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Lateral relocation of auxin efflux regulator PIN3 mediates tropism in Arabidopsis

Nature volume 415, pages 806–809 (2002)Cite this article

Abstract

Long-standing models propose that plant growth responses to light or gravity are mediated by asymmetric distribution of the phytohormone auxin1,2,3. Physiological studies implicated a specific transport system that relocates auxin laterally, thereby effecting differential growth4; however, neither the molecular components of this system nor the cellular mechanism of auxin redistribution on light or gravity perception have been identified. Here, we show that auxin accumulates asymmetrically during differential growth in an efflux-dependent manner. Mutations in the Arabidopsis gene PIN3, a regulator of auxin efflux, alter differential growth. PIN3 is expressed in gravity-sensing tissues, with PIN3 protein accumulating predominantly at the lateral cell surface. PIN3 localizes to the plasma membrane and to vesicles that cycle in an actin-dependent manner. In the root columella, PIN3 is positioned symmetrically at the plasma membrane but rapidly relocalizes laterally on gravity stimulation. Our data indicate that PIN3 is a component of the lateral auxin transport system regulating tropic growth. In addition, actin-dependent relocalization of PIN3 in response to gravity provides a mechanism for redirecting auxin flux to trigger asymmetric growth.

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Figure 1: Auxin response during differential hypocotyl growth.
Figure 2: pin3 mutants.
Figure 4: Localization of the PIN3 protein.
Figure 3: Expression of the PIN3 gene.
Figure 5: Subcellular localization, actin-dependent cycling and gravity-dependent asymmetric relocation of the PIN3 protein.

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References

  1. Darwin, C. & Darwin, F. in Darwins Gesammelte Werke Bd. 13 (Schweizer-bart'sche Verlagsbuchhandlung, Stuttgart, 1881).

    Google Scholar 

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

    Article  CAS  Google Scholar 

  3. Hart, J. W. Plant Tropism and Other Movements (Unwin Hyman, London, 1990).

    Google Scholar 

  4. 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 

  5. Li, Y., Hagen, G. & Guilfoyle, T. J. An auxin-responsive promoter is differentially induced by auxin gradients during tropisms. Plant Cell 3, 116–1176 (1991).

    Article  Google Scholar 

  6. Luschnig, C., Gaxiola, R. A., Grisafi, P. & Fink, G. R. EIR1, a root specific protein involved in auxin transport, is required for gravitropism in Arabidopsis thaliana. Genes Dev. 12, 2175–2187 (1998).

    Article  CAS  Google Scholar 

  7. Friml, J. & Palme, K. Polar auxin transport—old questions and new concepts. Plant Mol. Biol. (in the press).

  8. Palme, K. & Gälweiler, L. PIN-pointing the molecular basis of auxin transport. Curr. Opin. Plant Biol. 2, 375–381 (1999).

    Article  CAS  Google Scholar 

  9. Rubery, P. H. & Sheldrake, A. R. Carrier-mediated auxin transport. Planta 118, 101–121 (1974).

    Article  CAS  Google Scholar 

  10. Müller, A. et al. AtPIN2 defines a locus of Arabidopsis for root gravitropism control. EMBO J. 17, 6903–6911 (1998).

    Article  Google Scholar 

  11. Rashotte, A. et al. Basipetal auxin transport is required for gravitropism in roots of Arabidopsis. Plant Physiol. 122, 481–490 (2000).

    Article  CAS  Google Scholar 

  12. Gälweiler, L. et al. Regulation of polar auxin transport by AtPIN1 in Arabidopsis vascular tissue. Science 282, 2226–2230 (1998).

    Article  ADS  Google Scholar 

  13. Morris, D. A. & Thomas, A. A microautoradiographic study of auxin transport in the stem of intact pea seedlings (Pisum sativum L.) J. Exp. Bot. 29, 147–157 (1978).

    Article  CAS  Google Scholar 

  14. Bjorkman, T. & Cleland, R. E. The role of the epidermis and cortex in gravitropic curvature of maize roots. Planta 176, 513–518 (1988).

    Article  CAS  Google Scholar 

  15. Ulmasov, T., Murfett, J., Hagen, G. & Guilfoyle, T. J. Aux/1AA proteins repress expression of reporter genes containing natural and highly active synthetic auxin response elements. Plant Cell 9, 1963–1971 (1997).

    Article  CAS  Google Scholar 

  16. Casimiro, I. et al. Auxin transport promotes Arabidopsis lateral root initiation. Plant Cell 13, 843–852 (2001).

    Article  CAS  Google Scholar 

  17. Friml, J. et al. AtPIN4 mediates sink driven auxin gradients and patterning in Arabidopsis roots. Cell (in the press).

  18. Wisman, E., Cardon, G. H., Fransz, P. & Saedler, H. The behaviour of the autonomous maize transposable element En/Spm in Arabidopsis thaliana allows efficient mutagenesis. Plant Mol. Biol. 37, 989–999 (1998).

    Article  CAS  Google Scholar 

  19. Ruegger, M. et al. Reduced naphthylphthalamic acid binding in the tir3 mutant of Arabidopsis is associated with a reduction in polar auxin transport and diverse morphological defects. Plant Cell 9, 745–757 (1997).

    Article  CAS  Google Scholar 

  20. Jensen, P. J., Hangarter, R. P. & Estelle, M. Auxin transport is required for hypocotyl elongation in light-grown Arabidopsis. Plant Physiol. 16, 455–462 (1998).

    Article  Google Scholar 

  21. Geldner, N. et al. Polar auxin transport inhibitors block PIN1 cycling and vesicle trafficking. Nature 413, 425–428 (2001).

    Article  ADS  CAS  Google Scholar 

  22. Hasenstein, K. H. Gravisensing in plants and fungi. Adv. Space Res. 24, 677–685 (1999).

    Article  ADS  CAS  Google Scholar 

  23. Sievers, A., Sondag, C., Trebacz, K. & Hejnowicz, Z. Gravity induced changes in intracellular potentials in statocytes of cress roots. Planta 197, 392–394 (1995).

    Article  CAS  Google Scholar 

  24. Monshausen, G. B., Zieschang, H. E. & Sievers, A. Differential proton secretion in the apical elongation zone caused by gravistimulation is induced by a signal from the root cap. Plant Cell Environ. 19, 1408–1414 (1996).

    Article  CAS  Google Scholar 

  25. Collings, D. A., Zsuppan, G., Allen, N. S. & Blancaflor, E. B. Demonstration of prominent actin filaments in the root columella. Planta 212, 392–403 (2001).

    Article  CAS  Google Scholar 

  26. Fukaki, H. et al. Genetic evidence that the endodermis is essential for shoot gravitropism in Arabidopsis thaliana. Plant J. 14, 425–430 (1998).

    Article  CAS  Google Scholar 

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Acknowledgements

We thank G. Jürgens for enabling J.F. to accomplish part of this work in his laboratory; P. Tänzler and M. Sauer for technical assistance; H. Vahlenkamp for technical assistance in immunocytochemistry; M. Estelle for providing material and suggestions; T. Altman for BAC filter sets; the ADIS (Automated DNA Isolation and Sequencing) service group for DNA sequencing; ZIGIA (Center for Functional Genomics in Arabidopsis) for the En lines; and N. Geldner, T. Hamann, G. Jürgens, K. Schrick and C. Schwechheimer for comments and critical reading of the manuscript. This work was supported by a fellowship of the DAAD (J.F.), the DFG (Schwerpunktprogramm Phytohormone), the Fonds der chemischen Industrie, the European Communities Biotechnology Programs, the INCO-Copernicus Program and the European Space Agency MAP-Biotechnology Programme.

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Authors and Affiliations

  1. Max-Delbrück-Laboratorium in der Max-Planck-Gesellschaft, Köln, 50829, Germany

    Jiří Friml, Justyna Wiśniewska, Eva Benková & Klaus Palme

  2. Zentrum für Molekularbiologie der Pflanzen, Universität Tübingen, Tübingen, 72076, Germany

    Jiří Friml

  3. Department of Biotechnology, Institute of General and Molecular Biology, Torun, 87–100, Poland

    Justyna Wiśniewska

  4. Lehrstuhl Phytopathologie, Universität Konstanz, Konstanz, 78457, Germany

    Kurt Mendgen

  5. Institut für Biologie II, Universität Freiburg, Freiburg, 79104, Germany

    Klaus Palme

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  1. Jiří Friml
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Correspondence to Jiří Friml or Klaus Palme.

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Friml, J., Wiśniewska, J., Benková, E. et al. Lateral relocation of auxin efflux regulator PIN3 mediates tropism in Arabidopsis. Nature 415, 806–809 (2002). https://doi.org/10.1038/415806a

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