Generation of cell polarity in plants links endocytosis, auxin distribution and cell fate decisions

Pankaj Dhonukshe; Hirokazu Tanaka; Tatsuaki Goh; Kazuo Ebine; Ari Pekka Mähönen; Kalika Prasad; Ikram Blilou; Niko Geldner; Jian Xu; Tomohiro Uemura; Joanne Chory; Takashi Ueda; Akihiko Nakano; Ben Scheres; Jiří Friml

doi:10.1038/nature07409

Generation of cell polarity in plants links endocytosis, auxin distribution and cell fate decisions

Pankaj Dhonukshe^*, Hirokazu Tanaka, Tatsuaki Goh, Kazuo Ebine, Ari Pekka Mähönen, Kalika Prasad, Ikram Blilou, Niko Geldner, Jian Xu, Tomohiro Uemura, Joanne Chory, Takashi Ueda, Akihiko Nakano, Ben Scheres, Jiří Friml

^*Corresponding author for this work

Research output: Contribution to journal › Article › peer-review

202 Scopus citations

Abstract

Dynamically polarized membrane proteins define different cell boundaries and have an important role in intercellular communication - a vital feature of multicellular development. Efflux carriers for the signalling molecule auxin from the PIN family are landmarks of cell polarity in plants and have a crucial involvement in auxin distribution-dependent development including embryo patterning, organogenesis and tropisms. Polar PIN localization determines the direction of intercellular auxin flow, yet the mechanisms generating PIN polarity remain unclear. Here we identify an endocytosis-dependent mechanism of PIN polarity generation and analyse its developmental implications. Real-time PIN tracking showed that after synthesis, PINs are initially delivered to the plasma membrane in a non-polar manner and their polarity is established by subsequent endocytic recycling. Interference with PIN endocytosis either by auxin or by manipulation of the Arabidopsis Rab5 GTPase pathway prevents PIN polarization. Failure of PIN polarization transiently alters asymmetric auxin distribution during embryogenesis and increases the local auxin response in apical embryo regions. This results in ectopic expression of auxin pathway-associated root-forming master regulators in embryonic leaves and promotes homeotic transformation of leaves to roots. Our results indicate a two-step mechanism for the generation of PIN polar localization and the essential role of endocytosis in this process. It also highlights the link between endocytosis-dependent polarity of individual cells and auxin distribution-dependent cell fate establishment for multicellular patterning.

Original language	English (US)
Pages (from-to)	962-966
Number of pages	5
Journal	NATURE
Volume	456
Issue number	7224
DOIs	https://doi.org/10.1038/nature07409
State	Published - Dec 18 2008
Externally published	Yes

Bibliographical note

Funding Information:
Acknowledgements We thank M. Bennett, T. Gaude, L. Jiang, G. Jürgens, C. Luschnig, E. Meywerowitz, W. Michalke, R. Offringa, D. Robinson, K. Schumacher, J. Wiedenmann and D. Weijers for sharing published material and RIKEN, SALK and NASC Arabidopsis stock centres for providing mutant lines and the RNAi construct. We thank W. Muller for assistance with SEM and F. Kindt and R. Leito for photography. We acknowledge the Center for Plant Molecular Biology (ZMBP), University of Tübingen, Germany for the facilities during the initial phase of the project. This work was supported by VolkswagenStiftung (P.D. and J.F.), EMBO Long Term Fellowship and Netherlands Organization for Scientific Research (NWO)-VENI grant (P.D.), EMBO Young Investigator Program and Odysseus program of FWO (J.F.), HFSP fellowship (H.T.), EMBO Long Term Fellowship and HFSP fellowship (A.P.M.), EMBO Long Term Fellowship (K.P.), NWO-VIDI grant (I.B.), HFSP fellowship and Swiss National Science Foundation (N.G.), HHMI, USDA and NIH (J.C.), NWO-Spinoza award (B.S.) and Grants-in-Aid for Scientific Research from the Ministry of Education, Culture, Sports, Science and Technology of Japan (T.U. and A.N.).

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@article{c41218a70aae42c68fe815093129769c,

title = "Generation of cell polarity in plants links endocytosis, auxin distribution and cell fate decisions",

abstract = "Dynamically polarized membrane proteins define different cell boundaries and have an important role in intercellular communication - a vital feature of multicellular development. Efflux carriers for the signalling molecule auxin from the PIN family are landmarks of cell polarity in plants and have a crucial involvement in auxin distribution-dependent development including embryo patterning, organogenesis and tropisms. Polar PIN localization determines the direction of intercellular auxin flow, yet the mechanisms generating PIN polarity remain unclear. Here we identify an endocytosis-dependent mechanism of PIN polarity generation and analyse its developmental implications. Real-time PIN tracking showed that after synthesis, PINs are initially delivered to the plasma membrane in a non-polar manner and their polarity is established by subsequent endocytic recycling. Interference with PIN endocytosis either by auxin or by manipulation of the Arabidopsis Rab5 GTPase pathway prevents PIN polarization. Failure of PIN polarization transiently alters asymmetric auxin distribution during embryogenesis and increases the local auxin response in apical embryo regions. This results in ectopic expression of auxin pathway-associated root-forming master regulators in embryonic leaves and promotes homeotic transformation of leaves to roots. Our results indicate a two-step mechanism for the generation of PIN polar localization and the essential role of endocytosis in this process. It also highlights the link between endocytosis-dependent polarity of individual cells and auxin distribution-dependent cell fate establishment for multicellular patterning.",

author = "Pankaj Dhonukshe and Hirokazu Tanaka and Tatsuaki Goh and Kazuo Ebine and M{\"a}h{\"o}nen, {Ari Pekka} and Kalika Prasad and Ikram Blilou and Niko Geldner and Jian Xu and Tomohiro Uemura and Joanne Chory and Takashi Ueda and Akihiko Nakano and Ben Scheres and Ji{\v r}{\'i} Friml",

note = "Funding Information: Acknowledgements We thank M. Bennett, T. Gaude, L. Jiang, G. J{\"u}rgens, C. Luschnig, E. Meywerowitz, W. Michalke, R. Offringa, D. Robinson, K. Schumacher, J. Wiedenmann and D. Weijers for sharing published material and RIKEN, SALK and NASC Arabidopsis stock centres for providing mutant lines and the RNAi construct. We thank W. Muller for assistance with SEM and F. Kindt and R. Leito for photography. We acknowledge the Center for Plant Molecular Biology (ZMBP), University of T{\"u}bingen, Germany for the facilities during the initial phase of the project. This work was supported by VolkswagenStiftung (P.D. and J.F.), EMBO Long Term Fellowship and Netherlands Organization for Scientific Research (NWO)-VENI grant (P.D.), EMBO Young Investigator Program and Odysseus program of FWO (J.F.), HFSP fellowship (H.T.), EMBO Long Term Fellowship and HFSP fellowship (A.P.M.), EMBO Long Term Fellowship (K.P.), NWO-VIDI grant (I.B.), HFSP fellowship and Swiss National Science Foundation (N.G.), HHMI, USDA and NIH (J.C.), NWO-Spinoza award (B.S.) and Grants-in-Aid for Scientific Research from the Ministry of Education, Culture, Sports, Science and Technology of Japan (T.U. and A.N.).",

year = "2008",

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day = "18",

doi = "10.1038/nature07409",

language = "English (US)",

volume = "456",

pages = "962--966",

journal = "NATURE",

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TY - JOUR

T1 - Generation of cell polarity in plants links endocytosis, auxin distribution and cell fate decisions

AU - Dhonukshe, Pankaj

AU - Tanaka, Hirokazu

AU - Goh, Tatsuaki

AU - Ebine, Kazuo

AU - Mähönen, Ari Pekka

AU - Prasad, Kalika

AU - Blilou, Ikram

AU - Geldner, Niko

AU - Xu, Jian

AU - Uemura, Tomohiro

AU - Chory, Joanne

AU - Ueda, Takashi

AU - Nakano, Akihiko

AU - Scheres, Ben

AU - Friml, Jiří

N1 - Funding Information: Acknowledgements We thank M. Bennett, T. Gaude, L. Jiang, G. Jürgens, C. Luschnig, E. Meywerowitz, W. Michalke, R. Offringa, D. Robinson, K. Schumacher, J. Wiedenmann and D. Weijers for sharing published material and RIKEN, SALK and NASC Arabidopsis stock centres for providing mutant lines and the RNAi construct. We thank W. Muller for assistance with SEM and F. Kindt and R. Leito for photography. We acknowledge the Center for Plant Molecular Biology (ZMBP), University of Tübingen, Germany for the facilities during the initial phase of the project. This work was supported by VolkswagenStiftung (P.D. and J.F.), EMBO Long Term Fellowship and Netherlands Organization for Scientific Research (NWO)-VENI grant (P.D.), EMBO Young Investigator Program and Odysseus program of FWO (J.F.), HFSP fellowship (H.T.), EMBO Long Term Fellowship and HFSP fellowship (A.P.M.), EMBO Long Term Fellowship (K.P.), NWO-VIDI grant (I.B.), HFSP fellowship and Swiss National Science Foundation (N.G.), HHMI, USDA and NIH (J.C.), NWO-Spinoza award (B.S.) and Grants-in-Aid for Scientific Research from the Ministry of Education, Culture, Sports, Science and Technology of Japan (T.U. and A.N.).

PY - 2008/12/18

Y1 - 2008/12/18

N2 - Dynamically polarized membrane proteins define different cell boundaries and have an important role in intercellular communication - a vital feature of multicellular development. Efflux carriers for the signalling molecule auxin from the PIN family are landmarks of cell polarity in plants and have a crucial involvement in auxin distribution-dependent development including embryo patterning, organogenesis and tropisms. Polar PIN localization determines the direction of intercellular auxin flow, yet the mechanisms generating PIN polarity remain unclear. Here we identify an endocytosis-dependent mechanism of PIN polarity generation and analyse its developmental implications. Real-time PIN tracking showed that after synthesis, PINs are initially delivered to the plasma membrane in a non-polar manner and their polarity is established by subsequent endocytic recycling. Interference with PIN endocytosis either by auxin or by manipulation of the Arabidopsis Rab5 GTPase pathway prevents PIN polarization. Failure of PIN polarization transiently alters asymmetric auxin distribution during embryogenesis and increases the local auxin response in apical embryo regions. This results in ectopic expression of auxin pathway-associated root-forming master regulators in embryonic leaves and promotes homeotic transformation of leaves to roots. Our results indicate a two-step mechanism for the generation of PIN polar localization and the essential role of endocytosis in this process. It also highlights the link between endocytosis-dependent polarity of individual cells and auxin distribution-dependent cell fate establishment for multicellular patterning.

AB - Dynamically polarized membrane proteins define different cell boundaries and have an important role in intercellular communication - a vital feature of multicellular development. Efflux carriers for the signalling molecule auxin from the PIN family are landmarks of cell polarity in plants and have a crucial involvement in auxin distribution-dependent development including embryo patterning, organogenesis and tropisms. Polar PIN localization determines the direction of intercellular auxin flow, yet the mechanisms generating PIN polarity remain unclear. Here we identify an endocytosis-dependent mechanism of PIN polarity generation and analyse its developmental implications. Real-time PIN tracking showed that after synthesis, PINs are initially delivered to the plasma membrane in a non-polar manner and their polarity is established by subsequent endocytic recycling. Interference with PIN endocytosis either by auxin or by manipulation of the Arabidopsis Rab5 GTPase pathway prevents PIN polarization. Failure of PIN polarization transiently alters asymmetric auxin distribution during embryogenesis and increases the local auxin response in apical embryo regions. This results in ectopic expression of auxin pathway-associated root-forming master regulators in embryonic leaves and promotes homeotic transformation of leaves to roots. Our results indicate a two-step mechanism for the generation of PIN polar localization and the essential role of endocytosis in this process. It also highlights the link between endocytosis-dependent polarity of individual cells and auxin distribution-dependent cell fate establishment for multicellular patterning.

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U2 - 10.1038/nature07409

DO - 10.1038/nature07409

M3 - Article

C2 - 18953331

AN - SCOPUS:56349106623

SN - 0028-0836

VL - 456

SP - 962

EP - 966

JO - NATURE

JF - NATURE

IS - 7224

ER -

Generation of cell polarity in plants links endocytosis, auxin distribution and cell fate decisions

Abstract

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