Arabidopsis Flippases Cooperate with ARF GTPase Exchange Factors to Regulate the Trafficking and Polarity of PIN Auxin Transporters[OPEN].
Zhang, X., Adamowski, M., Marhava, P., Tan, S., Zhang, Y., Rodriguez, L., Zwiewka, M., Pukyšová, V., Sánchez, A. S., Raxwal, V. K., Hardtke, C. S., Nodzyński, T., & Friml, J.
The Plant Cell, 32(5): 1644–1664. May 2020.
Paper
doi
link
bibtex
abstract
@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.
Local and Systemic Effects of Brassinosteroid Perception in Developing Phloem.
Graeff, M., Rana, S., Marhava, P., Moret, B., & Hardtke, C. S.
Current Biology, 30(9): 1626–1638.e3. May 2020.
Paper
doi
link
bibtex
abstract
@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.
Local auxin competition explains fragmented differentiation patterns.
Moret, B., Marhava, P., Aliaga Fandino, A. C., Hardtke, C. S., & ten Tusscher, K. H. W.
Nature Communications, 11(1): 2965. June 2020.
Number: 1 Publisher: Nature Publishing Group
Paper
doi
link
bibtex
abstract
@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.
Plasma Membrane Domain Patterning and Self-Reinforcing Polarity in Arabidopsis.
Marhava, P., Aliaga Fandino, A. C., Koh, S. W. H., Jelínková, A., Kolb, M., Janacek, D. P., Breda, A. S., Cattaneo, P., Hammes, U. Z., Petrášek, J., & Hardtke, C. S.
Developmental Cell, 52(2): 223–235.e5. January 2020.
Paper
doi
link
bibtex
abstract
@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.
Wounding-induced changes in cellular pressure and localized auxin signalling spatially coordinate restorative divisions in roots.
Hoermayer, L., Montesinos, J. C., Marhava, P., Benková, E., Yoshida, S., & Friml, J.
Proceedings of the National Academy of Sciences, 117(26): 15322–15331. June 2020.
Publisher: Proceedings of the National Academy of Sciences
Paper
doi
link
bibtex
@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},
}