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Auxin transport inhibitors block PIN1 cycling and vesicle trafficking

Nature volume 413, pages 425–428 (2001)Cite this article

Abstract

Polar transport of the phytohormone auxin mediates various processes in plant growth and development, such as apical dominance, tropisms, vascular patterning and axis formation1,2. This view is based largely on the effects of polar auxin transport inhibitors. These compounds disrupt auxin efflux from the cell but their mode of action is unknown3. It is thought that polar auxin flux is caused by the asymmetric distribution of efflux carriers acting at the plasma membrane4. The polar localization of efflux carrier candidate PIN1 supports this model4. Here we show that the seemingly static localization of PIN1 results from rapid actin-dependent cycling between the plasma membrane and endosomal compartments. Auxin transport inhibitors block PIN1 cycling and inhibit trafficking of membrane proteins that are unrelated to auxin transport. Our data suggest that PIN1 cycling is of central importance for auxin transport and that auxin transport inhibitors affect efflux by generally interfering with membrane-trafficking processes. In support of our conclusion, the vesicle-trafficking inhibitor brefeldin A mimics physiological effects of auxin transport inhibitors.

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Figure 1: Reversible inhibition of PIN1 recycling by BFA treatment.
Figure 2: PIN1 localization affected by cytoskeleton-depolymerizing drugs.
Figure 3: Effects of polar auxin transport inhibitor TIBA on protein trafficking.
Figure 4: Physiological effects of BFA.

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References

  1. Estelle, M. Polar auxin transport. New support for an old model. Plant Cell 10, 1775–1778 (1998).

    Article  CAS  Google Scholar 

  2. Berleth, T. & Sachs, T. Plant morphogenesis: long-distance coordination and local patterning. Curr. Opin. Plant Biol. 4, 57–62 (2001).

    Article  CAS  Google Scholar 

  3. Morris, D. A. Transmembrane auxin carrier systems—dynamic regulators of polar auxin transport. Plant Growth Reg. 32, 161–172 (2000).

    Article  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  5. Hadfi, K., Speth, V. & Neuhaus, G. Auxin-induced developmental patterns in Brassica juncea embryos. Development 125, 879–887 (1998).

    CAS  PubMed  Google Scholar 

  6. Mattsson, J., Sung, Z. R. & Berleth, T. Responses of plant vascular systems to auxin transport inhibition. Development 126, 2979–2691 (1999).

    CAS  PubMed  Google Scholar 

  7. Sabatini, S. et al. An auxin-dependent distal organizer of pattern and polarity in the Arabidopsis root. Cell 99, 463–472 (1999).

    Article  CAS  Google Scholar 

  8. Delbarre, A., Muller, P. & Guern, J. Short-lived and phosphorylated proteins contribute to carrier-mediated efflux, but not to influx, of auxin in suspension-cultured tobacco cells. Plant Physiol. 116, 833–844 (1998).

    Article  CAS  Google Scholar 

  9. Morris, D. A. & Robinson, J. S. Targeting of auxin carriers to the plasma membrane: differential effects of brefeldin A on the traffic of auxin uptake and efflux carriers. Planta 205, 606–612 (1998).

    Article  CAS  Google Scholar 

  10. Michalke, W., Katekar, G. F. & Geissler, A. E. Phytotropin-binding sites and auxin transport in Cucurbita pepo: evidence for two recognition sites. Planta 187, 254–260 (1992).

    Article  CAS  Google Scholar 

  11. Cox, D. N. & Muday, G. K. NPA binding activity is peripheral to the plasma membrane and is associated with the cytoskeleton. Plant Cell 6, 1941–1953 (1994).

    Article  CAS  Google Scholar 

  12. Bernasconi, P., Patel, B. C., Reagan, J. D. & Subramanian, M. V. The N-1-naphthylphthalamic acid-binding protein is an integral membrane protein. Plant Physiol. 111, 427–432 (1996).

    Article  CAS  Google Scholar 

  13. Fujita, H. & Syono, K. Genetic analysis of the effects of polar auxin transport inhibitors on root growth in Arabidopsis thaliana. Plant Cell Physiol. 37, 1094–1101 (1996).

    Article  CAS  Google Scholar 

  14. Garbers, C. et al. A mutation in protein phosphatase 2A regulatory subunit A affects auxin transport in Arabidopsis. EMBO J. 15, 2115–2124 (1996).

    Article  CAS  Google Scholar 

  15. 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 

  16. Fujita, H. & Syono, K. PIS1, a negative regulator of the action of auxin transport inhibitors in Arabidopsis thaliana. Plant J. 12, 583–595 (1997).

    Article  CAS  Google Scholar 

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

    Article  ADS  Google Scholar 

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

    Article  Google Scholar 

  19. Steinmann, T. et al. Coordinated polar localization of auxin efflux carrier PIN1 by GNOM ARF GEF. Science 286, 316–318 (1999).

    Article  CAS  Google Scholar 

  20. Klausner, R. D., Donaldson, J. G. & Lippincott-Schwartz, J. Brefeldin A: insights into the control of membrane traffic and organelle structure. J. Cell Biol. 116, 1071–1080 (1992).

    Article  CAS  Google Scholar 

  21. Lippincott-Schwartz, J. et al. Microtubule-dependent retrograde transport of proteins into the ER in the presence of brefeldin A suggests an ER recycling pathway. Cell 60, 821–836 (1990).

    Article  CAS  Google Scholar 

  22. Wood, S. A., Park, J. E. & Brown, W. J. Brefeldin A causes a microtubule-mediated fusion of the trans-Golgi network and early endosomes. Cell 67, 591–600 (1991).

    Article  CAS  Google Scholar 

  23. Satiat-Jeunemaitre, B. & Hawes, C. Redistribution of a Golgi glycoprotein in plant cells treated with brefeldin A. J. Cell Sci. 103, 1153–1156 (1992).

    CAS  Google Scholar 

  24. Satiat-Jeunemaitre, B. et al. Brefeldin A effects in plant and fungal cells: something new about vesicle trafficking? J. Microsc. 181, 162–177 (1996).

    Article  CAS  Google Scholar 

  25. Satiat-Jeunemaitre, B., Steele, C. & Hawes, C. Golgi-membrane dynamics are cytoskeleton dependent: a study on Golgi stack movement induced by brefeldin A. Protoplasma 191, 21–33 (1996).

    Article  CAS  Google Scholar 

  26. Mathur, J., Spielhofer, P., Kost, B. & Chua, N.-H. The actin cytoskeleton is required to elaborate and maintain spatial patterning during trichome cell morphogenesis in Arabidopsis thaliana. Development 126, 5559–5568 (1999).

    CAS  PubMed  Google Scholar 

  27. Lauber, M. H. et al. The Arabidopsis KNOLLE protein is a cytokinesis-specific syntaxin. J. Cell Biol. 139, 1485–1493 (1997).

    Article  CAS  Google Scholar 

  28. Völker, A., Stierhof, Y.-D. & Jürgens, G. Cell cycle-independent expression of the Arabidopsis cytokinesis-specific syntaxin KNOLLE results in mistargeting to the plasma membrane and is not sufficient for cytokinesis. J. Cell Sci. (in the press).

  29. Hager, A. et al. Auxin induces exocytosis and the rapid synthesis of a high-turnover pool of plasma-membrane H+-ATPase. Planta 185, 527–537 (1991).

    Article  CAS  Google Scholar 

  30. Kategar, G. F. & Geissler, A. E. Auxin transport inhibitors. Plant Physiol. 60, 826–829 (1977).

    Article  Google Scholar 

Download references

Acknowledgements

We thank A. Vieten and S. Barth for technical assistance; L. Gälweiler, W. Michalke and K. Roberts for kind gifts of antibodies; S. M. Li for MS/NMR analysis; and M. Godde, M. Heese, T. Hamann, T. Pacher and K. Schrick for helpful comments and critical reading of the manuscript. J. F. was a recipient of a Deutscher Akademischer Austauschdienst fellowship. This work was supported by Deutsche Forschungsgemeinschaft (DFG), Schwerpunktprogramm‘Molekulare Analyse der Phytohormonwirkung’, European Communities Biotechnology Programme and INCO Copernicus Programme (K.P.), and DFG, Sonderforschungsbereich ‘Mechanismen des Zellverhaltens bei Eukaryoten’ (G. J.).

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Author notes

  1. Jiří Friml

    Present address: Zentrum für Molekularbiologie der Pflanzen, Universität Tübingen, Auf der Morgenstelle 3, D-72076, Tübingen, Germany

  2. Niko Geldner and Jiří Friml: These authors contributed equally to this work

Authors and Affiliations

  1. Zentrum für Molekularbiologie der Pflanzen, Universität Tübingen, Auf der Morgenstelle 3, Tübingen, D-72076, Germany

    Niko Geldner, York-Dieter Stierhof & Gerd Jürgens

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

    Jiří Friml & Klaus Palme

  3. Department of Biochemistry, Faculty of Science, Masaryk University, Kotlárská 2, Brno, 61137, Czech Republic

    Jiří Friml

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  1. Niko Geldner
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Correspondence to Gerd Jürgens.

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Geldner, N., Friml, J., Stierhof, YD. et al. Auxin transport inhibitors block PIN1 cycling and vesicle trafficking. Nature 413, 425–428 (2001). https://doi.org/10.1038/35096571

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