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Light-mediated polarization of the PIN3 auxin transporter for the phototropic response in Arabidopsis

Nature Cell Biology volume 13, pages 447–452 (2011)Cite this article

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Abstract

Phototropism is an adaptation response, through which plants grow towards the light1. It involves light perception and asymmetric distribution of the plant hormone auxin2,3,4,5,6,7,8,9,10,11,12. Here we identify a crucial part of the mechanism for phototropism, revealing how light perception initiates auxin redistribution that leads to directional growth. We show that light polarizes the cellular localization of the auxin efflux carrier PIN3 in hypocotyl endodermis cells, resulting in changes in auxin distribution and differential growth. In the dark, high expression and activity of the PINOID (PID) kinase correlates with apolar targeting of PIN3 to all cell sides. Following illumination, light represses PINOID transcription and PIN3 is polarized specifically to the inner cell sides by GNOM ARF GTPase GEF (guanine nucleotide exchange factor)-dependent trafficking. Thus, differential trafficking at the shaded and illuminated hypocotyl side aligns PIN3 polarity with the light direction, and presumably redirects auxin flow towards the shaded side, where auxin promotes growth, causing hypocotyls to bend towards the light. Our results imply that PID phosphorylation-dependent recruitment of PIN proteins into distinct trafficking pathways is a mechanism to polarize auxin fluxes in response to different environmental and endogenous cues.

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Figure 1: PIN3-mediated asymmetric auxin response during hypocotyl phototropism.
Figure 2: Light-mediated PIN3 polarization.
Figure 3: BFA-sensitive, GNOM-dependent PIN3 polarization by light.
Figure 4: PID involvement in PIN3 polarization and the phototropic response.
Figure 5: Model for the hypocotyl phototropic response.

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Acknowledgements

We thank W. Briggs, G. Jürgens and I. Moore for sharing published materials; the Nottingham Arabidopsis Stock Centre (NASC) for seed stocks; D. Van Der Straeten, F. Vandenbussche and Q. Zhu for help with the blue-light treatment; W. Briggs, J. Christie and A. Murphy for helpful discussions; and M. De Cock for help in preparing the manuscript. This work was supported by grants from the Research Foundation-Flanders (Odysseus), from the Research Council for Earth and Life Sciences (C.S.G-A., ALW 813.06.004) with financial aid from the Dutch Organization of Scientific Research (NWO) to R.O., and from the Chinese Science Council (Y.F.). Work in the Fankhauser laboratory is supported by the Swiss National Science Foundation (grant no. 31003A_124747/1).

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  1. Carlos S. Galván-Ampudia

    Present address: Present address: Swammerdam Institute for Life Sciences, University of Amsterdam, Science Park 904, 1098 XH Amsterdam, The Netherlands,

Authors and Affiliations

  1. Department of Plant Systems Biology, VIB, Universiteit Gent, Technologiepark 927, B-9052 Gent, Belgium

    Zhaojun Ding, Łukasz Łangowski, Jürgen Kleine-Vehn & Jiří Friml

  2. Department of Plant Biotechnology and Genetics, Ghent University, B-9052 Gent, Belgium

    Zhaojun Ding, Łukasz Łangowski, Jürgen Kleine-Vehn & Jiří Friml

  3. Molecular and Developmental Genetics, Institute of Biology Leiden, Leiden University, Sylviusweg 72, 2333 BE, The Netherlands

    Carlos S. Galván-Ampudia, Yuanwei Fan & Remko Offringa

  4. Center for Integrative Genomics, Genopode Building, University of Lausanne, CH-1015 Lausanne, Switzerland

    Emilie Demarsy & Christian Fankhauser

  5. Graduate School of Biological Sciences, Nara Institute of Science and Technology, 630-0101 Ikoma, Japan

    Miyo T. Morita & Masao Tasaka

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Contributions

Z.D., C.S.G-A., E.D., M.T., R.O., C.F. and J.F. conceived the study and designed the experiments. Z.D., E.D., C.S.G-A., J.K-V., Ł.Ł., Y.F. and M.T.M. carried out the experiments and analysed the data. Z.D. and J.F. wrote the manuscript.

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Correspondence to Jiří Friml.

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Ding, Z., Galván-Ampudia, C., Demarsy, E. et al. Light-mediated polarization of the PIN3 auxin transporter for the phototropic response in Arabidopsis. Nat Cell Biol 13, 447–452 (2011). https://doi.org/10.1038/ncb2208

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