Cell plate restricted association of DRP1A and PIN proteins is required for cell polarity establishment in arabidopsis

Jozef Mravec; Jan Petrášek; Na Li; Sjef Boeren; Rumyana Karlova; Saeko Kitakura; Markéta Pařezová; Satoshi Naramoto; Tomasz Nodzyński; Pankaj Dhonukshe; Sebastian Y. Bednarek; Eva Zažímalová; Sacco De Vries; Jiří Friml

doi:10.1016/j.cub.2011.05.018

Cell plate restricted association of DRP1A and PIN proteins is required for cell polarity establishment in arabidopsis

Jozef Mravec, Jan Petrášek, Na Li, Sjef Boeren, Rumyana Karlova, Saeko Kitakura, Markéta Pařezová, Satoshi Naramoto, Tomasz Nodzyński, Pankaj Dhonukshe, Sebastian Y. Bednarek, Eva Zažímalová, Sacco De Vries, Jiří Friml

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

53 Citations (Scopus)

Abstract

The polarized transport of the phytohormone auxin [1], which is crucial for the regulation of different stages of plant development [2, 3], depends on the asymmetric plasma membrane distribution of the PIN-FORMED (PIN) auxin efflux carriers [4, 5]. The PIN polar localization results from clathrin-mediated endocytosis (CME) from the plasma membrane and subsequent polar recycling [6]. The Arabidopsis genome encodes two groups of dynamin-related proteins (DRPs) that show homology to mammalian dynamin - a protein required for fission of endocytic vesicles during CME [7, 8]. Here we show by coimmunoprecipitation (coIP), bimolecular fluorescence complementation (BiFC), and Förster resonance energy transfer (FRET) that members of the DRP1 group closely associate with PIN proteins at the cell plate. Localization and phenotypic analysis of novel drp1 mutants revealed a requirement for DRP1 function in correct PIN distribution and in auxin-mediated development. We propose that rapid and specific internalization of PIN proteins mediated by the DRP1 proteins and the associated CME machinery from the cell plate membranes during cytokinesis is an important mechanism for proper polar PIN positioning in interphase cells.

Original language	English
Pages (from-to)	1055-1060
Number of pages	6
Journal	Current Biology
Volume	21
Issue number	12
DOIs	https://doi.org/10.1016/j.cub.2011.05.018
Publication status	Published - 2011 Jun 21

ASJC Scopus subject areas

Biochemistry, Genetics and Molecular Biology(all)
Agricultural and Biological Sciences(all)

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Mravec, J., Petrášek, J., Li, N., Boeren, S., Karlova, R., Kitakura, S., Pařezová, M., Naramoto, S., Nodzyński, T., Dhonukshe, P., Bednarek, S. Y., Zažímalová, E., De Vries, S., & Friml, J. (2011). Cell plate restricted association of DRP1A and PIN proteins is required for cell polarity establishment in arabidopsis. Current Biology, 21(12), 1055-1060. https://doi.org/10.1016/j.cub.2011.05.018

Cell plate restricted association of DRP1A and PIN proteins is required for cell polarity establishment in arabidopsis. / Mravec, Jozef; Petrášek, Jan; Li, Na; Boeren, Sjef; Karlova, Rumyana; Kitakura, Saeko; Pařezová, Markéta; Naramoto, Satoshi; Nodzyński, Tomasz; Dhonukshe, Pankaj; Bednarek, Sebastian Y.; Zažímalová, Eva; De Vries, Sacco; Friml, Jiří.

In: Current Biology, Vol. 21, No. 12, 21.06.2011, p. 1055-1060.

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

Mravec, J, Petrášek, J, Li, N, Boeren, S, Karlova, R, Kitakura, S, Pařezová, M, Naramoto, S, Nodzyński, T, Dhonukshe, P, Bednarek, SY, Zažímalová, E, De Vries, S & Friml, J 2011, 'Cell plate restricted association of DRP1A and PIN proteins is required for cell polarity establishment in arabidopsis', Current Biology, vol. 21, no. 12, pp. 1055-1060. https://doi.org/10.1016/j.cub.2011.05.018

Mravec, Jozef ; Petrášek, Jan ; Li, Na ; Boeren, Sjef ; Karlova, Rumyana ; Kitakura, Saeko ; Pařezová, Markéta ; Naramoto, Satoshi ; Nodzyński, Tomasz ; Dhonukshe, Pankaj ; Bednarek, Sebastian Y. ; Zažímalová, Eva ; De Vries, Sacco ; Friml, Jiří. / Cell plate restricted association of DRP1A and PIN proteins is required for cell polarity establishment in arabidopsis. In: Current Biology. 2011 ; Vol. 21, No. 12. pp. 1055-1060.

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title = "Cell plate restricted association of DRP1A and PIN proteins is required for cell polarity establishment in arabidopsis",

abstract = "The polarized transport of the phytohormone auxin [1], which is crucial for the regulation of different stages of plant development [2, 3], depends on the asymmetric plasma membrane distribution of the PIN-FORMED (PIN) auxin efflux carriers [4, 5]. The PIN polar localization results from clathrin-mediated endocytosis (CME) from the plasma membrane and subsequent polar recycling [6]. The Arabidopsis genome encodes two groups of dynamin-related proteins (DRPs) that show homology to mammalian dynamin - a protein required for fission of endocytic vesicles during CME [7, 8]. Here we show by coimmunoprecipitation (coIP), bimolecular fluorescence complementation (BiFC), and F{\"o}rster resonance energy transfer (FRET) that members of the DRP1 group closely associate with PIN proteins at the cell plate. Localization and phenotypic analysis of novel drp1 mutants revealed a requirement for DRP1 function in correct PIN distribution and in auxin-mediated development. We propose that rapid and specific internalization of PIN proteins mediated by the DRP1 proteins and the associated CME machinery from the cell plate membranes during cytokinesis is an important mechanism for proper polar PIN positioning in interphase cells.",

author = "Jozef Mravec and Jan Petr{\'a}{\v s}ek and Na Li and Sjef Boeren and Rumyana Karlova and Saeko Kitakura and Mark{\'e}ta Pa{\v r}ezov{\'a} and Satoshi Naramoto and Tomasz Nodzy{\'n}ski and Pankaj Dhonukshe and Bednarek, {Sebastian Y.} and Eva Za{\v z}{\'i}malov{\'a} and {De Vries}, Sacco and Ji{\v r}{\'i} Friml",

note = "Funding Information: We thank Caterina Brancato and Vassilena Gaykova for technical assistance, European Arabidopsis Stock Centre (NASC) for providing SALK insertional lines, Martine De Cock for help in preparing the manuscript, and Herman H{\"o}fte for enabling J.M. to finalize the work in his laboratory. This work was supported by the Volkswagenstiftung (J.F. and J.M.), the Odysseus Programme of The Research Foundation—Flanders (FWO) (J.F., J.M., J.Z. and T.N.), the project of The Ministry of Education, Youth and Sports of the Czech Republic LC06034 (J.P., M.P. and E.Z.), the European Fund for Regional Development, the Operational Programme Prague—Competitiveness, project number: CZ.2.16/3.1.00/21159, the Centre for Biosystems Genomics part of the Netherlands Genomics Initiative/Netherlands Organization for Scientific Research (N.L.) and ERA-Plant Genomics (R.K.), and the Agrotechnology and Food Sciences Group of Wageningen University (S.d.V.). J.M. is indebted to the Federation of the Societies of Biochemistry and Molecular Biology (FEBS) for a long-term fellowship. ",

year = "2011",

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doi = "10.1016/j.cub.2011.05.018",

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T1 - Cell plate restricted association of DRP1A and PIN proteins is required for cell polarity establishment in arabidopsis

AU - Mravec, Jozef

AU - Petrášek, Jan

AU - Li, Na

AU - Boeren, Sjef

AU - Karlova, Rumyana

AU - Kitakura, Saeko

AU - Pařezová, Markéta

AU - Naramoto, Satoshi

AU - Nodzyński, Tomasz

AU - Dhonukshe, Pankaj

AU - Bednarek, Sebastian Y.

AU - Zažímalová, Eva

AU - De Vries, Sacco

AU - Friml, Jiří

N1 - Funding Information: We thank Caterina Brancato and Vassilena Gaykova for technical assistance, European Arabidopsis Stock Centre (NASC) for providing SALK insertional lines, Martine De Cock for help in preparing the manuscript, and Herman Höfte for enabling J.M. to finalize the work in his laboratory. This work was supported by the Volkswagenstiftung (J.F. and J.M.), the Odysseus Programme of The Research Foundation—Flanders (FWO) (J.F., J.M., J.Z. and T.N.), the project of The Ministry of Education, Youth and Sports of the Czech Republic LC06034 (J.P., M.P. and E.Z.), the European Fund for Regional Development, the Operational Programme Prague—Competitiveness, project number: CZ.2.16/3.1.00/21159, the Centre for Biosystems Genomics part of the Netherlands Genomics Initiative/Netherlands Organization for Scientific Research (N.L.) and ERA-Plant Genomics (R.K.), and the Agrotechnology and Food Sciences Group of Wageningen University (S.d.V.). J.M. is indebted to the Federation of the Societies of Biochemistry and Molecular Biology (FEBS) for a long-term fellowship.

PY - 2011/6/21

Y1 - 2011/6/21

N2 - The polarized transport of the phytohormone auxin [1], which is crucial for the regulation of different stages of plant development [2, 3], depends on the asymmetric plasma membrane distribution of the PIN-FORMED (PIN) auxin efflux carriers [4, 5]. The PIN polar localization results from clathrin-mediated endocytosis (CME) from the plasma membrane and subsequent polar recycling [6]. The Arabidopsis genome encodes two groups of dynamin-related proteins (DRPs) that show homology to mammalian dynamin - a protein required for fission of endocytic vesicles during CME [7, 8]. Here we show by coimmunoprecipitation (coIP), bimolecular fluorescence complementation (BiFC), and Förster resonance energy transfer (FRET) that members of the DRP1 group closely associate with PIN proteins at the cell plate. Localization and phenotypic analysis of novel drp1 mutants revealed a requirement for DRP1 function in correct PIN distribution and in auxin-mediated development. We propose that rapid and specific internalization of PIN proteins mediated by the DRP1 proteins and the associated CME machinery from the cell plate membranes during cytokinesis is an important mechanism for proper polar PIN positioning in interphase cells.

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