Marhava, Petra - Plant acclimation to heat and cold stress

@article{aliaga_fandino_ectopic_2024,
	title = {Ectopic assembly of an auxin efflux control machinery shifts developmental trajectories},
	volume = {36},
	issn = {1040-4651},
	url = {https://doi.org/10.1093/plcell/koae023},
	doi = {10.1093/plcell/koae023},
	abstract = {Polar auxin transport in the Arabidopsis (Arabidopsis thaliana) root tip maintains high auxin levels around the stem cell niche that gradually decrease in dividing cells but increase again once they transition toward differentiation. Protophloem differentiates earlier than other proximal tissues and employs a unique auxin “canalization” machinery that is thought to balance auxin efflux with retention. It consists of a proposed activator of PIN-FORMED (PIN) auxin efflux carriers, the cAMP-, cGMP- and Calcium-dependent (AGC) kinase PROTEIN KINASE ASSOCIATED WITH BRX (PAX); its inhibitor, BREVIS RADIX (BRX); and PHOSPHATIDYLINOSITOL-4-PHOSPHATE-5-KINASE (PIP5K) enzymes, which promote polar PAX and BRX localization. Because of a dynamic PAX–BRX–PIP5K interplay, the net cellular output of this machinery remains unclear. In this study, we deciphered the dosage-sensitive regulatory interactions among PAX, BRX, and PIP5K by their ectopic expression in developing xylem vessels. The data suggest that the dominant collective output of the PAX–BRX–PIP5K module is a localized reduction in PIN abundance. This requires PAX-stimulated clathrin-mediated PIN endocytosis upon site-specific phosphorylation, which distinguishes PAX from other AGC kinases. An ectopic assembly of the PAX–BRX–PIP5K module is sufficient to cause cellular auxin retention and affects root growth vigor by accelerating the trajectory of xylem vessel development. Our data thus provide direct evidence that local manipulation of auxin efflux alters the timing of cellular differentiation in the root.},
	number = {5},
	urldate = {2024-10-02},
	journal = {The Plant Cell},
	author = {Aliaga Fandino, Ana Cecilia and Jelínková, Adriana and Marhava, Petra and Petrášek, Jan and Hardtke, Christian S},
	month = may,
	year = {2024},
	pages = {1791--1805},
}

Polar auxin transport in the Arabidopsis (Arabidopsis thaliana) root tip maintains high auxin levels around the stem cell niche that gradually decrease in dividing cells but increase again once they transition toward differentiation. Protophloem differentiates earlier than other proximal tissues and employs a unique auxin “canalization” machinery that is thought to balance auxin efflux with retention. It consists of a proposed activator of PIN-FORMED (PIN) auxin efflux carriers, the cAMP-, cGMP- and Calcium-dependent (AGC) kinase PROTEIN KINASE ASSOCIATED WITH BRX (PAX); its inhibitor, BREVIS RADIX (BRX); and PHOSPHATIDYLINOSITOL-4-PHOSPHATE-5-KINASE (PIP5K) enzymes, which promote polar PAX and BRX localization. Because of a dynamic PAX–BRX–PIP5K interplay, the net cellular output of this machinery remains unclear. In this study, we deciphered the dosage-sensitive regulatory interactions among PAX, BRX, and PIP5K by their ectopic expression in developing xylem vessels. The data suggest that the dominant collective output of the PAX–BRX–PIP5K module is a localized reduction in PIN abundance. This requires PAX-stimulated clathrin-mediated PIN endocytosis upon site-specific phosphorylation, which distinguishes PAX from other AGC kinases. An ectopic assembly of the PAX–BRX–PIP5K module is sufficient to cause cellular auxin retention and affects root growth vigor by accelerating the trajectory of xylem vessel development. Our data thus provide direct evidence that local manipulation of auxin efflux alters the timing of cellular differentiation in the root.

@article{hoermayer_mechanical_2024,
	title = {Mechanical forces in plant tissue matrix orient cell divisions via microtubule stabilization},
	volume = {59},
	issn = {1534-5807},
	url = {https://www.sciencedirect.com/science/article/pii/S1534580724001771},
	doi = {10.1016/j.devcel.2024.03.009},
	abstract = {Plant morphogenesis relies exclusively on oriented cell expansion and division. Nonetheless, the mechanism(s) determining division plane orientation remain elusive. Here, we studied tissue healing after laser-assisted wounding in roots of Arabidopsis thaliana and uncovered how mechanical forces stabilize and reorient the microtubule cytoskeleton for the orientation of cell division. We identified that root tissue functions as an interconnected cell matrix, with a radial gradient of tissue extendibility causing predictable tissue deformation after wounding. This deformation causes instant redirection of expansion in the surrounding cells and reorientation of microtubule arrays, ultimately predicting cell division orientation. Microtubules are destabilized under low tension, whereas stretching of cells, either through wounding or external aspiration, immediately induces their polymerization. The higher microtubule abundance in the stretched cell parts leads to the reorientation of microtubule arrays and, ultimately, informs cell division planes. This provides a long-sought mechanism for flexible re-arrangement of cell divisions by mechanical forces for tissue reconstruction and plant architecture.},
	number = {10},
	urldate = {2024-05-24},
	journal = {Developmental Cell},
	author = {Hoermayer, Lukas and Montesinos, Juan Carlos and Trozzi, Nicola and Spona, Leonhard and Yoshida, Saiko and Marhava, Petra and Caballero-Mancebo, Silvia and Benková, Eva and Heisenberg, Carl-Philip and Dagdas, Yasin and Majda, Mateusz and Friml, Jiří},
	month = may,
	year = {2024},
	keywords = {ablation, cell division, cell division plane, cell expansion, mechanical forces, microscopy, microtubules, plant development},
	pages = {1333--1344.e4},
}

Plant morphogenesis relies exclusively on oriented cell expansion and division. Nonetheless, the mechanism(s) determining division plane orientation remain elusive. Here, we studied tissue healing after laser-assisted wounding in roots of Arabidopsis thaliana and uncovered how mechanical forces stabilize and reorient the microtubule cytoskeleton for the orientation of cell division. We identified that root tissue functions as an interconnected cell matrix, with a radial gradient of tissue extendibility causing predictable tissue deformation after wounding. This deformation causes instant redirection of expansion in the surrounding cells and reorientation of microtubule arrays, ultimately predicting cell division orientation. Microtubules are destabilized under low tension, whereas stretching of cells, either through wounding or external aspiration, immediately induces their polymerization. The higher microtubule abundance in the stretched cell parts leads to the reorientation of microtubule arrays and, ultimately, informs cell division planes. This provides a long-sought mechanism for flexible re-arrangement of cell divisions by mechanical forces for tissue reconstruction and plant architecture.

@article{sharma_regulation_2023,
	title = {Regulation of {PIN} polarity in response to abiotic stress},
	volume = {76},
	issn = {1369-5266},
	url = {https://www.sciencedirect.com/science/article/pii/S1369526623001103},
	doi = {10.1016/j.pbi.2023.102445},
	abstract = {Plants have evolved robust adaptive mechanisms to withstand the ever-changing environment. Tightly regulated distribution of the hormone auxin throughout the plant body controls an impressive variety of developmental processes that tailor plant growth and morphology to environmental conditions. The proper flow and directionality of auxin between cells is mainly governed by asymmetrically localized efflux carriers – PINs – ensuring proper coordination of developmental processes in plants. Discerning the molecular players and cellular dynamics involved in the establishment and maintenance of PINs in specific membrane domains, as well as their ability to readjust in response to abiotic stressors is essential for understanding how plants balance adaptability and stability. While much is known about how PINs get polarized, there is still limited knowledge about how abiotic stresses alter PIN polarity by acting on these systems. In this review, we focus on the current understanding of mechanisms involved in (re)establishing and maintaining PIN polarity under abiotic stresses.},
	urldate = {2023-12-22},
	journal = {Current Opinion in Plant Biology},
	author = {Sharma, Manvi and Marhava, Petra},
	month = dec,
	year = {2023},
	pages = {102445},
}

Plants have evolved robust adaptive mechanisms to withstand the ever-changing environment. Tightly regulated distribution of the hormone auxin throughout the plant body controls an impressive variety of developmental processes that tailor plant growth and morphology to environmental conditions. The proper flow and directionality of auxin between cells is mainly governed by asymmetrically localized efflux carriers – PINs – ensuring proper coordination of developmental processes in plants. Discerning the molecular players and cellular dynamics involved in the establishment and maintenance of PINs in specific membrane domains, as well as their ability to readjust in response to abiotic stressors is essential for understanding how plants balance adaptability and stability. While much is known about how PINs get polarized, there is still limited knowledge about how abiotic stresses alter PIN polarity by acting on these systems. In this review, we focus on the current understanding of mechanisms involved in (re)establishing and maintaining PIN polarity under abiotic stresses.

@article{marhava_recent_2022,
	title = {Recent developments in the understanding of {PIN} polarity},
	volume = {233},
	issn = {1469-8137},
	url = {https://onlinelibrary.wiley.com/doi/abs/10.1111/nph.17867},
	doi = {10/gnr3sd},
	abstract = {Polar localization of PIN-FORMED proteins (PINs) at the plasma membrane is essential for plant development as they direct the transport of phytohormone auxin between cells. PIN polar localization to certain sides of a given cell is dynamic, strictly regulated and provides directionality to auxin flow. Signals that act upstream to control subcellular PIN localization modulate auxin distribution, thereby regulating diverse aspects of plant development. Here I summarize the current understanding of mechanisms by which PIN polarity is established, maintained and rearranged to provide a glimpse into the complexity of PIN polarity.},
	language = {en},
	number = {2},
	urldate = {2021-12-14},
	journal = {New Phytologist},
	author = {Marhava, Petra},
	month = jan,
	year = {2022},
	keywords = {PIN clustering, PIN polarity establishment, PIN polarity maintenance, auxin transport, self-reinforcing polarity},
	pages = {624--630},
}

Polar localization of PIN-FORMED proteins (PINs) at the plasma membrane is essential for plant development as they direct the transport of phytohormone auxin between cells. PIN polar localization to certain sides of a given cell is dynamic, strictly regulated and provides directionality to auxin flow. Signals that act upstream to control subcellular PIN localization modulate auxin distribution, thereby regulating diverse aspects of plant development. Here I summarize the current understanding of mechanisms by which PIN polarity is established, maintained and rearranged to provide a glimpse into the complexity of PIN polarity.

@article{koh_mapping_2021,
	title = {Mapping and engineering of auxin-induced plasma membrane dissociation in {BRX} family proteins},
	volume = {33},
	issn = {1040-4651},
	url = {https://doi.org/10.1093/plcell/koab076},
	doi = {10.1093/plcell/koab076},
	abstract = {Angiosperms have evolved the phloem for the long-distance transport of metabolites. The complex process of phloem development involves genes that only occur in vascular plant lineages. For example, in Arabidopsis thaliana, the BREVIS RADIX (BRX) gene is required for continuous root protophloem differentiation, together with PROTEIN KINASE ASSOCIATED WITH BRX (PAX). BRX and its BRX-LIKE (BRXL) homologs are composed of four highly conserved domains including the signature tandem BRX domains that are separated by variable spacers. Nevertheless, BRX family proteins have functionally diverged. For instance, BRXL2 can only partially replace BRX in the root protophloem. This divergence is reflected in physiologically relevant differences in protein behavior, such as auxin-induced plasma membrane dissociation of BRX, which is not observed for BRXL2. Here we dissected the differential functions of BRX family proteins using a set of amino acid substitutions and domain swaps. Our data suggest that the plasma membrane-associated tandem BRX domains are both necessary and sufficient to convey the biological outputs of BRX function and therefore constitute an important regulatory entity. Moreover, PAX target phosphosites in the linker between the two BRX domains mediate the auxin-induced plasma membrane dissociation. Engineering these sites into BRXL2 renders this modified protein auxin-responsive and thereby increases its biological activity in the root protophloem context.},
	number = {6},
	urldate = {2022-05-02},
	journal = {The Plant Cell},
	author = {Koh, Samuel W H and Marhava, Petra and Rana, Surbhi and Graf, Alina and Moret, Bernard and Bassukas, Alkistis E L and Zourelidou, Melina and Kolb, Martina and Hammes, Ulrich Z and Schwechheimer, Claus and Hardtke, Christian S},
	month = jun,
	year = {2021},
	pages = {1945--1960},
}

Angiosperms have evolved the phloem for the long-distance transport of metabolites. The complex process of phloem development involves genes that only occur in vascular plant lineages. For example, in Arabidopsis thaliana, the BREVIS RADIX (BRX) gene is required for continuous root protophloem differentiation, together with PROTEIN KINASE ASSOCIATED WITH BRX (PAX). BRX and its BRX-LIKE (BRXL) homologs are composed of four highly conserved domains including the signature tandem BRX domains that are separated by variable spacers. Nevertheless, BRX family proteins have functionally diverged. For instance, BRXL2 can only partially replace BRX in the root protophloem. This divergence is reflected in physiologically relevant differences in protein behavior, such as auxin-induced plasma membrane dissociation of BRX, which is not observed for BRXL2. Here we dissected the differential functions of BRX family proteins using a set of amino acid substitutions and domain swaps. Our data suggest that the plasma membrane-associated tandem BRX domains are both necessary and sufficient to convey the biological outputs of BRX function and therefore constitute an important regulatory entity. Moreover, PAX target phosphosites in the linker between the two BRX domains mediate the auxin-induced plasma membrane dissociation. Engineering these sites into BRXL2 renders this modified protein auxin-responsive and thereby increases its biological activity in the root protophloem context.

@article{zhang_arabidopsis_2020,
	title = {Arabidopsis {Flippases} {Cooperate} with {ARF} {GTPase} {Exchange} {Factors} to {Regulate} the {Trafficking} and {Polarity} of {PIN} {Auxin} {Transporters}[{OPEN}]},
	volume = {32},
	issn = {1040-4651},
	url = {https://doi.org/10.1105/tpc.19.00869},
	doi = {10.1105/tpc.19.00869},
	abstract = {Cell polarity is a fundamental feature of all multicellular organisms. PIN auxin transporters are important cell polarity markers that play crucial roles in a plethora of developmental processes in plants. Here, to identify components involved in cell polarity establishment and maintenance in plants, we performed a forward genetic screening of PIN2:PIN1-HA;pin2 Arabidopsis (Arabidopsis thaliana) plants, which ectopically express predominantly basally localized PIN1 in root epidermal cells, leading to agravitropic root growth. We identified the regulator of PIN polarity 12 (repp12) mutation, which restored gravitropic root growth and caused a switch in PIN1-HA polarity from the basal to apical side of root epidermal cells. Next Generation Sequencing and complementation experiments established the causative mutation of repp12 as a single amino acid exchange in Aminophospholipid ATPase3 (ALA3), a phospholipid flippase predicted to function in vesicle formation. repp12 and ala3 T-DNA mutants show defects in many auxin-regulated processes, asymmetric auxin distribution, and PIN trafficking. Analysis of quintuple and sextuple mutants confirmed the crucial roles of ALA proteins in regulating plant development as well as PIN trafficking and polarity. Genetic and physical interaction studies revealed that ALA3 functions together with the ADP ribosylation factor GTPase exchange factors GNOM and BIG3 in regulating PIN polarity, trafficking, and auxin-mediated development.},
	number = {5},
	urldate = {2022-05-02},
	journal = {The Plant Cell},
	author = {Zhang, Xixi and Adamowski, Maciek and Marhava, Petra and Tan, Shutang and Zhang, Yuzhou and Rodriguez, Lesia and Zwiewka, Marta and Pukyšová, Vendula and Sánchez, Adrià Sans and Raxwal, Vivek Kumar and Hardtke, Christian S. and Nodzyński, Tomasz and Friml, Jiří},
	month = may,
	year = {2020},
	pages = {1644--1664},
}

Cell polarity is a fundamental feature of all multicellular organisms. PIN auxin transporters are important cell polarity markers that play crucial roles in a plethora of developmental processes in plants. Here, to identify components involved in cell polarity establishment and maintenance in plants, we performed a forward genetic screening of PIN2:PIN1-HA;pin2 Arabidopsis (Arabidopsis thaliana) plants, which ectopically express predominantly basally localized PIN1 in root epidermal cells, leading to agravitropic root growth. We identified the regulator of PIN polarity 12 (repp12) mutation, which restored gravitropic root growth and caused a switch in PIN1-HA polarity from the basal to apical side of root epidermal cells. Next Generation Sequencing and complementation experiments established the causative mutation of repp12 as a single amino acid exchange in Aminophospholipid ATPase3 (ALA3), a phospholipid flippase predicted to function in vesicle formation. repp12 and ala3 T-DNA mutants show defects in many auxin-regulated processes, asymmetric auxin distribution, and PIN trafficking. Analysis of quintuple and sextuple mutants confirmed the crucial roles of ALA proteins in regulating plant development as well as PIN trafficking and polarity. Genetic and physical interaction studies revealed that ALA3 functions together with the ADP ribosylation factor GTPase exchange factors GNOM and BIG3 in regulating PIN polarity, trafficking, and auxin-mediated development.

@article{graeff_local_2020,
	title = {Local and {Systemic} {Effects} of {Brassinosteroid} {Perception} in {Developing} {Phloem}},
	volume = {30},
	issn = {0960-9822},
	url = {https://www.sciencedirect.com/science/article/pii/S0960982220302025},
	doi = {10.1016/j.cub.2020.02.029},
	abstract = {The plant vasculature is an essential adaptation to terrestrial growth. Its phloem component permits efficient transfer of photosynthates between source and sink organs but also transports signals that systemically coordinate physiology and development. Here, we provide evidence that developing phloem orchestrates cellular behavior of adjacent tissues in the growth apices of plants, the meristems. Arabidopsis thaliana plants that lack the three receptor kinases BRASSINOSTEROID INSENSITIVE 1 (BRI1), BRI1-LIKE 1 (BRL1), and BRL3 (“bri3” mutants) can no longer sense brassinosteroid phytohormones and display severe dwarfism as well as patterning and differentiation defects, including disturbed phloem development. We found that, despite the ubiquitous expression of brassinosteroid receptors in growing plant tissues, exclusive expression of the BRI1 receptor in developing phloem is sufficient to systemically correct cellular growth and patterning defects that underlie the bri3 phenotype. Although this effect is brassinosteroid-dependent, it cannot be reproduced with dominant versions of known downstream effectors of BRI1 signaling and therefore possibly involves a non-canonical signaling output. Interestingly, the rescue of bri3 by phloem-specific BRI1 expression is associated with antagonism toward phloem-specific CLAVATA3/EMBRYO SURROUNDING REGION-RELATED 45 (CLE45) peptide signaling in roots. Hyperactive CLE45 signaling causes phloem sieve element differentiation defects, and consistently, knockout of CLE45 perception in bri3 background restores proper phloem development. However, bri3 dwarfism is retained in such lines. Our results thus reveal local and systemic effects of brassinosteroid perception in the phloem: whereas it locally antagonizes CLE45 signaling to permit phloem differentiation, it systemically instructs plant organ formation via a phloem-derived, non-cell-autonomous signal.},
	language = {en},
	number = {9},
	urldate = {2022-05-02},
	journal = {Current Biology},
	author = {Graeff, Moritz and Rana, Surbhi and Marhava, Petra and Moret, Bernard and Hardtke, Christian S.},
	month = may,
	year = {2020},
	keywords = {BAM3, BRI1, CLE45, brassinosteroids, organizer, phloem},
	pages = {1626--1638.e3},
}

The plant vasculature is an essential adaptation to terrestrial growth. Its phloem component permits efficient transfer of photosynthates between source and sink organs but also transports signals that systemically coordinate physiology and development. Here, we provide evidence that developing phloem orchestrates cellular behavior of adjacent tissues in the growth apices of plants, the meristems. Arabidopsis thaliana plants that lack the three receptor kinases BRASSINOSTEROID INSENSITIVE 1 (BRI1), BRI1-LIKE 1 (BRL1), and BRL3 (“bri3” mutants) can no longer sense brassinosteroid phytohormones and display severe dwarfism as well as patterning and differentiation defects, including disturbed phloem development. We found that, despite the ubiquitous expression of brassinosteroid receptors in growing plant tissues, exclusive expression of the BRI1 receptor in developing phloem is sufficient to systemically correct cellular growth and patterning defects that underlie the bri3 phenotype. Although this effect is brassinosteroid-dependent, it cannot be reproduced with dominant versions of known downstream effectors of BRI1 signaling and therefore possibly involves a non-canonical signaling output. Interestingly, the rescue of bri3 by phloem-specific BRI1 expression is associated with antagonism toward phloem-specific CLAVATA3/EMBRYO SURROUNDING REGION-RELATED 45 (CLE45) peptide signaling in roots. Hyperactive CLE45 signaling causes phloem sieve element differentiation defects, and consistently, knockout of CLE45 perception in bri3 background restores proper phloem development. However, bri3 dwarfism is retained in such lines. Our results thus reveal local and systemic effects of brassinosteroid perception in the phloem: whereas it locally antagonizes CLE45 signaling to permit phloem differentiation, it systemically instructs plant organ formation via a phloem-derived, non-cell-autonomous signal.

@article{moret_local_2020,
	title = {Local auxin competition explains fragmented differentiation patterns},
	volume = {11},
	copyright = {2020 The Author(s)},
	issn = {2041-1723},
	url = {https://www.nature.com/articles/s41467-020-16803-7},
	doi = {10.1038/s41467-020-16803-7},
	abstract = {Trajectories of cellular ontogeny are tightly controlled and often involve feedback-regulated molecular antagonism. For example, sieve element differentiation along developing protophloem cell files of Arabidopsis roots requires two antagonistic regulators of auxin efflux. Paradoxically, loss-of-function in either regulator triggers similar, seemingly stochastic differentiation failures of individual sieve element precursors. Here we show that these patterning defects are distinct and non-random. They can be explained by auxin-dependent bistability that emerges from competition for auxin between neighboring cells. This bistability depends on the presence of an auxin influx facilitator, and can be triggered by either flux enhancement or repression. Our results uncover a hitherto overlooked aspect of auxin uptake, and highlight the contributions of local auxin influx, efflux and biosynthesis to protophloem formation. Moreover, the combined experimental-modeling approach suggests that without auxin efflux homeostasis, auxin influx interferes with coordinated differentiation.},
	language = {en},
	number = {1},
	urldate = {2022-05-02},
	journal = {Nature Communications},
	author = {Moret, Bernard and Marhava, Petra and Aliaga Fandino, Ana Cecilia and Hardtke, Christian S. and ten Tusscher, Kirsten H. W.},
	month = jun,
	year = {2020},
	note = {Number: 1
Publisher: Nature Publishing Group},
	keywords = {Auxin, Patterning},
	pages = {2965},
}

Trajectories of cellular ontogeny are tightly controlled and often involve feedback-regulated molecular antagonism. For example, sieve element differentiation along developing protophloem cell files of Arabidopsis roots requires two antagonistic regulators of auxin efflux. Paradoxically, loss-of-function in either regulator triggers similar, seemingly stochastic differentiation failures of individual sieve element precursors. Here we show that these patterning defects are distinct and non-random. They can be explained by auxin-dependent bistability that emerges from competition for auxin between neighboring cells. This bistability depends on the presence of an auxin influx facilitator, and can be triggered by either flux enhancement or repression. Our results uncover a hitherto overlooked aspect of auxin uptake, and highlight the contributions of local auxin influx, efflux and biosynthesis to protophloem formation. Moreover, the combined experimental-modeling approach suggests that without auxin efflux homeostasis, auxin influx interferes with coordinated differentiation.

@article{marhava_plasma_2020,
	title = {Plasma {Membrane} {Domain} {Patterning} and {Self}-{Reinforcing} {Polarity} in {Arabidopsis}},
	volume = {52},
	issn = {1534-5807},
	url = {https://www.sciencedirect.com/science/article/pii/S1534580719309840},
	doi = {10.1016/j.devcel.2019.11.015},
	abstract = {Cell polarity is a key feature in the development of multicellular organisms. For instance, asymmetrically localized plasma-membrane-integral PIN-FORMED (PIN) proteins direct transcellular fluxes of the phytohormone auxin that govern plant development. Fine-tuned auxin flux is important for root protophloem sieve element differentiation and requires the interacting plasma-membrane-associated BREVIS RADIX (BRX) and PROTEIN KINASE ASSOCIATED WITH BRX (PAX) proteins. We observed “donut-like” polar PIN localization in developing sieve elements that depends on complementary, “muffin-like” polar localization of BRX and PAX. Plasma membrane association and polarity of PAX, and indirectly BRX, largely depends on phosphatidylinositol-4,5-bisphosphate. Consistently, mutants in phosphatidylinositol-4-phosphate 5-kinases (PIP5Ks) display protophloem differentiation defects similar to brx mutants. The same PIP5Ks are in complex with BRX and display “muffin-like” polar localization. Our data suggest that the BRX-PAX module recruits PIP5Ks to reinforce PAX polarity and thereby the polarity of all three proteins, which is required to maintain a local PIN minimum.},
	language = {en},
	number = {2},
	urldate = {2022-05-02},
	journal = {Developmental Cell},
	author = {Marhava, Petra and Aliaga Fandino, Ana Cecilia and Koh, Samuel W. H. and Jelínková, Adriana and Kolb, Martina and Janacek, Dorina P. and Breda, Alice S. and Cattaneo, Pietro and Hammes, Ulrich Z. and Petrášek, Jan and Hardtke, Christian S.},
	month = jan,
	year = {2020},
	keywords = {DRP1A, PIP5K1, PIP5K2, endocytosis, phloem, polar auxin transport, polarity, protophloem, root},
	pages = {223--235.e5},
}

Cell polarity is a key feature in the development of multicellular organisms. For instance, asymmetrically localized plasma-membrane-integral PIN-FORMED (PIN) proteins direct transcellular fluxes of the phytohormone auxin that govern plant development. Fine-tuned auxin flux is important for root protophloem sieve element differentiation and requires the interacting plasma-membrane-associated BREVIS RADIX (BRX) and PROTEIN KINASE ASSOCIATED WITH BRX (PAX) proteins. We observed “donut-like” polar PIN localization in developing sieve elements that depends on complementary, “muffin-like” polar localization of BRX and PAX. Plasma membrane association and polarity of PAX, and indirectly BRX, largely depends on phosphatidylinositol-4,5-bisphosphate. Consistently, mutants in phosphatidylinositol-4-phosphate 5-kinases (PIP5Ks) display protophloem differentiation defects similar to brx mutants. The same PIP5Ks are in complex with BRX and display “muffin-like” polar localization. Our data suggest that the BRX-PAX module recruits PIP5Ks to reinforce PAX polarity and thereby the polarity of all three proteins, which is required to maintain a local PIN minimum.

@article{hoermayer_wounding-induced_2020,
	title = {Wounding-induced changes in cellular pressure and localized auxin signalling spatially coordinate restorative divisions in roots},
	volume = {117},
	url = {https://www.pnas.org/doi/full/10.1073/pnas.2003346117},
	doi = {10.1073/pnas.2003346117},
	number = {26},
	urldate = {2022-05-16},
	journal = {Proceedings of the National Academy of Sciences},
	author = {Hoermayer, Lukas and Montesinos, Juan Carlos and Marhava, Petra and Benková, Eva and Yoshida, Saiko and Friml, Jiří},
	month = jun,
	year = {2020},
	note = {Publisher: Proceedings of the National Academy of Sciences},
	pages = {15322--15331},
}

@article{cattaneo_conditional_2019,
	title = {Conditional effects of the epigenetic regulator {JUMONJI} 14 in {Arabidopsis} root growth},
	volume = {146},
	issn = {0950-1991},
	url = {https://doi.org/10.1242/dev.183905},
	doi = {10.1242/dev.183905},
	abstract = {Methylation of lysine 4 in histone 3 (H3K4) is a post-translational modification that promotes gene expression. H3K4 methylation can be reversed by specific demethylases with an enzymatic Jumonji C domain. In Arabidopsis thaliana, H3K4-specific JUMONJI (JMJ) proteins distinguish themselves by the association with an F/Y-rich (FYR) domain. Here, we report that jmj14 mutations partially suppress reduced root meristem size and growth vigor of brevis radix (brx) mutants. Similar to its close homologs, JMJ15, JMJ16 and JMJ18, the JMJ14 promoter confers expression in mature root vasculature. Yet, unlike jmj14, neither jmj16 nor jmj18 mutation markedly suppresses brx phenotypes. Domain-swapping experiments suggest that the specificity of JMJ14 function resides in the FYR domain. Despite JMJ14 promoter activity in the mature vasculature, jmj14 mutation affects root meristem size. However, JMJ14 protein is observed throughout the meristem, suggesting that the JMJ14 transcript region contributes substantially to the spatial aspect of JMJ14 expression. In summary, our data reveal a role for JMJ14 in root growth in sensitized genetic backgrounds that depends on its FYR domain and regulatory input from the JMJ14 cistron.},
	number = {23},
	urldate = {2022-05-02},
	journal = {Development},
	author = {Cattaneo, Pietro and Graeff, Moritz and Marhava, Petra and Hardtke, Christian S.},
	month = dec,
	year = {2019},
	pages = {dev183905},
}

Methylation of lysine 4 in histone 3 (H3K4) is a post-translational modification that promotes gene expression. H3K4 methylation can be reversed by specific demethylases with an enzymatic Jumonji C domain. In Arabidopsis thaliana, H3K4-specific JUMONJI (JMJ) proteins distinguish themselves by the association with an F/Y-rich (FYR) domain. Here, we report that jmj14 mutations partially suppress reduced root meristem size and growth vigor of brevis radix (brx) mutants. Similar to its close homologs, JMJ15, JMJ16 and JMJ18, the JMJ14 promoter confers expression in mature root vasculature. Yet, unlike jmj14, neither jmj16 nor jmj18 mutation markedly suppresses brx phenotypes. Domain-swapping experiments suggest that the specificity of JMJ14 function resides in the FYR domain. Despite JMJ14 promoter activity in the mature vasculature, jmj14 mutation affects root meristem size. However, JMJ14 protein is observed throughout the meristem, suggesting that the JMJ14 transcript region contributes substantially to the spatial aspect of JMJ14 expression. In summary, our data reveal a role for JMJ14 in root growth in sensitized genetic backgrounds that depends on its FYR domain and regulatory input from the JMJ14 cistron.

@article{marhava_re-activation_2019,
	title = {Re-activation of {Stem} {Cell} {Pathways} for {Pattern} {Restoration} in {Plant} {Wound} {Healing}},
	volume = {177},
	issn = {00928674},
	url = {https://linkinghub.elsevier.com/retrieve/pii/S0092867419304015},
	doi = {10/gfz9tc},
	language = {en},
	number = {4},
	urldate = {2021-06-07},
	journal = {Cell},
	author = {Marhava, Petra and Hoermayer, Lukas and Yoshida, Saiko and Marhavý, Peter and Benková, Eva and Friml, Jiří},
	month = may,
	year = {2019},
	pages = {957--969.e13},
}

@article{marhava_molecular_2018,
	title = {A molecular rheostat adjusts auxin flux to promote root protophloem differentiation},
	volume = {558},
	copyright = {2018 Macmillan Publishers Ltd., part of Springer Nature},
	issn = {1476-4687},
	url = {https://www.nature.com/articles/s41586-018-0186-z},
	doi = {10.1038/s41586-018-0186-z},
	abstract = {Auxin influences plant development through several distinct concentration-dependent effects1. In the Arabidopsis root tip, polar auxin transport by PIN-FORMED (PIN) proteins creates a local auxin accumulation that is required for the maintenance of the stem-cell niche2–4. Proximally, stem-cell daughter cells divide repeatedly before they eventually differentiate. This developmental gradient is accompanied by a gradual decrease in auxin levels as cells divide, and subsequently by a gradual increase as the cells differentiate5,6. However, the timing of differentiation is not uniform across cell files. For instance, developing protophloem sieve elements (PPSEs) differentiate as neighbouring cells still divide. Here we show that PPSE differentiation involves local steepening of the post-meristematic auxin gradient. BREVIS RADIX (BRX) and PROTEIN KINASE ASSOCIATED WITH BRX (PAX) are interacting plasma-membrane-associated, polarly localized proteins that co-localize with PIN proteins at the rootward end of developing PPSEs. Both brx and pax mutants display impaired PPSE differentiation. Similar to other AGC-family kinases, PAX activates PIN-mediated auxin efflux, whereas BRX strongly dampens this stimulation. Efficient BRX plasma-membrane localization depends on PAX, but auxin negatively regulates BRX plasma-membrane association and promotes PAX activity. Thus, our data support a model in which BRX and PAX are elements of a molecular rheostat that modulates auxin flux through developing PPSEs, thereby timing PPSE differentiation.},
	language = {en},
	number = {7709},
	urldate = {2022-05-02},
	journal = {Nature},
	author = {Marhava, P. and Bassukas, A. E. L. and Zourelidou, M. and Kolb, M. and Moret, B. and Fastner, A. and Schulze, W. X. and Cattaneo, P. and Hammes, U. Z. and Schwechheimer, C. and Hardtke, C. S.},
	month = jun,
	year = {2018},
	note = {Number: 7709
Publisher: Nature Publishing Group},
	keywords = {Auxin, Cell fate, Root apical meristem},
	pages = {297--300},
}

Auxin influences plant development through several distinct concentration-dependent effects1. In the Arabidopsis root tip, polar auxin transport by PIN-FORMED (PIN) proteins creates a local auxin accumulation that is required for the maintenance of the stem-cell niche2–4. Proximally, stem-cell daughter cells divide repeatedly before they eventually differentiate. This developmental gradient is accompanied by a gradual decrease in auxin levels as cells divide, and subsequently by a gradual increase as the cells differentiate5,6. However, the timing of differentiation is not uniform across cell files. For instance, developing protophloem sieve elements (PPSEs) differentiate as neighbouring cells still divide. Here we show that PPSE differentiation involves local steepening of the post-meristematic auxin gradient. BREVIS RADIX (BRX) and PROTEIN KINASE ASSOCIATED WITH BRX (PAX) are interacting plasma-membrane-associated, polarly localized proteins that co-localize with PIN proteins at the rootward end of developing PPSEs. Both brx and pax mutants display impaired PPSE differentiation. Similar to other AGC-family kinases, PAX activates PIN-mediated auxin efflux, whereas BRX strongly dampens this stimulation. Efficient BRX plasma-membrane localization depends on PAX, but auxin negatively regulates BRX plasma-membrane association and promotes PAX activity. Thus, our data support a model in which BRX and PAX are elements of a molecular rheostat that modulates auxin flux through developing PPSEs, thereby timing PPSE differentiation.

@article{marhavy_targeted_2016,
	title = {Targeted cell elimination reveals an auxin-guided biphasic mode of lateral root initiation},
	volume = {30},
	issn = {0890-9369, 1549-5477},
	url = {http://genesdev.cshlp.org/lookup/doi/10.1101/gad.276964.115},
	doi = {10.1101/gad.276964.115},
	language = {en},
	number = {4},
	urldate = {2021-06-07},
	journal = {Genes \& Development},
	author = {Marhavý, Peter and Montesinos, Juan Carlos and Abuzeineh, Anas and Van Damme, Daniel and Vermeer, Joop E.M. and Duclercq, Jerôme and Rakusová, Hana and Nováková, Petra and Friml, Jiři and Geldner, Niko and Benková, Eva},
	month = feb,
	year = {2016},
	keywords = {auxin, lateral root organogenesis, mechanical forces, meristem proliferation activity},
	pages = {471--483},
}

@article{marhava_real-time_2015,
	title = {Real-time {Analysis} of {Lateral} {Root} {Organogenesis} in {Arabidopsis}},
	volume = {5},
	issn = {2331-8325},
	url = {http://www.bio-protocol.org/e1446},
	doi = {10/ggsz3x},
	language = {en},
	number = {8},
	urldate = {2021-06-07},
	journal = {BIO-PROTOCOL},
	author = {Marhava, Peter and Benkova, Eva},
	year = {2015},
}

@article{novakova_sac_2014,
	title = {{SAC} phosphoinositide phosphatases at the tonoplast mediate vacuolar function in {Arabidopsis}},
	volume = {111},
	url = {https://www.pnas.org/doi/10.1073/pnas.1324264111},
	doi = {10.1073/pnas.1324264111},
	abstract = {Phosphatidylinositol (PtdIns) is a structural phospholipid that can be phosphorylated into various lipid signaling molecules, designated polyphosphoinositides (PPIs). The reversible phosphorylation of PPIs on the 3, 4, or 5 position of inositol is performed by a set of organelle-specific kinases and phosphatases, and the characteristic head groups make these molecules ideal for regulating biological processes in time and space. In yeast and mammals, PtdIns3P and PtdIns(3,5)P2 play crucial roles in trafficking toward the lytic compartments, whereas the role in plants is not yet fully understood. Here we identified the role of a land plant-specific subgroup of PPI phosphatases, the suppressor of actin 2 (SAC2) to SAC5, during vacuolar trafficking and morphogenesis in Arabidopsis thaliana. SAC2–SAC5 localize to the tonoplast along with PtdIns3P, the presumable product of their activity. In SAC gain- and loss-of-function mutants, the levels of PtdIns monophosphates and bisphosphates were changed, with opposite effects on the morphology of storage and lytic vacuoles, and the trafficking toward the vacuoles was defective. Moreover, multiple sac knockout mutants had an increased number of smaller storage and lytic vacuoles, whereas extralarge vacuoles were observed in the overexpression lines, correlating with various growth and developmental defects. The fragmented vacuolar phenotype of sac mutants could be mimicked by treating wild-type seedlings with PtdIns(3,5)P2, corroborating that this PPI is important for vacuole morphology. Taken together, these results provide evidence that PPIs, together with their metabolic enzymes SAC2–SAC5, are crucial for vacuolar trafficking and for vacuolar morphology and function in plants.},
	number = {7},
	urldate = {2024-10-02},
	journal = {Proceedings of the National Academy of Sciences},
	author = {Nováková, Petra and Hirsch, Sibylle and Feraru, Elena and Tejos, Ricardo and van Wijk, Ringo and Viaene, Tom and Heilmann, Mareike and Lerche, Jennifer and De Rycke, Riet and Feraru, Mugurel I. and Grones, Peter and Van Montagu, Marc and Heilmann, Ingo and Munnik, Teun and Friml, Jiří},
	month = feb,
	year = {2014},
	note = {Publisher: Proceedings of the National Academy of Sciences},
	pages = {2818--2823},
}

Phosphatidylinositol (PtdIns) is a structural phospholipid that can be phosphorylated into various lipid signaling molecules, designated polyphosphoinositides (PPIs). The reversible phosphorylation of PPIs on the 3, 4, or 5 position of inositol is performed by a set of organelle-specific kinases and phosphatases, and the characteristic head groups make these molecules ideal for regulating biological processes in time and space. In yeast and mammals, PtdIns3P and PtdIns(3,5)P2 play crucial roles in trafficking toward the lytic compartments, whereas the role in plants is not yet fully understood. Here we identified the role of a land plant-specific subgroup of PPI phosphatases, the suppressor of actin 2 (SAC2) to SAC5, during vacuolar trafficking and morphogenesis in Arabidopsis thaliana. SAC2–SAC5 localize to the tonoplast along with PtdIns3P, the presumable product of their activity. In SAC gain- and loss-of-function mutants, the levels of PtdIns monophosphates and bisphosphates were changed, with opposite effects on the morphology of storage and lytic vacuoles, and the trafficking toward the vacuoles was defective. Moreover, multiple sac knockout mutants had an increased number of smaller storage and lytic vacuoles, whereas extralarge vacuoles were observed in the overexpression lines, correlating with various growth and developmental defects. The fragmented vacuolar phenotype of sac mutants could be mimicked by treating wild-type seedlings with PtdIns(3,5)P2, corroborating that this PPI is important for vacuole morphology. Taken together, these results provide evidence that PPIs, together with their metabolic enzymes SAC2–SAC5, are crucial for vacuolar trafficking and for vacuolar morphology and function in plants.