmcid = {PMC3440217},
	keywords = {Arabidopsis, Arabidopsis Proteins, Feedback, Physiological, Flowers, Gene Expression Regulation, Plant, Genes, Plant, Genes, Reporter, Genetic Complementation Test, Genetic Loci, Green Fluorescent Proteins, Immunoprecipitation, MADS Domain Proteins, Promoter Regions, Genetic, Protein Binding, Regulatory Sequences, Nucleic Acid, Signal Transduction, Time Factors, Transcription, Genetic, Two-Hybrid System Techniques},
	pages = {433--449},
}

The transition from vegetative to reproductive development is one of the most important phase changes in the plant life cycle. This step is controlled by various environmental signals that are integrated at the molecular level by so-called floral integrators. One such floral integrator in Arabidopsis (Arabidopsis thaliana) is the MADS domain transcription factor SUPPRESSOR OF OVEREXPRESSION OF CONSTANS1 (SOC1). Despite extensive genetic studies, little is known about the transcriptional control of SOC1, and we are just starting to explore the network of genes under the direct control of SOC1 transcription factor complexes. Here, we show that several MADS domain proteins, including SOC1 heterodimers, are able to bind SOC1 regulatory sequences. Genome-wide target gene analysis by ChIP-seq confirmed the binding of SOC1 to its own locus and shows that it also binds to a plethora of flowering-time regulatory and floral homeotic genes. In turn, the encoded floral homeotic MADS domain proteins appear to bind SOC1 regulatory sequences. Subsequent in planta analyses revealed SOC1 repression by several floral homeotic MADS domain proteins, and we show that, mechanistically, this depends on the presence of the SOC1 protein. Together, our data show that SOC1 constitutes a major hub in the regulatory networks underlying floral timing and flower development and that these networks are composed of many positive and negative autoregulatory and feedback loops. The latter seems to be crucial for the generation of a robust flower-inducing signal, followed shortly after by repression of the SOC1 floral integrator.

@article{brandt_genome-wide_2012,
	title = {Genome-wide binding-site analysis of {REVOLUTA} reveals a link between leaf patterning and light-mediated growth responses},
	volume = {72},
	issn = {1365-313X},
	doi = {10/f3srjk},
	abstract = {Unlike the situation in animals, the final morphology of the plant body is highly modulated by the environment. During Arabidopsis development, intrinsic factors provide the framework for basic patterning processes. CLASS III HOMEODOMAIN LEUCINE ZIPPER (HD-ZIPIII) transcription factors are involved in embryo, shoot and root patterning. During vegetative growth HD-ZIPIII proteins control several polarity set-up processes such as in leaves and the vascular system. We have identified several direct target genes of the HD-ZIPIII transcription factor REVOLUTA (REV) using a chromatin immunoprecipitation/DNA sequencing (ChIP-Seq) approach. This analysis revealed that REV acts upstream of auxin biosynthesis and affects directly the expression of several class II HD-ZIP transcription factors that have been shown to act in the shade-avoidance response pathway. We show that, as well as involvement in basic patterning, HD-ZIPIII transcription factors have a critical role in the control of the elongation growth that is induced when plants experience shade. Leaf polarity is established by the opposed actions of HD-ZIPIII and KANADI transcription factors. Finally, our study reveals that the module that consists of HD-ZIPIII/KANADI transcription factors controls shade growth antagonistically and that this antagonism is manifested in the opposed regulation of shared target genes.},
	language = {eng},
	number = {1},
	journal = {The Plant Journal: For Cell and Molecular Biology},
	author = {Brandt, Ronny and Salla-Martret, Mercè and Bou-Torrent, Jordi and Musielak, Thomas and Stahl, Mark and Lanz, Christa and Ott, Felix and Schmid, Markus and Greb, Thomas and Schwarz, Martina and Choi, Sang-Bong and Barton, M. Kathryn and Reinhart, Brenda J. and Liu, Tie and Quint, Marcel and Palauqui, Jean-Christophe and Martínez-García, Jaime F. and Wenkel, Stephan},
	month = oct,
	year = {2012},
	keywords = {Adaptation, Physiological, Arabidopsis, Arabidopsis Proteins, Arabidopsis thaliana, Binding Sites, Body Patterning, Chromatin Immunoprecipitation, Gene Expression Regulation, Developmental, Gene Expression Regulation, Plant, Genome, Plant, HD-ZIPII, HD-ZIPIII, Homeodomain Proteins, Hypocotyl, In Situ Hybridization, Indoleacetic Acids, Light, Mutation, Phylogeny, Plant Leaves, Sequence Analysis, DNA, Signal Transduction, Transcription Factors, auxin, leaf development, shade avoidance},
	pages = {31--42},
}

Unlike the situation in animals, the final morphology of the plant body is highly modulated by the environment. During Arabidopsis development, intrinsic factors provide the framework for basic patterning processes. CLASS III HOMEODOMAIN LEUCINE ZIPPER (HD-ZIPIII) transcription factors are involved in embryo, shoot and root patterning. During vegetative growth HD-ZIPIII proteins control several polarity set-up processes such as in leaves and the vascular system. We have identified several direct target genes of the HD-ZIPIII transcription factor REVOLUTA (REV) using a chromatin immunoprecipitation/DNA sequencing (ChIP-Seq) approach. This analysis revealed that REV acts upstream of auxin biosynthesis and affects directly the expression of several class II HD-ZIP transcription factors that have been shown to act in the shade-avoidance response pathway. We show that, as well as involvement in basic patterning, HD-ZIPIII transcription factors have a critical role in the control of the elongation growth that is induced when plants experience shade. Leaf polarity is established by the opposed actions of HD-ZIPIII and KANADI transcription factors. Finally, our study reveals that the module that consists of HD-ZIPIII/KANADI transcription factors controls shade growth antagonistically and that this antagonism is manifested in the opposed regulation of shared target genes.

@article{yu_gibberellin_2012,
	title = {Gibberellin {Regulates} the {Arabidopsis} {Floral} {Transition} through {miR156}-{Targeted} {SQUAMOSA} {PROMOTER} {BINDING}–{LIKE} {Transcription} {Factors}[{W}]},
	volume = {24},
	issn = {1040-4651},
	url = {https://www.ncbi.nlm.nih.gov/pmc/articles/PMC3462634/},
	doi = {10.1105/tpc.112.101014},
	abstract = {This article examines the crosstalk between gibberellin responses, which result in degradation of DELLAs, and the microRNA-regulated SQUAMOSA PROMOTER BINDING LIKE (SPL) transcription factors, which activate miR172 and MADS box transcription factors. The authors find that DELLA binds to SPLs and interfere with SPL transcriptional activation of miR172 and MADS box genes, thereby delaying flowering., Gibberellin (), a diterpene hormone, plays diverse roles in plant growth and development, including seed germination, stem elongation, and flowering time. Although it is known that  accelerates flowering through degradation of transcription repressors, DELLAs, the underlying mechanism is poorly understood. We show here that DELLA directly binds to microRNA156 (miR156)-targeted SQUAMOSA PROMOTER BINDING–LIKE (SPL) transcription factors, which promote flowering by activating miR172 and MADS box genes. The interaction between DELLA and SPL interferes with SPL transcriptional activity and consequently delays floral transition through inactivating miR172 in leaves and MADS box genes at shoot apex under long-day conditions or through repressing MADS box genes at the shoot apex under short-day conditions. Our results elucidate the molecular mechanism by which  controls flowering and provide the missing link between DELLA and MADS box genes.},
	number = {8},
	urldate = {2021-10-22},
	journal = {The Plant Cell},
	author = {Yu, Sha and Galvão, Vinicius C. and Zhang, Yan-Chun and Horrer, Daniel and Zhang, Tian-Qi and Hao, Yan-Hong and Feng, Yu-Qi and Wang, Shui and Schmid, Markus and Wang, Jia-Wei},
	month = aug,
	year = {2012},
	pmid = {22942378},
	pmcid = {PMC3462634},
	pages = {3320--3332},
}

This article examines the crosstalk between gibberellin responses, which result in degradation of DELLAs, and the microRNA-regulated SQUAMOSA PROMOTER BINDING LIKE (SPL) transcription factors, which activate miR172 and MADS box transcription factors. The authors find that DELLA binds to SPLs and interfere with SPL transcriptional activation of miR172 and MADS box genes, thereby delaying flowering., Gibberellin (), a diterpene hormone, plays diverse roles in plant growth and development, including seed germination, stem elongation, and flowering time. Although it is known that accelerates flowering through degradation of transcription repressors, DELLAs, the underlying mechanism is poorly understood. We show here that DELLA directly binds to microRNA156 (miR156)-targeted SQUAMOSA PROMOTER BINDING–LIKE (SPL) transcription factors, which promote flowering by activating miR172 and MADS box genes. The interaction between DELLA and SPL interferes with SPL transcriptional activity and consequently delays floral transition through inactivating miR172 in leaves and MADS box genes at shoot apex under long-day conditions or through repressing MADS box genes at the shoot apex under short-day conditions. Our results elucidate the molecular mechanism by which controls flowering and provide the missing link between DELLA and MADS box genes.

@article{galvao_spatial_2012,
	title = {Spatial control of flowering by {DELLA} proteins in {Arabidopsis} thaliana},
	volume = {139},
	issn = {1477-9129},
	doi = {10/f4cgh5},
	abstract = {The transition from vegetative to reproductive development is a central event in the plant life cycle. To time the induction of flowering correctly, plants integrate environmental and endogenous signals such as photoperiod, temperature and hormonal status. The hormone gibberellic acid (GA) has long been known to regulate flowering. However, the spatial contribution of GA signaling in flowering time control is poorly understood. Here we have analyzed the effect of tissue-specific misexpression of wild-type and GA-insensitive (dellaΔ17) DELLA proteins on the floral transition in Arabidopsis thaliana. We demonstrate that under long days, GA affects the floral transition by promoting the expression of flowering time integrator genes such as FLOWERING LOCUS T (FT) and TWIN SISTER OF FT (TSF) in leaves independently of CONSTANS (CO) and GIGANTEA (GI). In addition, GA signaling promotes flowering independently of photoperiod through the regulation of SQUAMOSA PROMOTER BINDING PROTEIN-LIKE (SPL) genes in both the leaves and at the shoot meristem. Our data suggest that GA regulates flowering by controlling the spatial expression of floral regulatory genes throughout the plant in a day-length-specific manner.},
	language = {eng},
	number = {21},
	journal = {Development (Cambridge, England)},
	author = {Galvão, Vinicius C. and Horrer, Daniel and Küttner, Frank and Schmid, Markus},
	month = nov,
	year = {2012},
	pmid = {22992955},
	keywords = {Arabidopsis, Arabidopsis Proteins, Flowers, Gene Expression Regulation, Plant, Gibberellins},
	pages = {4072--4082},
}

The transition from vegetative to reproductive development is a central event in the plant life cycle. To time the induction of flowering correctly, plants integrate environmental and endogenous signals such as photoperiod, temperature and hormonal status. The hormone gibberellic acid (GA) has long been known to regulate flowering. However, the spatial contribution of GA signaling in flowering time control is poorly understood. Here we have analyzed the effect of tissue-specific misexpression of wild-type and GA-insensitive (dellaΔ17) DELLA proteins on the floral transition in Arabidopsis thaliana. We demonstrate that under long days, GA affects the floral transition by promoting the expression of flowering time integrator genes such as FLOWERING LOCUS T (FT) and TWIN SISTER OF FT (TSF) in leaves independently of CONSTANS (CO) and GIGANTEA (GI). In addition, GA signaling promotes flowering independently of photoperiod through the regulation of SQUAMOSA PROMOTER BINDING PROTEIN-LIKE (SPL) genes in both the leaves and at the shoot meristem. Our data suggest that GA regulates flowering by controlling the spatial expression of floral regulatory genes throughout the plant in a day-length-specific manner.

@article{galvao_synteny-based_2012,
	title = {Synteny-based mapping-by-sequencing enabled by targeted enrichment},
	volume = {71},
	issn = {1365-313X},
	doi = {10/gkgdms},
	abstract = {Mapping-by-sequencing, as implemented in SHOREmap ('SHOREmapping'), is greatly accelerating the identification of causal mutations. The original SHOREmap approach based on resequencing of bulked segregants required a highly accurate and complete reference sequence. However, current whole-genome or transcriptome assemblies from next-generation sequencing data of non-model organisms do not produce chromosome-length scaffolds. We have therefore developed a method that exploits synteny with a related genome for genetic mapping. We first demonstrate how mapping-by-sequencing can be performed using a reduced number of markers, and how the associated decrease in the number of markers can be compensated for by enrichment of marker sequences. As proof of concept, we apply this method to Arabidopsis thaliana gene models ordered by synteny with the genome sequence of the distant relative Brassica rapa, whose genome has several large-scale rearrangements relative to A. thaliana. Our approach provides an alternative method for high-resolution genetic mapping in species that lack finished genome reference sequences or for which only RNA-seq assemblies are available. Finally, for improved identification of causal mutations by fine-mapping, we introduce a new likelihood ratio test statistic, transforming local allele frequency estimations into a confidence interval similar to conventional mapping intervals.},
	language = {eng},
	number = {3},
	journal = {The Plant Journal: For Cell and Molecular Biology},
	author = {Galvão, Vinicius C. and Nordström, Karl J. V. and Lanz, Christa and Sulz, Patric and Mathieu, Johannes and Posé, David and Schmid, Markus and Weigel, Detlef and Schneeberger, Korbinian},
	month = aug,
	year = {2012},
	pmid = {22409706},
	keywords = {Arabidopsis, Arabidopsis Proteins, Brassica rapa, Chromosome Mapping, DNA Mutational Analysis, DNA, Plant, Flowers, Gene Frequency, Gene Library, Genetic Linkage, Genome, Plant, High-Throughput Nucleotide Sequencing, MADS Domain Proteins, Mutation, Sequence Analysis, DNA, Synteny, Transcriptome},
	pages = {517--526},
}

Mapping-by-sequencing, as implemented in SHOREmap ('SHOREmapping'), is greatly accelerating the identification of causal mutations. The original SHOREmap approach based on resequencing of bulked segregants required a highly accurate and complete reference sequence. However, current whole-genome or transcriptome assemblies from next-generation sequencing data of non-model organisms do not produce chromosome-length scaffolds. We have therefore developed a method that exploits synteny with a related genome for genetic mapping. We first demonstrate how mapping-by-sequencing can be performed using a reduced number of markers, and how the associated decrease in the number of markers can be compensated for by enrichment of marker sequences. As proof of concept, we apply this method to Arabidopsis thaliana gene models ordered by synteny with the genome sequence of the distant relative Brassica rapa, whose genome has several large-scale rearrangements relative to A. thaliana. Our approach provides an alternative method for high-resolution genetic mapping in species that lack finished genome reference sequences or for which only RNA-seq assemblies are available. Finally, for improved identification of causal mutations by fine-mapping, we introduce a new likelihood ratio test statistic, transforming local allele frequency estimations into a confidence interval similar to conventional mapping intervals.

@article{pose_end_2012,
	title = {The end of innocence: flowering networks explode in complexity},
	volume = {15},
	issn = {1879-0356},
	shorttitle = {The end of innocence},
	doi = {10/fphkmr},
	abstract = {Substantial recent advances in genome-scale transcription factor target mapping have provided a fresh view of the gene networks governing developmental transitions. In particular, our understanding of the fine-scale spatial and temporal dynamics underlying the floral transition at the shoot apex has seen great advances in the past two years. Single transcription factors are regularly observed to act in complex manners, directly promoting the expression of particular targets while directly repressing the expression of others, based at least partly on defined heterodimerization patterns. For single regulators this behavior reaches into distinct physiological processes, providing compelling evidence that particular transcription factors act to directly integrate diverse processes to orchestrate complex developmental transitions.},
	language = {eng},
	number = {1},
	journal = {Current Opinion in Plant Biology},
	author = {Posé, David and Yant, Levi and Schmid, Markus},
	month = feb,
	year = {2012},
	pmid = {21974961},
	keywords = {Flowers, Gene Expression Regulation, Developmental, Gene Expression Regulation, Plant, Gene Regulatory Networks, Genes, Plant, Plant Shoots},
	pages = {45--50},
}

Substantial recent advances in genome-scale transcription factor target mapping have provided a fresh view of the gene networks governing developmental transitions. In particular, our understanding of the fine-scale spatial and temporal dynamics underlying the floral transition at the shoot apex has seen great advances in the past two years. Single transcription factors are regularly observed to act in complex manners, directly promoting the expression of particular targets while directly repressing the expression of others, based at least partly on defined heterodimerization patterns. For single regulators this behavior reaches into distinct physiological processes, providing compelling evidence that particular transcription factors act to directly integrate diverse processes to orchestrate complex developmental transitions.

@article{dinh_floral_2012,
	title = {The floral homeotic protein {APETALA2} recognizes and acts through an {AT}-rich sequence element},
	volume = {139},
	issn = {1477-9129},
	doi = {10/f3xzq8},
	abstract = {Cell fate specification in development requires transcription factors for proper regulation of gene expression. In Arabidopsis, transcription factors encoded by four classes of homeotic genes, A, B, C and E, act in a combinatorial manner to control proper floral organ identity. The A-class gene APETALA2 (AP2) promotes sepal and petal identities in whorls 1 and 2 and restricts the expression of the C-class gene AGAMOUS (AG) from whorls 1 and 2. However, it is unknown how AP2 performs these functions. Unlike the other highly characterized floral homeotic proteins containing MADS domains, AP2 has two DNA-binding domains referred to as the AP2 domains and its DNA recognition sequence is still unknown. Here, we show that the second AP2 domain in AP2 binds a non-canonical AT-rich target sequence, and, using a GUS reporter system, we demonstrate that the presence of this sequence in the AG second intron is important for the restriction of AG expression in vivo. Furthermore, we show that AP2 binds the AG second intron and directly regulates AG expression through this sequence element. Computational analysis reveals that the binding site is highly conserved in the second intron of AG orthologs throughout Brassicaceae. By uncovering a biologically relevant AT-rich target sequence, this work shows that AP2 domains have wide-ranging target specificities and provides a missing link in the mechanisms that underlie flower development. It also sets the foundation for understanding the basis of the broad biological functions of AP2 in Arabidopsis, as well as the divergent biological functions of AP2 orthologs in dicotyledonous plants.},
	language = {eng},
	number = {11},
	journal = {Development (Cambridge, England)},
	author = {Dinh, Thanh Theresa and Girke, Thomas and Liu, Xigang and Yant, Levi and Schmid, Markus and Chen, Xuemei},
	month = jun,
	year = {2012},
	pmid = {22513376},
	pmcid = {PMC3347690},
	keywords = {AGAMOUS Protein, Arabidopsis, Arabidopsis, Arabidopsis Proteins, Base Sequence, Cell Differentiation, Chromatin Immunoprecipitation, Computational Biology, Electrophoretic Mobility Shift Assay, Flowers, Gene Expression Regulation, Developmental, Gene Expression Regulation, Plant, Homeodomain Proteins, Molecular Sequence Data, Nuclear Proteins, Sequence Analysis, DNA, Species Specificity},
	pages = {1978--1986},
}

Cell fate specification in development requires transcription factors for proper regulation of gene expression. In Arabidopsis, transcription factors encoded by four classes of homeotic genes, A, B, C and E, act in a combinatorial manner to control proper floral organ identity. The A-class gene APETALA2 (AP2) promotes sepal and petal identities in whorls 1 and 2 and restricts the expression of the C-class gene AGAMOUS (AG) from whorls 1 and 2. However, it is unknown how AP2 performs these functions. Unlike the other highly characterized floral homeotic proteins containing MADS domains, AP2 has two DNA-binding domains referred to as the AP2 domains and its DNA recognition sequence is still unknown. Here, we show that the second AP2 domain in AP2 binds a non-canonical AT-rich target sequence, and, using a GUS reporter system, we demonstrate that the presence of this sequence in the AG second intron is important for the restriction of AG expression in vivo. Furthermore, we show that AP2 binds the AG second intron and directly regulates AG expression through this sequence element. Computational analysis reveals that the binding site is highly conserved in the second intron of AG orthologs throughout Brassicaceae. By uncovering a biologically relevant AT-rich target sequence, this work shows that AP2 domains have wide-ranging target specificities and provides a missing link in the mechanisms that underlie flower development. It also sets the foundation for understanding the basis of the broad biological functions of AP2 in Arabidopsis, as well as the divergent biological functions of AP2 orthologs in dicotyledonous plants.

@article{moyroud_prediction_2011,
	title = {Prediction of regulatory interactions from genome sequences using a biophysical model for the {Arabidopsis} {LEAFY} transcription factor},
	volume = {23},
	issn = {1532-298X},
	doi = {10/dnkx8z},
	abstract = {Despite great advances in sequencing technologies, generating functional information for nonmodel organisms remains a challenge. One solution lies in an improved ability to predict genetic circuits based on primary DNA sequence in combination with detailed knowledge of regulatory proteins that have been characterized in model species. Here, we focus on the LEAFY (LFY) transcription factor, a conserved master regulator of floral development. Starting with biochemical and structural information, we built a biophysical model describing LFY DNA binding specificity in vitro that accurately predicts in vivo LFY binding sites in the Arabidopsis thaliana genome. Applying the model to other plant species, we could follow the evolution of the regulatory relationship between LFY and the AGAMOUS (AG) subfamily of MADS box genes and show that this link predates the divergence between monocots and eudicots. Remarkably, our model succeeds in detecting the connection between LFY and AG homologs despite extensive variation in binding sites. This demonstrates that the cis-element fluidity recently observed in animals also exists in plants, but the challenges it poses can be overcome with predictions grounded in a biophysical model. Therefore, our work opens new avenues to deduce the structure of regulatory networks from mere inspection of genomic sequences.},
	language = {eng},
	number = {4},
	journal = {The Plant Cell},
	author = {Moyroud, Edwige and Minguet, Eugenio Gómez and Ott, Felix and Yant, Levi and Posé, David and Monniaux, Marie and Blanchet, Sandrine and Bastien, Olivier and Thévenon, Emmanuel and Weigel, Detlef and Schmid, Markus and Parcy, François},
	month = apr,
	year = {2011},
	pmid = {21515819},
	pmcid = {PMC3101549},
	keywords = {AGAMOUS Protein, Arabidopsis, Arabidopsis, Arabidopsis Proteins, Base Sequence, Binding Sites, Biophysical Phenomena, Chromatin Immunoprecipitation, DNA, Plant, Evolution, Molecular, Flowers, Gene Expression Regulation, Plant, Genes, Plant, Genome, Plant, Introns, Models, Genetic, Molecular Sequence Data, Protein Binding, Regulatory Sequences, Nucleic Acid, Reproducibility of Results, Transcription Factors},
	pages = {1293--1306},
}

Despite great advances in sequencing technologies, generating functional information for nonmodel organisms remains a challenge. One solution lies in an improved ability to predict genetic circuits based on primary DNA sequence in combination with detailed knowledge of regulatory proteins that have been characterized in model species. Here, we focus on the LEAFY (LFY) transcription factor, a conserved master regulator of floral development. Starting with biochemical and structural information, we built a biophysical model describing LFY DNA binding specificity in vitro that accurately predicts in vivo LFY binding sites in the Arabidopsis thaliana genome. Applying the model to other plant species, we could follow the evolution of the regulatory relationship between LFY and the AGAMOUS (AG) subfamily of MADS box genes and show that this link predates the divergence between monocots and eudicots. Remarkably, our model succeeds in detecting the connection between LFY and AG homologs despite extensive variation in binding sites. This demonstrates that the cis-element fluidity recently observed in animals also exists in plants, but the challenges it poses can be overcome with predictions grounded in a biophysical model. Therefore, our work opens new avenues to deduce the structure of regulatory networks from mere inspection of genomic sequences.

@article{srikanth_regulation_2011,
	title = {Regulation of flowering time: all roads lead to {Rome}},
	volume = {68},
	issn = {1420-9071},
	shorttitle = {Regulation of flowering time},
	doi = {10/d99mmw},
	abstract = {Plants undergo a major physiological change as they transition from vegetative growth to reproductive development. This transition is a result of responses to various endogenous and exogenous signals that later integrate to result in flowering. Five genetically defined pathways have been identified that control flowering. The vernalization pathway refers to the acceleration of flowering on exposure to a long period of cold. The photoperiod pathway refers to regulation of flowering in response to day length and quality of light perceived. The gibberellin pathway refers to the requirement of gibberellic acid for normal flowering patterns. The autonomous pathway refers to endogenous regulators that are independent of the photoperiod and gibberellin pathways. Most recently, an endogenous pathway that adds plant age to the control of flowering time has been described. The molecular mechanisms of these pathways have been studied extensively in Arabidopsis thaliana and several other flowering plants.},
	language = {eng},
	number = {12},
	journal = {Cellular and molecular life sciences: CMLS},
	author = {Srikanth, Anusha and Schmid, Markus},
	month = jun,
	year = {2011},
	pmid = {21611891},
	keywords = {Arabidopsis, Flowers, Plant Physiological Phenomena, Signal Transduction},
	pages = {2013--2037},
}

Plants undergo a major physiological change as they transition from vegetative growth to reproductive development. This transition is a result of responses to various endogenous and exogenous signals that later integrate to result in flowering. Five genetically defined pathways have been identified that control flowering. The vernalization pathway refers to the acceleration of flowering on exposure to a long period of cold. The photoperiod pathway refers to regulation of flowering in response to day length and quality of light perceived. The gibberellin pathway refers to the requirement of gibberellic acid for normal flowering patterns. The autonomous pathway refers to endogenous regulators that are independent of the photoperiod and gibberellin pathways. Most recently, an endogenous pathway that adds plant age to the control of flowering time has been described. The molecular mechanisms of these pathways have been studied extensively in Arabidopsis thaliana and several other flowering plants.

@article{huijser_control_2011,
	title = {The control of developmental phase transitions in plants},
	volume = {138},
	issn = {1477-9129},
	doi = {10/ddvxq2},
	abstract = {Plant development progresses through distinct phases: vegetative growth, followed by a reproductive phase and eventually seed set and senescence. The transitions between these phases are controlled by distinct genetic circuits that integrate endogenous and environmental cues. In recent years, however, it has become evident that the genetic networks that underlie these phase transitions share some common factors. Here, we review recent advances in the field of plant phase transitions, highlighting the role of two microRNAs - miR156 and miR172 - and their respective targets during these transitions. In addition, we discuss the evolutionary conservation of the functions of these miRNAs in regulating the control of plant developmental phase transitions.},
	language = {eng},
	number = {19},
	journal = {Development (Cambridge, England)},
	author = {Huijser, Peter and Schmid, Markus},
	month = oct,
	year = {2011},
	pmid = {21896627},
	keywords = {Arabidopsis, Developmental Biology, Flowers, Gene Expression Regulation, Plant, Genes, Plant, MicroRNAs, Models, Biological, Models, Genetic, Plant Physiological Phenomena, Plants, Pollen, Transcription Factors},
	pages = {4117--4129},
}

Plant development progresses through distinct phases: vegetative growth, followed by a reproductive phase and eventually seed set and senescence. The transitions between these phases are controlled by distinct genetic circuits that integrate endogenous and environmental cues. In recent years, however, it has become evident that the genetic networks that underlie these phase transitions share some common factors. Here, we review recent advances in the field of plant phase transitions, highlighting the role of two microRNAs - miR156 and miR172 - and their respective targets during these transitions. In addition, we discuss the evolutionary conservation of the functions of these miRNAs in regulating the control of plant developmental phase transitions.

@article{ponnu_trehalose-6-phosphate_2011,
	title = {Trehalose-6-phosphate: connecting plant metabolism and development},
	volume = {2},
	issn = {1664-462X},
	shorttitle = {Trehalose-6-phosphate},
	doi = {10/djjn5z},
	abstract = {Beyond their metabolic roles, sugars can also act as messengers in signal transduction. Trehalose, a sugar found in many species of plants and animals, is a non-reducing disaccharide composed of two glucose moieties. Its synthesis in plants is a two-step process, involving the production of trehalose-6-phosphate (T6P) catalyzed by trehalose-6-phosphate synthase (TPS) and its consecutive dephosphorylation to trehalose, catalyzed by trehalose-6-phosphate phosphatase (TPP). T6P has recently emerged as an important signaling metabolite, regulating carbon assimilation and sugar status in plants. In addition, T6P has also been demonstrated to play an essential role in plant development. This review recapitulates the recent advances we have made in understanding the role of T6P in coordinating diverse metabolic and developmental processes.},
	language = {eng},
	journal = {Frontiers in Plant Science},
	author = {Ponnu, Jathish and Wahl, Vanessa and Schmid, Markus},
	year = {2011},
	pmid = {22639606},
	pmcid = {PMC3355582},
	keywords = {TPP, TPS, development, trehalose, trehalose-6-phosphate},
	pages = {70},
}

Beyond their metabolic roles, sugars can also act as messengers in signal transduction. Trehalose, a sugar found in many species of plants and animals, is a non-reducing disaccharide composed of two glucose moieties. Its synthesis in plants is a two-step process, involving the production of trehalose-6-phosphate (T6P) catalyzed by trehalose-6-phosphate synthase (TPS) and its consecutive dephosphorylation to trehalose, catalyzed by trehalose-6-phosphate phosphatase (TPP). T6P has recently emerged as an important signaling metabolite, regulating carbon assimilation and sugar status in plants. In addition, T6P has also been demonstrated to play an essential role in plant development. This review recapitulates the recent advances we have made in understanding the role of T6P in coordinating diverse metabolic and developmental processes.

@article{koo_control_2010,
	title = {Control of lateral organ development and flowering time by the {Arabidopsis} thaliana {MADS}-box {Gene} {AGAMOUS}-{LIKE6}},
	volume = {62},
	issn = {1365-313X},
	doi = {10/d7dmk9},
	abstract = {MADS-domain transcription factors play pivotal roles in various developmental processes. The lack of simple loss-of-function phenotypes provides impediments to understand the biological function of some of the MADS-box transcription factors. Here we have characterized the potential role of the Arabidopsis thaliana AGAMOUS-LIKE6 (AGL6) gene by fusing full-length coding sequence with transcriptional activator and repressor domains and suggest a role for AGL6 in lateral organ development and flowering. Upon photoperiodic induction of flowering, AGL6 becomes expressed in abaxial and proximal regions of cauline leaf primordia, as well as the cryptic bracts subtending flowers. In developing flowers, AGL6 is detected in the proximal regions of all floral organs and in developing ovules. Converting AGL6 into a strong activator through fusion to the VP16 domain triggers bract outgrowth, implicating AGL6 in the development of bractless flowers in Arabidopsis. In addition, ectopic reproductive structures form on both bracts and flowers in gAGL6::VP16 transgenic plants, which is dependent on B and C class homeotic genes, but independent of LEAFY. Overexpression of both AGL6 and its transcriptional repressor form, AGL6::EAR, causes precocious flowering and terminal flower formation, suggesting that AGL6 suppresses the function of a floral repressor.},
	language = {eng},
	number = {5},
	journal = {The Plant Journal: For Cell and Molecular Biology},
	author = {Koo, Sung C. and Bracko, Oliver and Park, Mi S. and Schwab, Rebecca and Chun, Hyun J. and Park, Kyoung M. and Seo, Jun S. and Grbic, Vojislava and Balasubramanian, Sureshkumar and Schmid, Markus and Godard, François and Yun, Dae-Jin and Lee, Sang Y. and Cho, Moo J. and Weigel, Detlef and Kim, Min C.},
	month = jun,
	year = {2010},
	pmid = {20230491},
	keywords = {Arabidopsis, Arabidopsis Proteins, Flowers, Gene Expression Regulation, Developmental, Gene Expression Regulation, Plant, MADS Domain Proteins, Microscopy, Electron, Scanning, Ovule, Plants, Genetically Modified, RNA, Plant},
	pages = {807--816},
}

MADS-domain transcription factors play pivotal roles in various developmental processes. The lack of simple loss-of-function phenotypes provides impediments to understand the biological function of some of the MADS-box transcription factors. Here we have characterized the potential role of the Arabidopsis thaliana AGAMOUS-LIKE6 (AGL6) gene by fusing full-length coding sequence with transcriptional activator and repressor domains and suggest a role for AGL6 in lateral organ development and flowering. Upon photoperiodic induction of flowering, AGL6 becomes expressed in abaxial and proximal regions of cauline leaf primordia, as well as the cryptic bracts subtending flowers. In developing flowers, AGL6 is detected in the proximal regions of all floral organs and in developing ovules. Converting AGL6 into a strong activator through fusion to the VP16 domain triggers bract outgrowth, implicating AGL6 in the development of bractless flowers in Arabidopsis. In addition, ectopic reproductive structures form on both bracts and flowers in gAGL6::VP16 transgenic plants, which is dependent on B and C class homeotic genes, but independent of LEAFY. Overexpression of both AGL6 and its transcriptional repressor form, AGL6::EAR, causes precocious flowering and terminal flower formation, suggesting that AGL6 suppresses the function of a floral repressor.

@article{schlereth_monopteros_2010,
	title = {{MONOPTEROS} controls embryonic root initiation by regulating a mobile transcription factor},
	volume = {464},
	issn = {1476-4687},
	doi = {10/fvkmp7},
	abstract = {Acquisition of cell identity in plants relies strongly on positional information, hence cell-cell communication and inductive signalling are instrumental for developmental patterning. During Arabidopsis embryogenesis, an extra-embryonic cell is specified to become the founder cell of the primary root meristem, hypophysis, in response to signals from adjacent embryonic cells. The auxin-dependent transcription factor MONOPTEROS (MP) drives hypophysis specification by promoting transport of the hormone auxin from the embryo to the hypophysis precursor. However, auxin accumulation is not sufficient for hypophysis specification, indicating that additional MP-dependent signals are required. Here we describe the microarray-based isolation of MP target genes that mediate signalling from embryo to hypophysis. Of three direct transcriptional target genes, TARGET OF MP 5 (TMO5) and TMO7 encode basic helix-loop-helix (bHLH) transcription factors that are expressed in the hypophysis-adjacent embryo cells, and are required and partially sufficient for MP-dependent root initiation. Importantly, the small TMO7 transcription factor moves from its site of synthesis in the embryo to the hypophysis precursor, thus representing a novel MP-dependent intercellular signal in embryonic root specification.},
	language = {eng},
	number = {7290},
	journal = {Nature},
	author = {Schlereth, Alexandra and Möller, Barbara and Liu, Weilin and Kientz, Marika and Flipse, Jacky and Rademacher, Eike H. and Schmid, Markus and Jürgens, Gerd and Weijers, Dolf},
	month = apr,
	year = {2010},
	pmid = {20220754},
	keywords = {Arabidopsis, Arabidopsis Proteins, Basic Helix-Loop-Helix Transcription Factors, DNA-Binding Proteins, Embryonic Development, Gene Expression Regulation, Plant, Genes, Plant, Indoleacetic Acids, Meristem, Oligonucleotide Array Sequence Analysis, Plant Roots, Signal Transduction, Transcription Factors},
	pages = {913--916},
}

Acquisition of cell identity in plants relies strongly on positional information, hence cell-cell communication and inductive signalling are instrumental for developmental patterning. During Arabidopsis embryogenesis, an extra-embryonic cell is specified to become the founder cell of the primary root meristem, hypophysis, in response to signals from adjacent embryonic cells. The auxin-dependent transcription factor MONOPTEROS (MP) drives hypophysis specification by promoting transport of the hormone auxin from the embryo to the hypophysis precursor. However, auxin accumulation is not sufficient for hypophysis specification, indicating that additional MP-dependent signals are required. Here we describe the microarray-based isolation of MP target genes that mediate signalling from embryo to hypophysis. Of three direct transcriptional target genes, TARGET OF MP 5 (TMO5) and TMO7 encode basic helix-loop-helix (bHLH) transcription factors that are expressed in the hypophysis-adjacent embryo cells, and are required and partially sufficient for MP-dependent root initiation. Importantly, the small TMO7 transcription factor moves from its site of synthesis in the embryo to the hypophysis precursor, thus representing a novel MP-dependent intercellular signal in embryonic root specification.

@article{yant_orchestration_2010,
	title = {Orchestration of the floral transition and floral development in {Arabidopsis} by the bifunctional transcription factor {APETALA2}},
	volume = {22},
	issn = {1532-298X},
	doi = {10/bqpgn4},
	abstract = {The Arabidopsis thaliana transcription factor APETALA2 (AP2) has numerous functions, including roles in seed development, stem cell maintenance, and specification of floral organ identity. To understand the relationship between these different roles, we mapped direct targets of AP2 on a genome-wide scale in two tissue types. We find that AP2 binds to thousands of loci in the developing flower, many of which exhibit AP2-dependent transcription. Opposing, logical effects are evident in AP2 binding to two microRNA genes that influence AP2 expression, with AP2 positively regulating miR156 and negatively regulating miR172, forming a complex direct feedback loop, which also included all but one of the AP2-like miR172 target clade members. We compare the genome-wide direct target repertoire of AP2 with that of SCHLAFMUTZE, a closely related transcription factor that also represses the transition to flowering. We detect clear similarities and important differences in the direct target repertoires that are also tissue specific. Finally, using an inducible expression system, we demonstrate that AP2 has dual molecular roles. It functions as both a transcriptional activator and repressor, directly inducing the expression of the floral repressor AGAMOUS-LIKE15 and directly repressing the transcription of floral activators like SUPPRESSOR OF OVEREXPRESSION OF CONSTANS1.},
	language = {eng},
	number = {7},
	journal = {The Plant Cell},
	author = {Yant, Levi and Mathieu, Johannes and Dinh, Thanh Theresa and Ott, Felix and Lanz, Christa and Wollmann, Heike and Chen, Xuemei and Schmid, Markus},
	month = jul,
	year = {2010},
	pmid = {20675573},
	pmcid = {PMC2929098},
	keywords = {Arabidopsis, Arabidopsis Proteins, Binding Sites, Flowers, Gene Expression, Genome, Plant, Homeodomain Proteins, Mutation, Nuclear Proteins},
	pages = {2156--2170},
}

The Arabidopsis thaliana transcription factor APETALA2 (AP2) has numerous functions, including roles in seed development, stem cell maintenance, and specification of floral organ identity. To understand the relationship between these different roles, we mapped direct targets of AP2 on a genome-wide scale in two tissue types. We find that AP2 binds to thousands of loci in the developing flower, many of which exhibit AP2-dependent transcription. Opposing, logical effects are evident in AP2 binding to two microRNA genes that influence AP2 expression, with AP2 positively regulating miR156 and negatively regulating miR172, forming a complex direct feedback loop, which also included all but one of the AP2-like miR172 target clade members. We compare the genome-wide direct target repertoire of AP2 with that of SCHLAFMUTZE, a closely related transcription factor that also represses the transition to flowering. We detect clear similarities and important differences in the direct target repertoires that are also tissue specific. Finally, using an inducible expression system, we demonstrate that AP2 has dual molecular roles. It functions as both a transcriptional activator and repressor, directly inducing the expression of the floral repressor AGAMOUS-LIKE15 and directly repressing the transcription of floral activators like SUPPRESSOR OF OVEREXPRESSION OF CONSTANS1.

@article{wahl_fantastic_2010,
	title = {The {FANTASTIC} {FOUR} proteins influence shoot meristem size in {Arabidopsis} thaliana},
	volume = {10},
	issn = {1471-2229},
	doi = {10/dt2kjb},
	abstract = {BACKGROUND: Throughout their lives plants produce new organs from groups of pluripotent cells called meristems, located at the tips of the shoot and the root. The size of the shoot meristem is tightly controlled by a feedback loop, which involves the homeodomain transcription factor WUSCHEL (WUS) and the CLAVATA (CLV) proteins. This regulatory circuit is further fine-tuned by morphogenic signals such as hormones and sugars.
RESULTS: Here we show that a family of four plant-specific proteins, encoded by the FANTASTIC FOUR (FAF) genes, has the potential to regulate shoot meristem size in Arabidopsis thaliana. FAF2 and FAF4 are expressed in the centre of the shoot meristem, overlapping with the site of WUS expression. Consistent with a regulatory interaction between the FAF gene family and WUS, our experiments indicate that the FAFs can repress WUS, which ultimately leads to an arrest of meristem activity in FAF overexpressing lines. The finding that meristematic expression of FAF2 and FAF4 is under negative control by CLV3 further supports the hypothesis that the FAFs are modulators of the genetic circuit that regulates the meristem.
CONCLUSION: This study reports the initial characterization of the Arabidopsis thaliana FAF gene family. Our data indicate that the FAF genes form a plant specific gene family, the members of which have the potential to regulate the size of the shoot meristem by modulating the CLV3-WUS feedback loop.},
	language = {eng},
	journal = {BMC plant biology},
	author = {Wahl, Vanessa and Brand, Luise H. and Guo, Ya-Long and Schmid, Markus},
	month = dec,
	year = {2010},
	pmid = {21176196},
	pmcid = {PMC3023791},
	keywords = {Arabidopsis, Arabidopsis Proteins, Flowers, Gene Expression Profiling, Gene Expression Regulation, Developmental, Gene Expression Regulation, Plant, Glucuronidase, Homeodomain Proteins, In Situ Hybridization, Meristem, Microscopy, Electron, Scanning, Oligonucleotide Array Sequence Analysis, Plant Shoots, Plant Vascular Bundle, Repressor Proteins},
	pages = {285},
}

BACKGROUND: Throughout their lives plants produce new organs from groups of pluripotent cells called meristems, located at the tips of the shoot and the root. The size of the shoot meristem is tightly controlled by a feedback loop, which involves the homeodomain transcription factor WUSCHEL (WUS) and the CLAVATA (CLV) proteins. This regulatory circuit is further fine-tuned by morphogenic signals such as hormones and sugars. RESULTS: Here we show that a family of four plant-specific proteins, encoded by the FANTASTIC FOUR (FAF) genes, has the potential to regulate shoot meristem size in Arabidopsis thaliana. FAF2 and FAF4 are expressed in the centre of the shoot meristem, overlapping with the site of WUS expression. Consistent with a regulatory interaction between the FAF gene family and WUS, our experiments indicate that the FAFs can repress WUS, which ultimately leads to an arrest of meristem activity in FAF overexpressing lines. The finding that meristematic expression of FAF2 and FAF4 is under negative control by CLV3 further supports the hypothesis that the FAFs are modulators of the genetic circuit that regulates the meristem. CONCLUSION: This study reports the initial characterization of the Arabidopsis thaliana FAF gene family. Our data indicate that the FAF genes form a plant specific gene family, the members of which have the potential to regulate the size of the shoot meristem by modulating the CLV3-WUS feedback loop.

@article{yant_just_2009,
	title = {Just say no: floral repressors help {Arabidopsis} bide the time},
	volume = {12},
	issn = {1879-0356},
	shorttitle = {Just say no},
	doi = {10/cnm97d},
	abstract = {Floral repressors ensure correct reproductive timing by safeguarding against premature flowering. In the past decade, several mechanisms of floral repression have come to light. Discrimination between direct and indirect repressors has been facilitated by increasing the use of chromatin immunoprecipitation assays. Certain MADS-domain transcription factors such as SHORT VEGETATIVE PHASE and FLOWERING LOCUS C bind directly to target euchromatin to repress specific loci including FLOWERING LOCUS T (FT) and FD. The AP2-domain transcription factor TEMPRANILLO 1 has also been shown to directly repress FT by binding its 5' UTR. We highlight emerging systems level approaches, including genome-scale direct binding studies (ChIP-chip and ChIP-Seq), which stand out in their promise to elucidate the complex network underlying the transition to flowering at an unprecedented level.},
	language = {eng},
	number = {5},
	journal = {Current Opinion in Plant Biology},
	author = {Yant, Levi and Mathieu, Johannes and Schmid, Markus},
	month = oct,
	year = {2009},
	pmid = {19695946},
	keywords = {Arabidopsis, Arabidopsis Proteins, Chromatin Immunoprecipitation, Flowers, Gene Expression Regulation, Plant, MADS Domain Proteins, Plant Leaves, Plant Shoots, Repressor Proteins, Transcription Factors},
	pages = {580--586},
}

Floral repressors ensure correct reproductive timing by safeguarding against premature flowering. In the past decade, several mechanisms of floral repression have come to light. Discrimination between direct and indirect repressors has been facilitated by increasing the use of chromatin immunoprecipitation assays. Certain MADS-domain transcription factors such as SHORT VEGETATIVE PHASE and FLOWERING LOCUS C bind directly to target euchromatin to repress specific loci including FLOWERING LOCUS T (FT) and FD. The AP2-domain transcription factor TEMPRANILLO 1 has also been shown to directly repress FT by binding its 5' UTR. We highlight emerging systems level approaches, including genome-scale direct binding studies (ChIP-chip and ChIP-Seq), which stand out in their promise to elucidate the complex network underlying the transition to flowering at an unprecedented level.

@article{mathieu_repression_2009,
	title = {Repression of flowering by the {miR172} target {SMZ}},
	volume = {7},
	issn = {1545-7885},
	doi = {10/dcc259},
	abstract = {A small mobile protein, encoded by the FLOWERING LOCUS T (FT) locus, plays a central role in the control of flowering. FT is regulated positively by CONSTANS (CO), the output of the photoperiod pathway, and negatively by FLC, which integrates the effects of prolonged cold exposure. Here, we reveal the mechanisms of regulation by the microRNA miR172 target SCHLAFMUTZE (SMZ), a potent repressor of flowering. Whole-genome mapping of SMZ binding sites demonstrates not only direct regulation of FT, but also of many other flowering time regulators acting both upstream and downstream of FT, indicating an important role of miR172 and its targets in fine tuning the flowering response. A role for the miR172/SMZ module as a rheostat in flowering time is further supported by SMZ binding to several other genes encoding miR172 targets. Finally, we show that the action of SMZ is completely dependent on another floral repressor, FLM, providing the first direct connection between two important classes of flowering time regulators, AP2- and MADS-domain proteins.},
	language = {eng},
	number = {7},
	journal = {PLoS biology},
	author = {Mathieu, Johannes and Yant, Levi J. and Mürdter, Felix and Küttner, Frank and Schmid, Markus},
	month = jul,
	year = {2009},
	pmid = {19582143},
	pmcid = {PMC2701598},
	keywords = {Agrobacterium tumefaciens, Arabidopsis, Arabidopsis Proteins, Chromatin Immunoprecipitation, DNA-Binding Proteins, Flowers, Gene Expression Regulation, Plant, Genes, Reporter, MADS Domain Proteins, Meristem, MicroRNAs, Mutant Proteins, Oligonucleotide Array Sequence Analysis, Photoperiod, Plant Leaves, Plants, Genetically Modified, Protein Biosynthesis, RNA, Messenger, RNA, Plant, Reproduction, Transcription Factors, Transformation, Genetic},
	pages = {e1000148},
}

A small mobile protein, encoded by the FLOWERING LOCUS T (FT) locus, plays a central role in the control of flowering. FT is regulated positively by CONSTANS (CO), the output of the photoperiod pathway, and negatively by FLC, which integrates the effects of prolonged cold exposure. Here, we reveal the mechanisms of regulation by the microRNA miR172 target SCHLAFMUTZE (SMZ), a potent repressor of flowering. Whole-genome mapping of SMZ binding sites demonstrates not only direct regulation of FT, but also of many other flowering time regulators acting both upstream and downstream of FT, indicating an important role of miR172 and its targets in fine tuning the flowering response. A role for the miR172/SMZ module as a rheostat in flowering time is further supported by SMZ binding to several other genes encoding miR172 targets. Finally, we show that the action of SMZ is completely dependent on another floral repressor, FLM, providing the first direct connection between two important classes of flowering time regulators, AP2- and MADS-domain proteins.

@article{dohmann_auxin_2008,
	title = {Auxin {Responses} in {Mutants} of the {Arabidopsis} {CONSTITUTIVE} {PHOTOMORPHOGENIC9} {Signalosome}},
	volume = {147},
	issn = {0032-0889},
	url = {https://www.ncbi.nlm.nih.gov/pmc/articles/PMC2442533/},
	doi = {10.1104/pp.108.121061},
	abstract = {The CONSTITUTIVE PHOTOMORPHOGENIC9 (COP9) signalosome (CSN) is an evolutionarily conserved multiprotein complex that interacts with cullin-RING type E3 ubiquitin ligases (CRLs). CSN subunit 5 (CSN5), which, when incorporated into CSN, can deconjugate the NEDD8 modification from the cullin subunit of CRLs, is essential for CSN's role in controlling CRL activity. Whether the CSN5 monomer, which is maintained in csn mutants such as csn3 or csn4, has a functional role, remains to be established. We performed a comparative gene expression-profiling experiment with Arabidopsis (Arabidopsis thaliana) csn3, csn4, and csn5 mutants, and we show here that these mutants cannot be distinguished at the transcriptional level. Furthermore, we show that csn3 csn5 mutants are morphologically indistinguishable from csn3 or csn5 mutants. Taken together, these data suggest that the CSN5 monomer does not have a function that leads to transcriptional or morphological changes in the csn mutants. We further examined auxin responses in csn mutants. Whereas CSN had previously been shown to be required for the auxin response-regulatory E3 complexes, specifically SCFTIR1, the csn mutant phenotype suggests that CSN is not essential for auxin responses. We present physiological and genetic data that indicate that auxin responses are indeed only partially impaired in csn mutants and that this is not the result of maternally contributed CSN. Finally, we discuss these findings in the context of the current understanding of the role of neddylation and CSN-mediated deneddylation for CRL activity.},
	number = {3},
	urldate = {2021-10-22},
	journal = {Plant Physiology},
	author = {Dohmann, Esther Mirjam Natascha and Levesque, Mitchell Paul and Isono, Erika and Schmid, Markus and Schwechheimer, Claus},
	month = jul,
	year = {2008},
	pmid = {18467458},
	pmcid = {PMC2442533},
	pages = {1369--1379},
}

The CONSTITUTIVE PHOTOMORPHOGENIC9 (COP9) signalosome (CSN) is an evolutionarily conserved multiprotein complex that interacts with cullin-RING type E3 ubiquitin ligases (CRLs). CSN subunit 5 (CSN5), which, when incorporated into CSN, can deconjugate the NEDD8 modification from the cullin subunit of CRLs, is essential for CSN's role in controlling CRL activity. Whether the CSN5 monomer, which is maintained in csn mutants such as csn3 or csn4, has a functional role, remains to be established. We performed a comparative gene expression-profiling experiment with Arabidopsis (Arabidopsis thaliana) csn3, csn4, and csn5 mutants, and we show here that these mutants cannot be distinguished at the transcriptional level. Furthermore, we show that csn3 csn5 mutants are morphologically indistinguishable from csn3 or csn5 mutants. Taken together, these data suggest that the CSN5 monomer does not have a function that leads to transcriptional or morphological changes in the csn mutants. We further examined auxin responses in csn mutants. Whereas CSN had previously been shown to be required for the auxin response-regulatory E3 complexes, specifically SCFTIR1, the csn mutant phenotype suggests that CSN is not essential for auxin responses. We present physiological and genetic data that indicate that auxin responses are indeed only partially impaired in csn mutants and that this is not the result of maternally contributed CSN. Finally, we discuss these findings in the context of the current understanding of the role of neddylation and CSN-mediated deneddylation for CRL activity.

@article{helm_kdel-tailed_2008,
	title = {{KDEL}-tailed cysteine endopeptidases involved in programmed cell death, intercalation of new cells, and dismantling of extensin scaffolds},
	volume = {95},
	copyright = {© 2008 Botanical Society of America},
	issn = {1537-2197},
	url = {https://bsapubs.onlinelibrary.wiley.com/doi/abs/10.3732/ajb.2007404},
	doi = {10/ddb996},
	abstract = {KDEL-tailed cysteine endopeptidases are a group of papain-type peptidases found in senescing tissue undergoing programmed cell death (PCD). Their genes have so far been cloned and analyzed in 12 angiosperms. They are synthesized as proenzymes with a C-terminal KDEL endoplasmatic reticulum retention signal, which is removed with the prosequence to activate enzyme activity. We previously identified three genes for KDEL-tailed cysteine endopeptidases (AtCEP1, AtCEP2, AtCEP3) in Arabidopsis thaliana. Transgenic plants of A. thaliana expressing β-glucuronidase (GUS) under the control of the promoters for the three genes were produced and analyzed histochemically. GUS activity was promoter- and tissue-specific GUS activity during seedling, flower, and root development, especially in tissues that collapse during final stages of PCD, and in the course of lateral root formation. KDEL-tailed cysteine endopeptidases are unique in being able to digest the extensins that form the basic scaffold for cell wall formation. The broad substrate specificity is due to the structure of the active site cleft of the KDEL-tailed cysteine endopeptidase that accepts a wide variety of amino acids, including proline and glycosylated hydroxyproline of the hydroxyproline rich glycoproteins of the cell wall.},
	language = {en},
	number = {9},
	urldate = {2021-06-10},
	journal = {American Journal of Botany},
	author = {Helm, Michael and Schmid, Markus and Hierl, Georg and Terneus, Kimberly and Tan, Li and Lottspeich, Friedrich and Kieliszewski, Marcia J. and Gietl, Christine},
	year = {2008},
	note = {\_eprint: https://bsapubs.onlinelibrary.wiley.com/doi/pdf/10.3732/ajb.2007404},
	keywords = {Arabidopsis thaliana, Brassicaceae, Euphorbiaceae, KDEL-tailed cysteine endopeptidases, Ricinus communis, cell wall degradation, development in generative and vegetative tissues, programmed cell death, ricinosome, β-glucuronidase (GUS)},
	pages = {1049--1062},
}

KDEL-tailed cysteine endopeptidases are a group of papain-type peptidases found in senescing tissue undergoing programmed cell death (PCD). Their genes have so far been cloned and analyzed in 12 angiosperms. They are synthesized as proenzymes with a C-terminal KDEL endoplasmatic reticulum retention signal, which is removed with the prosequence to activate enzyme activity. We previously identified three genes for KDEL-tailed cysteine endopeptidases (AtCEP1, AtCEP2, AtCEP3) in Arabidopsis thaliana. Transgenic plants of A. thaliana expressing β-glucuronidase (GUS) under the control of the promoters for the three genes were produced and analyzed histochemically. GUS activity was promoter- and tissue-specific GUS activity during seedling, flower, and root development, especially in tissues that collapse during final stages of PCD, and in the course of lateral root formation. KDEL-tailed cysteine endopeptidases are unique in being able to digest the extensins that form the basic scaffold for cell wall formation. The broad substrate specificity is due to the structure of the active site cleft of the KDEL-tailed cysteine endopeptidase that accepts a wide variety of amino acids, including proline and glycosylated hydroxyproline of the hydroxyproline rich glycoproteins of the cell wall.

@article{dohmann_arabidopsis_2008,
	title = {The {Arabidopsis} {COP9} signalosome is essential for {G2} phase progression and genomic stability},
	volume = {135},
	issn = {0950-1991},
	doi = {10/b8t2wz},
	abstract = {The COP9 signalosome (CSN) is required for the full activity of cullin-RING E3 ubiquitin ligases (CRLs) in eukaryotes. CSN exerts its function on CRLs by removing the ubiquitin-related NEDD8 conjugate from the cullin subunit of CRLs. CSN seems, thereby, to control CRL disassembly or CRL subunit stability. In Arabidopsis thaliana, loss of CSN function leads to constitutive photomorphogenic (cop) seedling development and a post-germination growth arrest. The underlying molecular cause of this growth arrest is currently unknown. Here, we show that Arabidopsis csn mutants are delayed in G2 phase progression. This cell cycle arrest correlates with the induction of the DNA damage response pathway and is suggestive of the activation of a DNA damage checkpoint. In support of this hypothesis, we detected gene conversion events in csn mutants that are indicative of DNA double-strand breaks. DNA damage is also apparent in mutants of the NEDD8 conjugation pathway and in mutants of the E3 ligase subunits CULLIN4, COP1 and DET1, which share phenotypes with csn mutants. In summary, our data suggest that Arabidopsis csn mutants undergo DNA damage, which might be the cause of the delay in G2 cell cycle progression.},
	language = {eng},
	number = {11},
	journal = {Development (Cambridge, England)},
	author = {Dohmann, Esther M. N. and Levesque, Mitchell P. and De Veylder, Lieven and Reichardt, Ilka and Jürgens, Gerd and Schmid, Markus and Schwechheimer, Claus},
	month = jun,
	year = {2008},
	pmid = {18434413},
	keywords = {ATP-Binding Cassette Transporters, Arabidopsis Proteins, COP9 Signalosome Complex, Cell Cycle, Cell Division, Cullin Proteins, Cyclin B, DNA Damage, Flow Cytometry, G2 Phase, Gene Expression Regulation, Developmental, Gene Expression Regulation, Plant, Genomic Instability, Immunoblotting, In Situ Nick-End Labeling, Intracellular Signaling Peptides and Proteins, Multiprotein Complexes, Nuclear Proteins, Oligonucleotide Array Sequence Analysis, Peptide Hydrolases, Plant Roots, Protein Kinases, Protein-Serine-Threonine Kinases, Seedlings, Ubiquitin-Protein Ligases, Ubiquitins},
	pages = {2013--2022},
}

The COP9 signalosome (CSN) is required for the full activity of cullin-RING E3 ubiquitin ligases (CRLs) in eukaryotes. CSN exerts its function on CRLs by removing the ubiquitin-related NEDD8 conjugate from the cullin subunit of CRLs. CSN seems, thereby, to control CRL disassembly or CRL subunit stability. In Arabidopsis thaliana, loss of CSN function leads to constitutive photomorphogenic (cop) seedling development and a post-germination growth arrest. The underlying molecular cause of this growth arrest is currently unknown. Here, we show that Arabidopsis csn mutants are delayed in G2 phase progression. This cell cycle arrest correlates with the induction of the DNA damage response pathway and is suggestive of the activation of a DNA damage checkpoint. In support of this hypothesis, we detected gene conversion events in csn mutants that are indicative of DNA double-strand breaks. DNA damage is also apparent in mutants of the NEDD8 conjugation pathway and in mutants of the E3 ligase subunits CULLIN4, COP1 and DET1, which share phenotypes with csn mutants. In summary, our data suggest that Arabidopsis csn mutants undergo DNA damage, which might be the cause of the delay in G2 cell cycle progression.

@article{henz_distinct_2007,
	title = {Distinct expression patterns of natural antisense transcripts in {Arabidopsis}},
	volume = {144},
	issn = {0032-0889},
	doi = {10/d6krth},
	abstract = {It has been shown that overlapping cis-natural antisense transcripts (cis-NATs) can form a regulatory circuit in which small RNAs derived from one transcript regulate stability of the other transcript, which manifests itself as anticorrelated expression. However, little is known about how widespread antagonistic expression of cis-NATs is. We have determined how frequently cis-NAT pairs, which make up 7.4\% of annotated transcription units in the Arabidopsis (Arabidopsis thaliana) genome, show anticorrelated expression patterns. Indeed, global expression profiles of pairs of cis-NATs on average have significantly lower pairwise Pearson correlation coefficients than other pairs of neighboring genes whose transcripts do not overlap. However, anticorrelated expression that is greater than expected by chance is found in only a small number of cis-NAT pairs. The degree of anticorrelation does not depend on the length of the overlap or on the distance of the 5' ends of the transcripts. Consistent with earlier findings, cis-NATs do not exhibit an increased likelihood to give rise to small RNAs, as determined from available small RNA sequences and massively parallel signature sequencing tags. However, the overlapping regions of cis-NATs appeared to be enriched for small RNA loci compared to nonoverlapping regions. Furthermore, expression of cis-NATs was not disproportionately affected in various RNA-silencing mutants. Our results demonstrate that there is a trend toward anticorrelated expression of cis-NAT pairs in Arabidopsis, but currently available data do not produce a strong signature of small RNA-mediated silencing for this process.},
	language = {eng},
	number = {3},
	journal = {Plant Physiology},
	author = {Henz, Stefan R. and Cumbie, Jason S. and Kasschau, Kristin D. and Lohmann, Jan U. and Carrington, James C. and Weigel, Detlef and Schmid, Markus},
	month = jul,
	year = {2007},
	pmid = {17496106},
	pmcid = {PMC1914114},
	keywords = {Arabidopsis, Gene Expression Regulation, Plant, Genome, Plant, Oligonucleotide Array Sequence Analysis, Promoter Regions, Genetic, RNA Interference, RNA, Antisense},
	pages = {1247--1255},
}

It has been shown that overlapping cis-natural antisense transcripts (cis-NATs) can form a regulatory circuit in which small RNAs derived from one transcript regulate stability of the other transcript, which manifests itself as anticorrelated expression. However, little is known about how widespread antagonistic expression of cis-NATs is. We have determined how frequently cis-NAT pairs, which make up 7.4% of annotated transcription units in the Arabidopsis (Arabidopsis thaliana) genome, show anticorrelated expression patterns. Indeed, global expression profiles of pairs of cis-NATs on average have significantly lower pairwise Pearson correlation coefficients than other pairs of neighboring genes whose transcripts do not overlap. However, anticorrelated expression that is greater than expected by chance is found in only a small number of cis-NAT pairs. The degree of anticorrelation does not depend on the length of the overlap or on the distance of the 5' ends of the transcripts. Consistent with earlier findings, cis-NATs do not exhibit an increased likelihood to give rise to small RNAs, as determined from available small RNA sequences and massively parallel signature sequencing tags. However, the overlapping regions of cis-NATs appeared to be enriched for small RNA loci compared to nonoverlapping regions. Furthermore, expression of cis-NATs was not disproportionately affected in various RNA-silencing mutants. Our results demonstrate that there is a trend toward anticorrelated expression of cis-NAT pairs in Arabidopsis, but currently available data do not produce a strong signature of small RNA-mediated silencing for this process.

@article{mathieu_export_2007,
	title = {Export of {FT} protein from phloem companion cells is sufficient for floral induction in {Arabidopsis}},
	volume = {17},
	issn = {0960-9822},
	doi = {10/bts4m3},
	abstract = {Several endogenous and environmental factors need to be integrated to time the onset of flowering. Genetic and molecular analyses, primarily in Arabidopsis thaliana and rice, have shown that CONSTANS (CO) and FLOWERING LOCUS T (FT) play central roles in photoperiod-dependent flowering. The overall picture is that CO acts in the phloem companion cells of leaves and that its main effect is to induce FT mRNA in these cells. Surprisingly, FT, a small globular protein of 20 kDa, interacts at the shoot apex with the bZIP transcription factor FLOWERING LOCUS D (FD) to induce downstream targets. Given that green fluorescent protein (GFP), which as a monomer is 27 kDa, can be easily exported to sink tissue including flowers when expressed in phloem companion cells, the latter finding strongly implied that FT protein is the mobile floral-inductive signal. In agreement with this hypothesis, an FT-GFP fusion, just like GFP, can be exported from the phloem of both rice and Arabidopsis. It has been unknown, however, whether mobile FT protein is sufficient for transmitting the flowering signal. Here we show that FT mRNA is required in phloem companion cells where it acts partially redundant with its paralog TWIN SISTER OF FT (TSF) to induce flowering. Furthermore, we have devised a method that uncouples FT mRNA and protein effects in vivo. We demonstrate that export of FT protein from phloem companion cells is sufficient to induce flowering.},
	language = {eng},
	number = {12},
	journal = {Current biology: CB},
	author = {Mathieu, Johannes and Warthmann, Norman and Küttner, Frank and Schmid, Markus},
	month = jun,
	year = {2007},
	pmid = {17540570},
	keywords = {Arabidopsis, Arabidopsis Proteins, Flowers, Gene Expression Regulation, Plant, Phloem, Phosphatidylethanolamine Binding Protein, RNA, Messenger, Signal Transduction},
	pages = {1055--1060},
}

Several endogenous and environmental factors need to be integrated to time the onset of flowering. Genetic and molecular analyses, primarily in Arabidopsis thaliana and rice, have shown that CONSTANS (CO) and FLOWERING LOCUS T (FT) play central roles in photoperiod-dependent flowering. The overall picture is that CO acts in the phloem companion cells of leaves and that its main effect is to induce FT mRNA in these cells. Surprisingly, FT, a small globular protein of 20 kDa, interacts at the shoot apex with the bZIP transcription factor FLOWERING LOCUS D (FD) to induce downstream targets. Given that green fluorescent protein (GFP), which as a monomer is 27 kDa, can be easily exported to sink tissue including flowers when expressed in phloem companion cells, the latter finding strongly implied that FT protein is the mobile floral-inductive signal. In agreement with this hypothesis, an FT-GFP fusion, just like GFP, can be exported from the phloem of both rice and Arabidopsis. It has been unknown, however, whether mobile FT protein is sufficient for transmitting the flowering signal. Here we show that FT mRNA is required in phloem companion cells where it acts partially redundant with its paralog TWIN SISTER OF FT (TSF) to induce flowering. Furthermore, we have devised a method that uncouples FT mRNA and protein effects in vivo. We demonstrate that export of FT protein from phloem companion cells is sufficient to induce flowering.

@article{schmid_gene_2005,
	title = {A gene expression map of {Arabidopsis} thaliana development},
	volume = {37},
	issn = {1061-4036},
	doi = {10.1038/ng1543},
	abstract = {Regulatory regions of plant genes tend to be more compact than those of animal genes, but the complement of transcription factors encoded in plant genomes is as large or larger than that found in those of animals. Plants therefore provide an opportunity to study how transcriptional programs control multicellular development. We analyzed global gene expression during development of the reference plant Arabidopsis thaliana in samples covering many stages, from embryogenesis to senescence, and diverse organs. Here, we provide a first analysis of this data set, which is part of the AtGenExpress expression atlas. We observed that the expression levels of transcription factor genes and signal transduction components are similar to those of metabolic genes. Examining the expression patterns of large gene families, we found that they are often more similar than would be expected by chance, indicating that many gene families have been co-opted for specific developmental processes.},
	language = {eng},
	number = {5},
	journal = {Nature Genetics},
	author = {Schmid, Markus and Davison, Timothy S. and Henz, Stefan R. and Pape, Utz J. and Demar, Monika and Vingron, Martin and Schölkopf, Bernhard and Weigel, Detlef and Lohmann, Jan U.},
	month = may,
	year = {2005},
	pmid = {15806101},
	keywords = {Arabidopsis, Gene Expression, Gene Expression Profiling, Genetic Markers},
	pages = {501--506},
}

Regulatory regions of plant genes tend to be more compact than those of animal genes, but the complement of transcription factors encoded in plant genomes is as large or larger than that found in those of animals. Plants therefore provide an opportunity to study how transcriptional programs control multicellular development. We analyzed global gene expression during development of the reference plant Arabidopsis thaliana in samples covering many stages, from embryogenesis to senescence, and diverse organs. Here, we provide a first analysis of this data set, which is part of the AtGenExpress expression atlas. We observed that the expression levels of transcription factor genes and signal transduction components are similar to those of metabolic genes. Examining the expression patterns of large gene families, we found that they are often more similar than would be expected by chance, indicating that many gene families have been co-opted for specific developmental processes.

@article{lempe_diversity_2005,
	title = {Diversity of flowering responses in wild {Arabidopsis} thaliana strains},
	volume = {1},
	issn = {1553-7390},
	doi = {10.1371/journal.pgen.0010006},
	abstract = {Although multiple environmental cues regulate the transition to flowering in Arabidopsis thaliana, previous studies have suggested that wild A. thaliana accessions fall primarily into two classes, distinguished by their requirement for vernalization (extended winter-like temperatures), which enables rapid flowering under long days. Much of the difference in vernalization response is apparently due to variation at two epistatically acting loci, FRI and FLC. We present the response of over 150 wild accessions to three different environmental variables. In long days, FLC is among those genes whose expression is most highly correlated with flowering. In short days, FRI and FLC are less important, although their contribution is still significant. In addition, there is considerable variation not only in vernalization response, but also in the response to differences in day length or ambient growth temperature. The identification of accessions that flower relatively early or late in specific environments suggests that many of the flowering-time pathways identified by mutagenesis, such as those that respond to day length, contribute to flowering-time variation in the wild. In contrast to differences in vernalization requirement, which are mainly mediated by FRI and FLC, it seems that variation in these other pathways is due to allelic effects at several different loci.},
	language = {eng},
	number = {1},
	journal = {PLoS genetics},
	author = {Lempe, Janne and Balasubramanian, Sureshkumar and Sureshkumar, Sridevi and Singh, Anandita and Schmid, Markus and Weigel, Detlef},
	month = jul,
	year = {2005},
	pmid = {16103920},
	pmcid = {PMC1183525},
	pages = {109--118},
}

Although multiple environmental cues regulate the transition to flowering in Arabidopsis thaliana, previous studies have suggested that wild A. thaliana accessions fall primarily into two classes, distinguished by their requirement for vernalization (extended winter-like temperatures), which enables rapid flowering under long days. Much of the difference in vernalization response is apparently due to variation at two epistatically acting loci, FRI and FLC. We present the response of over 150 wild accessions to three different environmental variables. In long days, FLC is among those genes whose expression is most highly correlated with flowering. In short days, FRI and FLC are less important, although their contribution is still significant. In addition, there is considerable variation not only in vernalization response, but also in the response to differences in day length or ambient growth temperature. The identification of accessions that flower relatively early or late in specific environments suggests that many of the flowering-time pathways identified by mutagenesis, such as those that respond to day length, contribute to flowering-time variation in the wild. In contrast to differences in vernalization requirement, which are mainly mediated by FRI and FLC, it seems that variation in these other pathways is due to allelic effects at several different loci.

@article{wigge_integration_2005,
	title = {Integration of spatial and temporal information during floral induction in {Arabidopsis}},
	volume = {309},
	issn = {1095-9203},
	doi = {10/c6nzdx},
	abstract = {Flowering of Arabidopsis is regulated by several environmental and endogenous signals. An important integrator of these inputs is the FLOWERING LOCUS T (FT) gene, which encodes a small, possibly mobile protein. A primary response to floral induction is the activation of FT RNA expression in leaves. Because flowers form at a distant site, the shoot apex, these data suggest that FT primarily controls the timing of flowering. Integration of temporal and spatial information is mediated in part by the bZIP transcription factor FD, which is already expressed at the shoot apex before floral induction. A complex of FT and FD proteins in turn can activate floral identity genes such as APETALA1 (AP1).},
	language = {eng},
	number = {5737},
	journal = {Science (New York, N.Y.)},
	author = {Wigge, Philip A. and Kim, Min Chul and Jaeger, Katja E. and Busch, Wolfgang and Schmid, Markus and Lohmann, Jan U. and Weigel, Detlef},
	month = aug,
	year = {2005},
	pmid = {16099980},
	keywords = {Arabidopsis, Arabidopsis Proteins, Chromatin Immunoprecipitation, DNA-Binding Proteins, Flowers, Gene Expression Regulation, Plant, Homeodomain Proteins, MADS Domain Proteins, Models, Biological, Mutation, Oligonucleotide Array Sequence Analysis, Phenotype, Plant Leaves, Plant Proteins, Plant Shoots, Protein Interaction Mapping, Recombinant Fusion Proteins, Signal Transduction, Time Factors, Transcription Factors, Transcription, Genetic, Two-Hybrid System Techniques},
	pages = {1056--1059},
}

Flowering of Arabidopsis is regulated by several environmental and endogenous signals. An important integrator of these inputs is the FLOWERING LOCUS T (FT) gene, which encodes a small, possibly mobile protein. A primary response to floral induction is the activation of FT RNA expression in leaves. Because flowers form at a distant site, the shoot apex, these data suggest that FT primarily controls the timing of flowering. Integration of temporal and spatial information is mediated in part by the bZIP transcription factor FD, which is already expressed at the shoot apex before floral induction. A complex of FT and FD proteins in turn can activate floral identity genes such as APETALA1 (AP1).

@article{schwab_specific_2005,
	title = {Specific effects of {microRNAs} on the plant transcriptome},
	volume = {8},
	issn = {1534-5807},
	doi = {10.1016/j.devcel.2005.01.018},
	abstract = {Most plant microRNAs (miRNAs) have perfect or near-perfect complementarity with their targets. This is consistent with their primary mode of action being cleavage of target mRNAs, similar to that induced by perfectly complementary small interfering RNAs (siRNAs). However, there are natural targets with up to five mismatches. Furthermore, artificial siRNAs can have substantial effects on so-called off-targets, to which they have only limited complementarity. By analyzing the transcriptome of plants overexpressing different miRNAs, we have deduced a set of empirical parameters for target recognition. Compared to artificial siRNAs, authentic plant miRNAs appear to have much higher specificity, which may reflect their coevolution with the remainder of the transcriptome. We also demonstrate that miR172, previously thought to act primarily by translational repression, can efficiently guide mRNA cleavage, although the effects on steady-state levels of target transcripts are obscured by strong feedback regulation. This finding unifies the view of plant miRNA action.},
	language = {eng},
	number = {4},
	journal = {Developmental Cell},
	author = {Schwab, Rebecca and Palatnik, Javier F. and Riester, Markus and Schommer, Carla and Schmid, Markus and Weigel, Detlef},
	month = apr,
	year = {2005},
	pmid = {15809034},
	keywords = {Base Pairing, Base Sequence, Gene Expression Profiling, Gene Expression Regulation, Plant, MicroRNAs, Nucleic Acid Conformation, Oligonucleotide Array Sequence Analysis, Phenotype, Plant Proteins, Plants, Genetically Modified, RNA, Plant, Reproducibility of Results, Transcription, Genetic},
	pages = {517--527},
}

Most plant microRNAs (miRNAs) have perfect or near-perfect complementarity with their targets. This is consistent with their primary mode of action being cleavage of target mRNAs, similar to that induced by perfectly complementary small interfering RNAs (siRNAs). However, there are natural targets with up to five mismatches. Furthermore, artificial siRNAs can have substantial effects on so-called off-targets, to which they have only limited complementarity. By analyzing the transcriptome of plants overexpressing different miRNAs, we have deduced a set of empirical parameters for target recognition. Compared to artificial siRNAs, authentic plant miRNAs appear to have much higher specificity, which may reflect their coevolution with the remainder of the transcriptome. We also demonstrate that miR172, previously thought to act primarily by translational repression, can efficiently guide mRNA cleavage, although the effects on steady-state levels of target transcripts are obscured by strong feedback regulation. This finding unifies the view of plant miRNA action.

@article{schumann_athpex10_2003,
	title = {{AthPEX10}, a nuclear gene essential for peroxisome and storage organelle formation during {Arabidopsis} embryogenesis},
	volume = {100},
	issn = {0027-8424},
	doi = {10/dzx29q},
	abstract = {In yeasts and mammals, PEX10 encodes an integral membrane protein with a C3HC4 RING finger motif in its C-terminal domain and is required for peroxisome biogenesis and matrix protein import. In humans, its dysfunction in peroxisome biogenesis leads to severe Zellweger Syndrome and infantile Refsum disease. Here we show that dysfunction of a homologous gene in Arabidopsis leads to lethality at the heart stage of embryogenesis, impairing the biogenesis of peroxisomes, lipid bodies, and protein bodies. In a T-DNA insertion mutant disrupting the fourth exon of the AthPEX10 gene, ultrastructural analyses fail to detect peroxisomes characteristic for wild-type embryogenesis. Storage triacyl glycerides are not assembled into lipid bodies (oil bodies; oleosomes) surrounded by the phospholipid-protein monolayer membrane. Instead, the dysfunctional monolayer membranes, which derive from the bilayer membrane of the endoplasmic reticulum, accumulate in the cytosol. Concomitantly the transfer of the storage proteins from their site of synthesis at the endoplasmic reticulum to the vacuoles is disturbed. The mutant can be rescued by transformation with wild-type AthPEX10 cDNA. Transformants of wild-type Hansenula polymorpha cells with the AthPEX10 cDNA did produce the encoded protein without targeting it to peroxisomes. Additionally, the cDNA could not complement a Hansenula pex10 mutant unable to form peroxisomes. The ultrastructural knockout phenotype of AthPEX10p suggests that this protein in Arabidopsis is essential for peroxisome, oleosome, and protein transport vesicle formation.},
	language = {eng},
	number = {16},
	journal = {Proceedings of the National Academy of Sciences of the United States of America},
	author = {Schumann, Uwe and Wanner, Gerhard and Veenhuis, Marten and Schmid, Markus and Gietl, Christine},
	month = aug,
	year = {2003},
	pmid = {12883010},
	pmcid = {PMC170968},
	keywords = {Amino Acid Sequence, Arabidopsis, Arabidopsis Proteins, Carrier Proteins, Cell Membrane, Cell Nucleus, Cytosol, DNA, Complementary, Endoplasmic Reticulum, Exons, Lipid Bilayers, Lipid Metabolism, Membrane Transport Proteins, Microscopy, Electron, Molecular Sequence Data, Mutation, Organelles, Peroxins, Peroxisomes, Phospholipids, Plants, Genetically Modified, Protein Structure, Tertiary, Receptors, Cytoplasmic and Nuclear},
	pages = {9626--9631},
}

In yeasts and mammals, PEX10 encodes an integral membrane protein with a C3HC4 RING finger motif in its C-terminal domain and is required for peroxisome biogenesis and matrix protein import. In humans, its dysfunction in peroxisome biogenesis leads to severe Zellweger Syndrome and infantile Refsum disease. Here we show that dysfunction of a homologous gene in Arabidopsis leads to lethality at the heart stage of embryogenesis, impairing the biogenesis of peroxisomes, lipid bodies, and protein bodies. In a T-DNA insertion mutant disrupting the fourth exon of the AthPEX10 gene, ultrastructural analyses fail to detect peroxisomes characteristic for wild-type embryogenesis. Storage triacyl glycerides are not assembled into lipid bodies (oil bodies; oleosomes) surrounded by the phospholipid-protein monolayer membrane. Instead, the dysfunctional monolayer membranes, which derive from the bilayer membrane of the endoplasmic reticulum, accumulate in the cytosol. Concomitantly the transfer of the storage proteins from their site of synthesis at the endoplasmic reticulum to the vacuoles is disturbed. The mutant can be rescued by transformation with wild-type AthPEX10 cDNA. Transformants of wild-type Hansenula polymorpha cells with the AthPEX10 cDNA did produce the encoded protein without targeting it to peroxisomes. Additionally, the cDNA could not complement a Hansenula pex10 mutant unable to form peroxisomes. The ultrastructural knockout phenotype of AthPEX10p suggests that this protein in Arabidopsis is essential for peroxisome, oleosome, and protein transport vesicle formation.

@article{schmid_dissection_2003,
	title = {Dissection of floral induction pathways using global expression analysis},
	volume = {130},
	issn = {0950-1991},
	doi = {10/c56qz2},
	abstract = {Flowering of the reference plant Arabidopsis thaliana is controlled by several signaling pathways, which converge on a small set of genes that function as pathway integrators. We have analyzed the genomic response to one type of floral inductive signal, photoperiod, to dissect the function of several genes transducing this stimulus, including CONSTANS, thought to be the major output of the photoperiod pathway. Comparing the effects of CONSTANS with those of FLOWERING LOCUS T, which integrates inputs from CONSTANS and other floral inductive pathways, we find that expression profiles of shoot apices from plants with mutations in either gene are very similar. In contrast, a mutation in LEAFY, which also acts downstream of CONSTANS, has much more limited effects. Another pathway integrator, SUPPRESSOR OF OVEREXPRESSION OF CO 1, is responsive to acute induction by photoperiod even in the presence of the floral repressor encoded by FLOWERING LOCUS C. We have discovered a large group of potential floral repressors that are down-regulated upon photoperiodic induction. These include two AP2 domain-encoding genes that can repress flowering. The two paralogous genes, SCHLAFMUTZE and SCHNARCHZAPFEN, share a signature with partial complementarity to the miR172 microRNA, whose precursor we show to be induced upon flowering. These and related findings on SPL genes suggest that microRNAs play an important role in the regulation of flowering.},
	language = {eng},
	number = {24},
	journal = {Development (Cambridge, England)},
	author = {Schmid, Markus and Uhlenhaut, N. Henriette and Godard, François and Demar, Monika and Bressan, Ray and Weigel, Detlef and Lohmann, Jan U.},
	month = dec,
	year = {2003},
	pmid = {14573523},
	keywords = {Animals, Arabidopsis, Arabidopsis Proteins, DNA-Binding Proteins, Flowers, Gene Expression Profiling, Gene Expression Regulation, Plant, MicroRNAs, Photoperiod, Polymorphism, Genetic, Signal Transduction, Statistics as Topic, Transcription Factors},
	pages = {6001--6012},
}

Flowering of the reference plant Arabidopsis thaliana is controlled by several signaling pathways, which converge on a small set of genes that function as pathway integrators. We have analyzed the genomic response to one type of floral inductive signal, photoperiod, to dissect the function of several genes transducing this stimulus, including CONSTANS, thought to be the major output of the photoperiod pathway. Comparing the effects of CONSTANS with those of FLOWERING LOCUS T, which integrates inputs from CONSTANS and other floral inductive pathways, we find that expression profiles of shoot apices from plants with mutations in either gene are very similar. In contrast, a mutation in LEAFY, which also acts downstream of CONSTANS, has much more limited effects. Another pathway integrator, SUPPRESSOR OF OVEREXPRESSION OF CO 1, is responsive to acute induction by photoperiod even in the presence of the floral repressor encoded by FLOWERING LOCUS C. We have discovered a large group of potential floral repressors that are down-regulated upon photoperiodic induction. These include two AP2 domain-encoding genes that can repress flowering. The two paralogous genes, SCHLAFMUTZE and SCHNARCHZAPFEN, share a signature with partial complementarity to the miR172 microRNA, whose precursor we show to be induced upon flowering. These and related findings on SPL genes suggest that microRNAs play an important role in the regulation of flowering.

@article{alonso_genome-wide_2003,
	title = {Genome-wide insertional mutagenesis of {Arabidopsis} thaliana},
	volume = {301},
	issn = {1095-9203},
	doi = {10/fqhtnq},
	abstract = {Over 225,000 independent Agrobacterium transferred DNA (T-DNA) insertion events in the genome of the reference plant Arabidopsis thaliana have been created that represent near saturation of the gene space. The precise locations were determined for more than 88,000 T-DNA insertions, which resulted in the identification of mutations in more than 21,700 of the approximately 29,454 predicted Arabidopsis genes. Genome-wide analysis of the distribution of integration events revealed the existence of a large integration site bias at both the chromosome and gene levels. Insertion mutations were identified in genes that are regulated in response to the plant hormone ethylene.},
	language = {eng},
	number = {5633},
	journal = {Science (New York, N.Y.)},
	author = {Alonso, José M. and Stepanova, Anna N. and Leisse, Thomas J. and Kim, Christopher J. and Chen, Huaming and Shinn, Paul and Stevenson, Denise K. and Zimmerman, Justin and Barajas, Pascual and Cheuk, Rosa and Gadrinab, Carmelita and Heller, Collen and Jeske, Albert and Koesema, Eric and Meyers, Cristina C. and Parker, Holly and Prednis, Lance and Ansari, Yasser and Choy, Nathan and Deen, Hashim and Geralt, Michael and Hazari, Nisha and Hom, Emily and Karnes, Meagan and Mulholland, Celene and Ndubaku, Ral and Schmidt, Ian and Guzman, Plinio and Aguilar-Henonin, Laura and Schmid, Markus and Weigel, Detlef and Carter, David E. and Marchand, Trudy and Risseeuw, Eddy and Brogden, Debra and Zeko, Albana and Crosby, William L. and Berry, Charles C. and Ecker, Joseph R.},
	month = aug,
	year = {2003},
	pmid = {12893945},
	keywords = {3' Untranslated Regions, 5' Untranslated Regions, Alleles, Arabidopsis, Arabidopsis Proteins, Base Composition, Chromosomes, Plant, DNA, Bacterial, DNA, Plant, Ethylenes, Exons, Expressed Sequence Tags, Gene Expression, Gene Expression Profiling, Gene Expression Regulation, Plant, Genes, Plant, Genome, Plant, Introns, Mutagenesis, Insertional, Mutation, Oligonucleotide Array Sequence Analysis, Promoter Regions, Genetic, Recombination, Genetic, Rhizobium},
	pages = {653--657},
}

Over 225,000 independent Agrobacterium transferred DNA (T-DNA) insertion events in the genome of the reference plant Arabidopsis thaliana have been created that represent near saturation of the gene space. The precise locations were determined for more than 88,000 T-DNA insertions, which resulted in the identification of mutations in more than 21,700 of the approximately 29,454 predicted Arabidopsis genes. Genome-wide analysis of the distribution of integration events revealed the existence of a large integration site bias at both the chromosome and gene levels. Insertion mutations were identified in genes that are regulated in response to the plant hormone ethylene.

@article{gietl_ricinosomes_2001,
	title = {Ricinosomes: an organelle for developmentally regulated programmed cell death in senescing plant tissues},
	volume = {88},
	issn = {1432-1904},
	shorttitle = {Ricinosomes},
	url = {https://doi.org/10.1007/s001140000203},
	doi = {10.1007/s001140000203},
	abstract = {This review describes aspects of programmed cell death (PCD). Present research maps the enzymes involved and explores the signal transduction pathways involved in their synthesis. A special organelle (the ricinosome) has been discovered in the senescing endosperm of germinating castor beans (Ricinus communis) that develops at the beginning of PCD and delivers large amounts of a papain-type cysteine endopeptidase (CysEP) in the final stages of cellular disintegration. Castor beans store oil and proteins in a living endosperm surrounding the cotyledons. These stores are mobilized during germination and transferred into the cotyledons. PCD is initiated after this transfer is complete. The CysEP is synthesized in the lumen of the endoplasmic reticulum (ER) where it is retained by its C-terminal KDEL peptide as a rather inactive pro-enzyme. Large number of ricinosomes bud from the ER at the same time as the nuclear DNA is characteristically fragmented during PCD. The mitochondria, glyoxysomes and ribosomes are degraded in autophagic vacuoles, while the endopeptidase is activated by removal of the propeptide and the KDEL tail and enters the cytosol. The endosperm dries and detaches from the cotyledons. A homologous KDEL-tailed cysteine endopeptidase has been found in several senescing tissues; it has been localized in ricinosomes of withering day-lily petals and dying seed coats. Three genes for a KDEL-tailed cysteine endopeptidase have been identified in Arabidopsis. One is expressed in senescing ovules, the second in the vascular vessels and the third in maturing siliques. These genes open the way to exploring PCD in plants.},
	language = {en},
	number = {2},
	urldate = {2021-10-22},
	journal = {Naturwissenschaften},
	author = {Gietl, C. and Schmid, M.},
	month = feb,
	year = {2001},
	pages = {49--58},
}

This review describes aspects of programmed cell death (PCD). Present research maps the enzymes involved and explores the signal transduction pathways involved in their synthesis. A special organelle (the ricinosome) has been discovered in the senescing endosperm of germinating castor beans (Ricinus communis) that develops at the beginning of PCD and delivers large amounts of a papain-type cysteine endopeptidase (CysEP) in the final stages of cellular disintegration. Castor beans store oil and proteins in a living endosperm surrounding the cotyledons. These stores are mobilized during germination and transferred into the cotyledons. PCD is initiated after this transfer is complete. The CysEP is synthesized in the lumen of the endoplasmic reticulum (ER) where it is retained by its C-terminal KDEL peptide as a rather inactive pro-enzyme. Large number of ricinosomes bud from the ER at the same time as the nuclear DNA is characteristically fragmented during PCD. The mitochondria, glyoxysomes and ribosomes are degraded in autophagic vacuoles, while the endopeptidase is activated by removal of the propeptide and the KDEL tail and enters the cytosol. The endosperm dries and detaches from the cotyledons. A homologous KDEL-tailed cysteine endopeptidase has been found in several senescing tissues; it has been localized in ricinosomes of withering day-lily petals and dying seed coats. Three genes for a KDEL-tailed cysteine endopeptidase have been identified in Arabidopsis. One is expressed in senescing ovules, the second in the vascular vessels and the third in maturing siliques. These genes open the way to exploring PCD in plants.

@article{schmid_ricinosomes_2001,
	title = {The ricinosomes of senescing plant tissue bud from the endoplasmic reticulum},
	volume = {98},
	copyright = {Copyright © 2001, The National Academy of Sciences},
	issn = {0027-8424, 1091-6490},
	url = {https://www.pnas.org/content/98/9/5353},
	doi = {10.1073/pnas.061038298},
	abstract = {The ricinosome (synonym, precursor protease vesicle) is a novel organelle, found so far exclusively in plant cells. Electron microscopic studies suggest that it buds off from the endoplasmic reticulum in senescing tissues. Biochemical support for this unusual origin now comes from the composition of the purified organelle, which contains large amounts of a 45-kDa cysteine endoprotease precursor with a C-terminal KDEL motif and the endoplasmic reticulum lumen residents BiP (binding protein) and protein disulfide isomerase. Western blot analysis, peptide sequencing, and mass spectrometry demonstrate retention of KDEL in the protease proform. Acidification of isolated ricinosomes causes castor bean cysteine endopeptidase activation, with cleavage of the N-terminal propeptide and the C-terminal KDEL motif. We propose that ricinosomes accumulate during senescence by programmed cell death and are activated by release of protons from acidic vacuoles.},
	language = {en},
	number = {9},
	urldate = {2021-11-02},
	journal = {Proceedings of the National Academy of Sciences},
	author = {Schmid, Markus and Simpson, David J. and Sarioglu, Hakan and Lottspeich, Friedrich and Gietl, Christine},
	month = apr,
	year = {2001},
	pmid = {11296243},
	note = {Publisher: National Academy of Sciences
Section: Biological Sciences},
	keywords = {Ricinus communis, papain-type KDEL peptidase},
	pages = {5353--5358},
}

The ricinosome (synonym, precursor protease vesicle) is a novel organelle, found so far exclusively in plant cells. Electron microscopic studies suggest that it buds off from the endoplasmic reticulum in senescing tissues. Biochemical support for this unusual origin now comes from the composition of the purified organelle, which contains large amounts of a 45-kDa cysteine endoprotease precursor with a C-terminal KDEL motif and the endoplasmic reticulum lumen residents BiP (binding protein) and protein disulfide isomerase. Western blot analysis, peptide sequencing, and mass spectrometry demonstrate retention of KDEL in the protease proform. Acidification of isolated ricinosomes causes castor bean cysteine endopeptidase activation, with cleavage of the N-terminal propeptide and the C-terminal KDEL motif. We propose that ricinosomes accumulate during senescence by programmed cell death and are activated by release of protons from acidic vacuoles.

@article{schmid_programmed_1999,
	title = {Programmed cell death in castor bean endosperm is associated with the accumulation and release of a cysteine endopeptidase from ricinosomes},
	volume = {96},
	copyright = {Copyright © 1999, The National Academy of Sciences},
	issn = {0027-8424, 1091-6490},
	url = {https://www.pnas.org/content/96/24/14159},
	doi = {10/fwpzcr},
	abstract = {The cells of the endosperm of castor bean seeds (Ricinus communis) undergo programmed cell death during germination, after their oil and protein reserves have been mobilized. Nuclear DNA fragmentation first was observed at day 3 in the endosperm cells immediately adjacent to the cotyledons and progressed across to the outermost cell layers by day 5. We also detected the accumulation of small organelles known as ricinosomes, by using an antibody against a cysteine endoprotease. By the time the nuclear DNA was susceptible to heavy label by terminal deoxynucleotidyltransferase-mediated dUTP nick end labeling, the ricinosomes had released into the cytoplasm their content of cysteine endoprotease, which became activated because of the cleavage of its propeptide. The cysteine endoprotease is distinguished by a C-terminal KDEL sequence, although it is not retained in the lumen of the endoplasmic reticulum and is a marker for ricinosomes. Homologous proteases are found in the senescing tissues of other plants, including the petals of the daylily. Ricinosomes were identified in this tissue by electron microscopy and immunocytochemistry. It seems that ricinosomes are not unique to Ricinus and play an important role in the degradation of plant cell contents during programmed cell death.},
	language = {en},
	number = {24},
	urldate = {2021-11-08},
	journal = {Proceedings of the National Academy of Sciences},
	author = {Schmid, Markus and Simpson, David and Gietl, Christine},
	month = nov,
	year = {1999},
	pmid = {10570215},
	note = {Publisher: National Academy of Sciences
Section: Biological Sciences},
	keywords = {Apoptosis, Castor Bean, Cell Nucleus, Cysteine Endopeptidases, DNA Fragmentation, DNA, Plant, Germination, Hemerocallis sp., In Situ Hybridization, Organelles, Plants, Toxic, Ricinus communis, Seeds, papain-type KDEL peptidase},
	pages = {14159--14164},
}

The cells of the endosperm of castor bean seeds (Ricinus communis) undergo programmed cell death during germination, after their oil and protein reserves have been mobilized. Nuclear DNA fragmentation first was observed at day 3 in the endosperm cells immediately adjacent to the cotyledons and progressed across to the outermost cell layers by day 5. We also detected the accumulation of small organelles known as ricinosomes, by using an antibody against a cysteine endoprotease. By the time the nuclear DNA was susceptible to heavy label by terminal deoxynucleotidyltransferase-mediated dUTP nick end labeling, the ricinosomes had released into the cytoplasm their content of cysteine endoprotease, which became activated because of the cleavage of its propeptide. The cysteine endoprotease is distinguished by a C-terminal KDEL sequence, although it is not retained in the lumen of the endoplasmic reticulum and is a marker for ricinosomes. Homologous proteases are found in the senescing tissues of other plants, including the petals of the daylily. Ricinosomes were identified in this tissue by electron microscopy and immunocytochemistry. It seems that ricinosomes are not unique to Ricinus and play an important role in the degradation of plant cell contents during programmed cell death.

@article{schmid_cysteine_1998,
	title = {A cysteine endopeptidase with a {C}-terminal {KDEL} motif isolated from castor bean endosperm is a marker enzyme for the ricinosome, a putative lytic compartment},
	volume = {206},
	issn = {0032-0935},
	doi = {10.1007/s004250050423},
	abstract = {A papain-type cysteine endopeptidase with a molecular mass of 35 kDa for the mature enzyme, was purified from germinating castor bean (Ricinus communis L.) endosperm by virtue of its capacity to process the glyoxysomal malate dehydrogenase precursor protein to the mature subunit in vitro (C. Gietl et al., 1997, Plant Physiol 113: 863-871). The cDNA clones from endosperm of germinating seedlings and from developing seeds were isolated and sequence analysis revealed that a very similar or identical peptidase is synthesised in both tissues. Sequencing established a presequence for co-translational targeting into the endoplasmic reticulum, an N-terminal propeptide and a C-terminal KDEL motif for the castor bean cysteine endopeptidase precursor. The 45-kDa pro-enzyme stably present in isolated organelles was enzymatically active. Immunocytochemistry with antibodies raised against the purified cysteine endopeptidase revealed highly specific labelling of ricinosomes, organelles which co-purify with glyoxysomes from germinating Ricinus endosperm. The cysteine endopeptidase from castor bean endosperm, which represents a senescing tissue, is homologous to cysteine endopeptidases from other senescing tissues such as the cotyledons of germinating mung bean (Vigna mungo) and vetch (Vicia sativa), the seed pods of maturing French bean (Phaseolus vulgaris) and the flowers of daylily (Hemerocallis sp.).},
	language = {eng},
	number = {3},
	journal = {Planta},
	author = {Schmid, M. and Simpson, D. and Kalousek, F. and Gietl, C.},
	month = oct,
	year = {1998},
	pmid = {9763713},
	keywords = {Base Sequence, Biomarkers, Castor Bean, Cell Compartmentation, Centrifugation, Density Gradient, Cysteine Endopeptidases, DNA, Complementary, DNA, Plant, Enzyme Precursors, Molecular Sequence Data, Oligopeptides, Organelles, Plants, Toxic, Protein Sorting Signals, Sucrose},
	pages = {466--475},
}

A papain-type cysteine endopeptidase with a molecular mass of 35 kDa for the mature enzyme, was purified from germinating castor bean (Ricinus communis L.) endosperm by virtue of its capacity to process the glyoxysomal malate dehydrogenase precursor protein to the mature subunit in vitro (C. Gietl et al., 1997, Plant Physiol 113: 863-871). The cDNA clones from endosperm of germinating seedlings and from developing seeds were isolated and sequence analysis revealed that a very similar or identical peptidase is synthesised in both tissues. Sequencing established a presequence for co-translational targeting into the endoplasmic reticulum, an N-terminal propeptide and a C-terminal KDEL motif for the castor bean cysteine endopeptidase precursor. The 45-kDa pro-enzyme stably present in isolated organelles was enzymatically active. Immunocytochemistry with antibodies raised against the purified cysteine endopeptidase revealed highly specific labelling of ricinosomes, organelles which co-purify with glyoxysomes from germinating Ricinus endosperm. The cysteine endopeptidase from castor bean endosperm, which represents a senescing tissue, is homologous to cysteine endopeptidases from other senescing tissues such as the cotyledons of germinating mung bean (Vigna mungo) and vetch (Vicia sativa), the seed pods of maturing French bean (Phaseolus vulgaris) and the flowers of daylily (Hemerocallis sp.).

@article{wimmer_plant_1998,
	title = {The plant {PTS1} receptor: similarities and differences to its human and yeast counterparts},
	volume = {16},
	issn = {1365-313X},
	shorttitle = {The plant {PTS1} receptor},
	url = {https://onlinelibrary.wiley.com/doi/abs/10.1046/j.1365-313x.1998.00320.x},
	doi = {10.1046/j.1365-313x.1998.00320.x},
	abstract = {Two targeting signals, PTS1 and PTS2, mediate import of proteins into the peroxisomal matrix. We have cloned and sequenced the watermelon ( Citrullus vulgaris ) cDNA homologue to the PTS1 receptor gene (PEX5). Its gene product, CvPex5p, belongs to the family of tetratricopeptide repeat (TPR) containing proteins like the human and yeast counterparts, and exhibits 11 repeats of the sequence W-X2-(E/S)-(Y/F/Q) in its N-terminal half. According to fractionation studies the plant Pex5p is located mainly in the cytosolic fraction and therefore could function as a cycling receptor between the cytosol and glyoxysomes, as has been proposed for the Pex5p of human and some yeast peroxisomes. Transformation of the Hansenula polymorpha peroxisome deficient pex5 mutant with watermelon PEX5 resulted in restoration of peroxisome formation and the synthesis of additional membranes surrounding the peroxisomes. These structures are labeled in immunogold experiments using antibodies against the Hansenula polymorpha integral membrane protein Pex3p, confirming their peroxisomal nature. The plant Pex5p was localized by immunogold labelling mainly in the cytosol of the yeast, but also inside the newly formed peroxisomes. However, import of the PTS1 protein alcohol oxidase is only partially restored by CvPex5p.},
	language = {en},
	number = {4},
	urldate = {2021-10-22},
	journal = {The Plant Journal},
	author = {Wimmer, Christine and Schmid, Markus and Veenhuis, Marten and Gietl, Christine},
	year = {1998},
	note = {\_eprint: https://onlinelibrary.wiley.com/doi/pdf/10.1046/j.1365-313x.1998.00320.x},
	pages = {453--464},
}

Two targeting signals, PTS1 and PTS2, mediate import of proteins into the peroxisomal matrix. We have cloned and sequenced the watermelon ( Citrullus vulgaris ) cDNA homologue to the PTS1 receptor gene (PEX5). Its gene product, CvPex5p, belongs to the family of tetratricopeptide repeat (TPR) containing proteins like the human and yeast counterparts, and exhibits 11 repeats of the sequence W-X2-(E/S)-(Y/F/Q) in its N-terminal half. According to fractionation studies the plant Pex5p is located mainly in the cytosolic fraction and therefore could function as a cycling receptor between the cytosol and glyoxysomes, as has been proposed for the Pex5p of human and some yeast peroxisomes. Transformation of the Hansenula polymorpha peroxisome deficient pex5 mutant with watermelon PEX5 resulted in restoration of peroxisome formation and the synthesis of additional membranes surrounding the peroxisomes. These structures are labeled in immunogold experiments using antibodies against the Hansenula polymorpha integral membrane protein Pex3p, confirming their peroxisomal nature. The plant Pex5p was localized by immunogold labelling mainly in the cytosol of the yeast, but also inside the newly formed peroxisomes. However, import of the PTS1 protein alcohol oxidase is only partially restored by CvPex5p.