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

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.

References

  1. Whippo, C. W. & Hangarter, R. P. Phototropism: bending towards enlightenment. Plant Cell 18, 1110–1119 (2006).

    Article  CAS  Google Scholar 

  2. Sakai, T. et al. Arabidopsis nph1 and npl1: blue light receptors that mediate both phototropism and chloroplast relocation. Proc. Natl Acad. Sci. USA 98, 6969–6974 (2001).

    Article  CAS  Google Scholar 

  3. Briggs, W. R. et al. The phototropin family of photoreceptors. Plant Cell 13, 993–997 (2001).

    Article  CAS  Google Scholar 

  4. Inada, S., Ohgishi, M., Mayama, T., Okada, K. & Sakai, T. RPT2 is a signal transducer involved in phototropic response and stomatal opening by association with phototropin 1 in Arabidopsis thaliana. Plant Cell 16, 887–896 (2004).

    Article  CAS  Google Scholar 

  5. Lariguet, P. et al. PHYTOCHROME KINASE SUBSTRATE 1 is a phototropin 1 binding protein required for phototropism. Proc. Natl Acad. Sci. USA 103, 10134–10139 (2006).

    Article  CAS  Google Scholar 

  6. Motchoulski, A. & Liscum, E. Arabidopsis NPH3: a NPH1 photoreceptor-interacting protein essential for phototropism. Science 286, 961–964 (1999).

    Article  CAS  Google Scholar 

  7. Haga, K., Takano, M., Neumann, R. & Iino, M. The rice COLEOPTILE PHOTOTROPISM1 gene encoding an ortholog of Arabidopsis NPH3 is required for phototropism of coleoptiles and lateral translocation of auxin. Plant Cell 17, 103–115 (2005).

    Article  CAS  Google Scholar 

  8. Went, F. W. Reflections and speculations. Annu. Rev. Plant Physiol. 25, 1–26 (1974).

    Article  CAS  Google Scholar 

  9. Li, Y., Hagen, G. & Guilfoyle, T. J. An auxin-responsive promoter is differentially induced by auxin gradients during tropisms. Plant Cell 3, 1167–1175 (1991).

    Article  CAS  Google Scholar 

  10. Esmon, C. A. et al. A gradient of auxin and auxin-dependent transcription precedes tropic growth responses. Proc. Natl Acad. Sci. USA 103, 236–241 (2006).

    Article  CAS  Google Scholar 

  11. Fuchs, I., Philippar, K., Ljung, K., Sandberg, G. & Hedrich, R. Blue light regulates an auxin-induced K+-channel gene in the maize coleoptile. Proc. Natl Acad. Sci. USA 100, 11795–11800 (2003).

    Article  CAS  Google Scholar 

  12. Briggs, W. R. Mediation of phototropic responses of corn coleoptiles by lateral transport of auxin. Plant Physiol. 38, 237–247 (1963).

    Article  CAS  Google Scholar 

  13. Epel, B. L., Warmbrodt, R. P. & Bandurski, R. S. Studies on the longitudinal and lateral transport of IAA in the shoots of etiolated corn seedlings. J. Plant Physiol. 140, 310–318 (1992).

    Article  CAS  Google Scholar 

  14. Bethany, B. S-E. & EL Liscum, E. Disruptions in AUX1-dependent auxin influx alter hypocotyl phototropism in Arabidopsis. Mol. Plant 1, 129–144 (2008).

    Article  Google Scholar 

  15. Swarup, R. et al. Root gravitropism requires lateral root cap and epidermal cells for transport and response to a mobile auxin signal. Nat. Cell Biol. 7, 1057–1065 (2005).

    Article  CAS  Google Scholar 

  16. Geisler, M. & Murphy, A. S. The ABC of auxin transport: the role of p-glycoproteins in plant development. FEBS Lett. 580, 1094–1102 (2006).

    Article  CAS  Google Scholar 

  17. Petrášek, J. et al. PIN proteins perform a rate-limiting function in cellular auxin efflux. Science 312, 914–918 (2006).

    Article  Google Scholar 

  18. Winiewska, J. et al. Polar PIN localization directs auxin flow in plants. Science 312, 883 (2006).

    Article  Google Scholar 

  19. Blakeslee, J. J. et al. Relocalization of the PIN1 auxin efflux facilitator plays a role in phototropic responses. Plant Physiol. 134, 28–31 (2004).

    Article  CAS  Google Scholar 

  20. Friml, J., Winiewska, J., Benková, E., Mendgen, K. & Palme, K. Lateral relocation of auxin efflux regulator PIN3 mediates tropism in Arabidopsis. Nature 415, 806–809 (2002).

    Article  Google Scholar 

  21. Benková, E. et al. Local, efflux-dependent auxin gradients as a common module for plant organ formation. Cell 115, 591–602 (2003).

    Article  Google Scholar 

  22. Friml, J. et al. Efflux-dependent auxin gradients establish the apical-basal axis of Arabidopsis. Nature 426, 147–153 (2003).

    Article  CAS  Google Scholar 

  23. Blakeslee, J. J. et al. Interactions among PIN-FORMED and P-glycoprotein auxin transporters in Arabidopsis. Plant Cell 19, 131–147 (2007).

    Article  CAS  Google Scholar 

  24. Mravec, J. et al. Interaction of PIN and PGP transport mechanisms in auxin distribution-dependent development. Development 135, 3345–3354 (2008).

    Article  CAS  Google Scholar 

  25. Nagashima, A. et al. Phytochromes and cryptochromes regulate the differential growth of Arabidopsis hypocotyls in both a PGP19-dependent and a PGP19-independent manner. Plant J. 53, 516–529 (2008).

    Article  CAS  Google Scholar 

  26. Gendreau, E. et al. Cellular basis of hypocotyl growth in Arabidopsis thaliana. Plant Physiol. 114, 295–305 (1997).

    Article  CAS  Google Scholar 

  27. Gray, W. M., Ostin, A., Sandberg, G., Romano, C. P. & Estelle, M. High temperature promotes auxin-mediated hypocotyl elongation in Arabidopsis. Proc. Natl Acad. Sci. USA 95, 7197–7202 (1998).

    Article  CAS  Google Scholar 

  28. Abas, L. et al. Intracellular trafficking and proteolysis of the Arabidopsis auxin-efflux facilitator PIN2 are involved in root gravitropism. Nat. Cell Biol. 8, 249–256 (2006).

    Article  CAS  Google Scholar 

  29. Kleine-Vehn, J. et al. ARF GEF-dependent transcytosis and polar delivery of PIN auxin carriers in Arabidopsis. Curr. Biol. 18, 526–531 (2008).

    Article  CAS  Google Scholar 

  30. Dhonukshe, P. et al. Clathrin-mediated constitutive endocytosis of PIN auxin efflux carriers in Arabidopsis. Curr. Biol. 17, 520–527 (2007).

    Article  CAS  Google Scholar 

  31. Geldner, N., Friml, J., Stierhof, Y. D., Jürgens, G. & Palme, K. Auxin transport inhibitors block PIN1 cycling and vesicle trafficking. Nature 413, 425–428 (2001).

    Article  CAS  Google Scholar 

  32. Shevell, D. E. et al. EMB30 is essential for normal cell division, cell expansion, and cell adhesion in Arabidopsis and encodes a protein that has similarity to Sec7. Cell 77, 1051–1062 (1994).

    Article  CAS  Google Scholar 

  33. Geldner, N. et al. The Arabidopsis GNOM ARF-GEF mediates endosomal recycling, auxin transport, and auxin-dependent plant growth. Cell 112, 219–230 (2003).

    Article  CAS  Google Scholar 

  34. Geldner, N. et al. Partial loss-of-function alleles reveal a role for GNOM in auxin transport-related, post-embryonic development of Arabidopsis. Development 131, 389–400 (2004).

    Article  CAS  Google Scholar 

  35. Kaiserli, E., Sullivan, S., Jones, M. A., Feeney, K. A. & Christie, J. M. Domain swapping to assess the mechanistic basis of Arabidopsis phototropin 1 receptor kinase activation and endocytosis by blue light. Plant Cell 21, 3226–3244 (2009).

    Article  CAS  Google Scholar 

  36. Wan, Y. L. et al. The subcellular localization and blue light-induced movement of phototropin 1-GFP in etiolated seedlings of Arabidopsis thaliana. Mol. Plant 103, 103–117 (2008).

    Article  Google Scholar 

  37. Christensen, S. K., Dagenais, N., Chory, J. & Weigel, D. Regulation of auxin response by the protein kinase PINOID. Cell 100, 469–478 (2000).

    Article  CAS  Google Scholar 

  38. Benjamins, R., Quint, A., Weijers, D., Hooykaas, P. & Offringa, R. The PINOID protein kinase regulates organ development in Arabidopsis by enhancing polar auxin transport. Development 128, 4057–4067 (2001).

    CAS  PubMed  Google Scholar 

  39. Friml, J. et al. A PINOID-dependent binary switch in apical-basal PIN polar targeting directs auxin efflux. Science 306, 862–865 (2004).

    Article  CAS  Google Scholar 

  40. Michniewicz, M. et al. Antagonistic regulation of PIN phosphorylation by PP2A and PINOID directs auxin flux. Cell 130, 1044–1056 (2007).

    Article  CAS  Google Scholar 

  41. Huang, F. et al. Phosphorylation of conserved PIN motifs directs Arabidopsis PIN1 polarity and auxin transport. Plant Cell 22, 1129–1142 (2010).

    Article  CAS  Google Scholar 

  42. Inoue, S. et al. Blue light-induced autophosphorylation of phototropin is a primary step for signalling. Proc. Natl Acad. Sci. USA 105, 5626–5631 (2008).

    Article  CAS  Google Scholar 

  43. Dhonukshe, P. et al. Plasma membrane bound AGC3 kinases phosphorylate PIN auxin carriers at TPRXS(N/S) motifs to direct apical PIN recycling. Development 137, 3245–3255 (2010).

    Article  CAS  Google Scholar 

  44. Sorefan, K. et al. A regulated auxin minimum is required for seed dispersal in Arabidopsis. Nature 459, 583–586 (2009).

    Article  CAS  Google Scholar 

  45. Kleine-Vehn, J. et al. PIN auxin efflux carrier polarity is regulated by PINOID kinase-mediated recruitment into GNOM-independent trafficking in Arabidopsis. Plant Cell 21, 3839–3849 (2009).

    Article  CAS  Google Scholar 

  46. Kleine-Vehn, J., Ding, Z., Jones, A. R., Tasaka, M., Morita, M. T. & Friml, J. Gravity-induced PIN transcytosis for polarization of auxin fluxes in gravity-sensing root cells. Proc. Natl Acad. Sci. USA 107, 22344–22349 (2010).

    Article  CAS  Google Scholar 

  47. Zádníková, P. et al. Role of PIN-mediated auxin efflux in apical hook development of Arabidopsis thaliana. Development 137, 607–617 (2010).

    Article  Google Scholar 

  48. Hellemans, J., Mortier, G., De Paepe, A., Speleman, F. & Vandesompele, J. qBase relative quantification framework and software for management and automated analysis of real-time quantitative PCR data. Genome Biol. 8, R19.1–R19.14 (2007).

    Article  Google Scholar 

  49. Christie, J. M., Swartz, T. E., Bogomolni, R. A. & Briggs, W. R. Phototropin LOV domains exhibit distinct roles in regulating photoreceptor function. Plant J. 32, 205–219 (2002).

    Article  CAS  Google Scholar 

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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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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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