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Subcellular homeostasis of phytohormone auxin is mediated by the ER-localized PIN5 transporter

Nature volume 459, pages 1136–1140 (2009)Cite this article

Abstract

The plant signalling molecule auxin provides positional information in a variety of developmental processes by means of its differential distribution (gradients) within plant tissues1. Thus, cellular auxin levels often determine the developmental output of auxin signalling. Conceptually, transmembrane transport and metabolic processes regulate the steady-state levels of auxin in any given cell2,3. In particular, PIN auxin-efflux-carrier-mediated, directional transport between cells is crucial for generating auxin gradients2,4,5. Here we show that Arabidopsis thaliana PIN5, an atypical member of the PIN gene family, encodes a functional auxin transporter that is required for auxin-mediated development. PIN5 does not have a direct role in cell-to-cell transport but regulates intracellular auxin homeostasis and metabolism. PIN5 localizes, unlike other characterized plasma membrane PIN proteins, to endoplasmic reticulum (ER), presumably mediating auxin flow from the cytosol to the lumen of the ER. The ER localization of other PIN5-like transporters (including the moss PIN) indicates that the diversification of PIN protein functions in mediating auxin homeostasis at the ER, and cell-to-cell auxin transport at the plasma membrane, represent an ancient event during the evolution of land plants.

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Figure 1: PIN5 auxin transporter.
Figure 2: Phenotypes of pin5 knockout and gain-of-function mutants.
Figure 3: PIN5 in regulation of auxin homeostasis.
Figure 4: PIN5 localization at the ER.

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Acknowledgements

We thank D. G. Robinson, J. Clarke and NASC for providing material; B. Scheres and H. Höfte for sharing unpublished data, E. Bellinvia, M. Pařezová, B. Pešek and V. Vincenzetti for technical help and M. De Cock for critical reading and help with preparing the manuscript. This work was supported by the Volkswagenstiftung (J.F., J.M., V.G.), the Odysseus programme of the FWO (J.M., J.Z.), GA ASCR IAA601630703 (J.F.) and KJB600380604 (J.P., K.S.), the Ministry of Education, Youth and Sports of the Czech Republic, project number LC06034 (E.Z., P.S., P.K., K.H., J.P., D.S.) and MSM6198959216 (J.R.), a European Research Council starting independent research grant to E.B. (A.Bi.), the Novartis Foundation (M.G.), the Swiss National Funds (M.G.), the Forschungskredit of the University of Zurich (A.Ba.) and the Austrian Science Fund (C.L).

Author Contributions J.F. and J.M. designed the research. J.M. cloned the constructs, established the mutants and performed the expression and localization analyses, P.S. designed and performed metabolic profiling, and established transgenic tobacco lines, A.Ba. and M.G. performed the transport assays in yeast and protoplasts, K.H. performed the free IAA measurements, P.I.D. and J.R. ran HPLC and MS auxin analyses, J.P. and K.S. analysed localization of PINs in BY-2 tobacco cells, D.S. prepared PIN6-GFP construct, A.Bi. and E.B. performed the analysis of the lateral root phenotypes, J.Z. performed the site-directed mutagenesis, V.G. performed the phenotype analyses, Y.-D.S. performed the electron microscopy, C.L. originally identified the PIN5 gene, isolated the PIN5 cDNA and generated overexpression lines, J.F. performed the in situ hybridization, P.K. constructed the cladogram, and J.M., E.Z. and J.F. wrote the manuscript.

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Authors and Affiliations

  1. Department of Plant Systems Biology, VIB and Department of Plant Biotechnology and Genetics, Ghent University, 9052 Gent, Belgium

    Jozef Mravec, Agnieszka Bielach, Jing Zhang, Eva Benková & Jiří Friml

  2. Center for Plant Molecular Biology (ZMBP), University Tübingen, D-72076 Tübingen, Germany

    Jozef Mravec, Jing Zhang, Vassilena Gaykova & York-Dieter Stierhof

  3. Institute of Experimental Botany, ASCR, 165 02 Praha 6, Czech Republic ,

    Petr Skůpa, Klára Hoyerová, Pavel Křeček, Jan Petrášek, Petre I. Dobrev, Daniela Seifertová & Eva Zažímalová

  4. Zürich-Basel Plant Science Center, University of Zurich, Institute of Plant Biology, Molecular Plant Physiology, CH-8008 Zurich, Switzerland

    Aurélien Bailly & Markus Geisler

  5. Department of Plant Physiology, Faculty of Science, Charles University, 128 44 Praha 2, Czech Republic

    Jan Petrášek & Kateřina Schwarzerová

  6. Laboratory of Growth Regulators of the Institute of Experimental Botany, ASCR and Faculty of Science, Palacký University, 783 71 Olomouc, Czech Republic

    Jakub Rolčík

  7. Department for Applied Genetics and Cell Biology, University of Natural Resources and Applied Life Sciences - BOKU, A-1190 Wien, Austria

    Christian Luschnig

  8. Department of Functional Genomics and Proteomics, Faculty of Science, Masaryk University, 625 00 Brno, Czech Republic

    Jiří Friml

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  1. Jozef Mravec
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Mravec, J., Skůpa, P., Bailly, A. et al. Subcellular homeostasis of phytohormone auxin is mediated by the ER-localized PIN5 transporter. Nature 459, 1136–1140 (2009). https://doi.org/10.1038/nature08066

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