Skip to main content

Polar auxin transport — old questions and new concepts?

  • Chapter
Auxin Molecular Biology

Abstract

Polar auxin transport controls multiple aspects of plant development including differential growth, embryo and root patterning and vascular tissue differentiation. Identification of proteins involved in this process and availability of new tools enabling’ visualization’ of auxin and auxin routes in planta largely contributed to the significant progress that has recently been made. New data support classical concepts, but several recent findings are likely to challenge our view on the mechanism of auxin transport. The aim of this review is to provide a comprehensive overview of the polar auxin transport field. It starts with classical models resulting from physiological studies, describes the genetic contributions and discusses the molecular basis of auxin influx and efflux. Finally, selected questions are presented in the context of developmental biology, integrating available data from different fields.

This is a preview of subscription content, log in via an institution to check access.

Access this chapter

Chapter
USD 29.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD 39.99
Price excludes VAT (USA)
  • Available as EPUB and PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD 54.99
Price excludes VAT (USA)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info
Hardcover Book
USD 54.99
Price excludes VAT (USA)
  • Durable hardcover edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Institutional subscriptions

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

Abbreviations

AEI:

auxin efflux inhibitors

agr:

agravitropic

ARF:

auxin response factor

ARF GEF:

guanine nucleotide exchange factor on ADP-ribosylation factor G protein

BFA:

Brefeldin A

eir:

ethylene-insensitive root

IAA:

indole-3-acetic acid

1-NAA:

1-naphtylacetic acid

NPA:

1-N-naphthylphthalamic acid

PAT:

polar auxin transport

rcnl:

roots curl in NPA

TIBA:

2,3,5’-triiodobenzoic acid

tir:

transport inhibitor response

References

  • Baker, D.A. 2000. Long-distance vascular transport of endogenous hormones in plants and their role in source: sink regulation. Israel J. Plant Sci. 48: 199–203.

    Article  CAS  Google Scholar 

  • Benjamins, R., Quint, A., Weijers, D., Hooykaas, P. and Offringa, R. 2001. The PINOID protein kinase regulates organ development in Arabidopsis by enhancing polar auxin transport. Development, 28: 4057–4067.

    Google Scholar 

  • Bennett, M.J., Marchant, A., Green, H.G., May, S.T., Ward, S.P., Millner, P.A., Walker, A.R., Schulz, B. and Feldmann, K.A. 1996. Arabidopsis AUX1 gene: a permease-like regulator of root gravitropism. Science 273: 948–950.

    Article  PubMed  CAS  Google Scholar 

  • Benning, C. 1986. Evidence supporting a model of voltage-dependent uptake of auxin into cucurbita-pepo vesicles. Planta 169: 228–237.

    Article  CAS  Google Scholar 

  • Berleth, T. and Jürgens, G. 1993. The role of the MONOPTEROS gene in organizing the basal body region of the Arabidopsis embryo. Development 118: 575–587.

    Google Scholar 

  • Bernasconi, P., Bhavesh, P.C., Reagan, J.D. and Subramanian, M.V. 1996. The N-naphthylphthalamic acid-binding protein is an integral membrane protein. Plant Physiol. 111: 427–432.

    PubMed  CAS  Google Scholar 

  • Cambridge, A.P. and Morris, D.A. 1996. Transfer of exogenous auxin from the phloem to the polar auxin transport pathway in pea (Pisum sativum L.). Planta 199: 583–588.

    Article  CAS  Google Scholar 

  • Camus, G. 1949. Recherches sur le role de bourgeons dans les phénomènes de morphogènes. Rev. Cytol. Biol. Vég. 11: 1–195.

    CAS  Google Scholar 

  • Casimiro, I., Marchant, A., Bhalerao, R.P., Beeckman, T., Dhooge, S., Swarup, R., Graham, N., Inzé, D., Sandberg, G., Casero, P.J. and Bennett, M. 2001. Auxin transport promotes Arabidopsis lateral root initiation. Plant Cell. 13: 843–852.

    PubMed  CAS  Google Scholar 

  • Chen, R., Hilson, P., Sedbrook, J., Rosen, E., Caspar, T. and Masson, P.H. 1998. The Arabidopsis thaliana AGRAV1TROPIC1 gene encodes a component of polar auxin-transport efflux carrier. Proc. Natl. Acad. Sci. USA 95: 15112–15117.

    Article  PubMed  CAS  Google Scholar 

  • Christensen, S.K., Dagenais, N., Chory, J. and Weigel, D. 2000. Regulation of auxin response by the protein kinase PINOID. Cell 100: 469–478.

    Article  PubMed  CAS  Google Scholar 

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

    PubMed  CAS  Google Scholar 

  • Darwin, C. and Darwin, F. 1881. The power of movement in plants (Deutsche Übersetzung: Das Bewegungsvermögen der Planze). Darwins gesammelte Werke, Bd. 13, Schweizer-bart’sche Verlagsbuchhandlung, Stuttgart, Germany.

    Google Scholar 

  • Davies, P.J. 1995. Plant Hormones: Physiology, Biochemistry and Molecular Biology. Martinus Nijhoff, Dordrecht, Netherlands.

    Google Scholar 

  • Delbarre, A., Muller, P. and Guern, J. 1998. 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.

    Article  PubMed  CAS  Google Scholar 

  • Epel, B.L., Warmbrodt, R.P. and Bandurski., R.S. 1992. The ethylene signal transduction pathway in plants. Science 268: 667–675.

    Google Scholar 

  • Firn, R.D., Wagstaff, C. and Digby, J. 2000. The use of mutants to probe models of gravitropism. J. Exp. Bot. 51: 1323–1340.

    Article  PubMed  CAS  Google Scholar 

  • Friml, J., Wisniewska, J., Benková, E., Mendger, K. and Palme, K. 2002a. Lateral relocation of auxin efflux regulator AtPIN3 mediates tropism in Arabidopsis. Nature: in press.

    Google Scholar 

  • Friml, J., Benková, E., Blilou, I., Wisniewska, J., Hamann, T., Ljung, K., Woody, S., Sandberg, G., Scheres, B., Jürgens, G. and Palme, K. 2002b. AtPIN4 mediates sink driven auxin gradients and patterning in Arabidopsis roots. Submitted.

    Google Scholar 

  • Gälweiler, L., Guan, C., Müller, A., Wisman, E., Mendgen, K., Yephremov, A. and Palme, K. 1998. Regulation of polar auxin transport by AtPIN1 in Arabidopsis vascular tissue. Science 282: 2226–2230.

    Article  PubMed  Google Scholar 

  • Garbers, C., DeLong, A., Deruere, J., Bernasconi, P. and Soll, D. 1996. A mutation in protein phosphatase 2A regulatory subunit A affects auxin transport in Arabidopsis. EMBO J. 15: 2115–2124.

    PubMed  CAS  Google Scholar 

  • Gaxiola, R.A., Juan, D.S., Klausner, R.D. and Fink, G.R. 1998. The yeast CLC chloride channel functions in cation homeostasis. Proc. Natl. Acad. Sci USA 95: 4046–4050.

    Article  PubMed  CAS  Google Scholar 

  • Geldner, N., Friml, J., Stierhof, YD., Jurgens, G. and Palme, K. 2001. Auxin transport inhibitors block PIN1 cycling and vesicle trafficking. Nature 413: 425–428.

    Article  PubMed  CAS  Google Scholar 

  • Gil, P., Dewey, E., Friml, J., Zhao, Y., Snowden, K.C., Putterill, J., Palme, K., Estelle, M. and Chory, J. 2001. BIG: a calossin-like protein required for polar auxin transport in Arabidopsis. Genes Dev. 15: 1985–1997.

    Article  PubMed  CAS  Google Scholar 

  • Goldsmith, M.H.M. 1977. The polar transport of auxin. Annu. Rev. Plant. Physiol. 28: 439–478.

    Article  CAS  Google Scholar 

  • Hadfi, K., Speth, V. and Neuhaus, G. 1998. Auxin-induced developmental patterns in Brassica juncea embryos. Development 125: 879–887.

    PubMed  CAS  Google Scholar 

  • Hardtke, C.S. and Berleth, T. 1998. The Arabidopsis gene MONOPTEROS encodes a transription factor mediating embryo axis formation and vascular development. EMBO J. 17: 1405–1411.

    Article  PubMed  CAS  Google Scholar 

  • Hertel, R. 1983. The mechanism of auxin transport as a model for auxin action. Z. Pflanzenphysiol. 112: 53–67.

    CAS  Google Scholar 

  • Hobbie, L.J. 1998. Auxin: molecular genetic approaches in Arabidopsis. Plant Physiol. Biochem. 36: 91–102.

    Article  CAS  Google Scholar 

  • Imhoff, V., Muller, P., Guern, J. and Delbarre, A. 2000. Inhibitors of the carrier-mediated influx of auxin in suspension-cultured tobacco cells. Planta 210: 580–588.

    Article  PubMed  CAS  Google Scholar 

  • Katekar, G.F and Geisler, A.E. 1977. Auxin transport inhibitors. Plant Physiol. 60: 826–829.

    Article  PubMed  CAS  Google Scholar 

  • Kerk, N. and Feldman, L. 1994. The quiescent center in roots of maize: initiation, maintenance and role in organization of the root apical meristem. Protoplasma 183: 100–106.

    Article  CAS  Google Scholar 

  • Kerk, N.M., Jiang, K. and Feldman, L.J. 2000. Auxin metabolism in the root apical meristem. Plant Physiol. 122: 925–932.

    Article  PubMed  CAS  Google Scholar 

  • Knutson V.P. 1991. Cellular trafficking and processing of the insulin receptor. FASEB J. 5: 2130–2138.

    PubMed  CAS  Google Scholar 

  • Koizumi, K., Sugiyama, M. and Fukuda, H. 2000. A series of novel mutants of Arabidopsis thaliana that are defective in the formation of continuous vascular network: calling the auxin signal flow canalization hypothesis into question. Development 127: 3197–3204.

    PubMed  CAS  Google Scholar 

  • Lalonde, S., Boles, E., Hellmann, H., Barker, L., Patrick, J.W., Frommer, W.B. and Ward, J. 1999. The dual function of sugar carriers: transport and sugar sensing. Plant Cell 11: 707–726.

    PubMed  CAS  Google Scholar 

  • Lehman, A., Black, R. and Ecker, J.R. 1996. HOOKLESS1, an ethylene response gene, is required for differential cell elongation in the Arabidopsis hypocotyl. Cell 85: 183–194.

    Article  PubMed  CAS  Google Scholar 

  • Li, Y., Hagen, G. and Guilfoyle, T.J. 1991. An auxin-responsive promoter is differentially induced by auxin gradients during tropisms. Plant Cell 3: 1167–1176.

    PubMed  CAS  Google Scholar 

  • Lincoln, C., Britton, J.H. and Estelle, M. 1990. Growth and development of the axr1 mutants of Arabidopsis. Plant Cell 2: 1071–1080.

    PubMed  CAS  Google Scholar 

  • Ljung, K., Ostin, A., Lioussanne, L. and Sandberg, G. 2001. Developmental regulation of indole-3-acetic acid turnover in Scots pine seedlings. Plant Physiol. 125: 464–475.

    Article  PubMed  CAS  Google Scholar 

  • Lomax, T.L., Mehlhorn, R.J. and Briggs, W.R. 1985. Active auxin uptake by zucchini membrane vesicles: quantitation using ESR volume and ΔpH determinations. Proc. Natl. Acad. Sci USA 82 1986: 6541–6545.

    Article  PubMed  CAS  Google Scholar 

  • Lomax, T.L., Muday, G.K. and Rubery, P.H. 1995. Auxin transport. In: P.J. Davies (Ed.) Plant Hormones: Physiology, Biochemistry and Molecular Biology, Kluwer, Dordrecht, Netherlands, pp. 509–530.

    Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Maher, E.P. and Martindale, S.J. 1980. Mutants of Arabidopsis thaliana with altered responses to auxins and gravity. Biochem. Genet. 18: 1041–1053.

    Article  PubMed  CAS  Google Scholar 

  • Marchant, A., Kargul, J., May, ST., Muller, P., Delbarre, A., Perrot-Rechenmann, C. and Bennett, M.J. 1999. AUX1 regulates root gravitropism in Arabidopsis by facilitating uptake within root apical tissue. EMBO J. 18: 2066–2073.

    Article  PubMed  CAS  Google Scholar 

  • Mattsson, J., Sung, Z.R. and Berleth, T. 1999. Responses of plant vascular system to auxin transport inhibition. Development 126: 2979–2991.

    PubMed  CAS  Google Scholar 

  • Mayer, U., Buettner, G. and Jürgens, G. 1993. Apical-basal pattern formation in the Arabidopsis embryo: studies on the role of the gnomgem. Development 117: 149–162.

    Google Scholar 

  • Morris, D. A. and Robinson, J. 1998. 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.

    Article  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Morris, D.A., Rubery, P.H., Jarman, J. and Sabater, M. 1991. Effects of inhibitors of protein synthesis on transmembrane auxin transport in Cucurbita pepo L. hypocotyl segments. J. Exp. Bot. 42: 773–783.

    Article  CAS  Google Scholar 

  • Müller, A., Guan, C., Gälweiler, L., Tänzler, P., Huijser, P., Marchant, A., Parry, G., Bennet, M., Wisman, E. and Palme, K. 1998. AtPIN2 defines a locus of Arabidopsis for root gravitropism control. EMBO J. 17: 6903–6911.

    Article  PubMed  Google Scholar 

  • Newcomb, W. and Wetherell, D.F. 1970. The effects of 2,4,6-trichlorophenoxyacetic acid on embryogenesis in wild type carrot tissue cultures. Bot. Gaz. 131: 242–245.

    Article  CAS  Google Scholar 

  • Normanly, J., Cohen, J.D. and Fink, G.R. 1991. Arabidopsis thaliana auxotrophs reveal a tryptophan-independent biosynthetic pathway for indole-3-acetic acid. Proc. Natl. Acad. Sci. USA 90: 10355–10359.

    Article  Google Scholar 

  • Nowacki, J. and Bandurski, R.S. 1980. Myo-inositol esters of indole-3-acetic acid as seed auxin precursors of Zea mays L. Plant Physiol. 65: 422–427.

    Article  PubMed  CAS  Google Scholar 

  • Okada, K., Ueda, J., Komaki, M.K., Bell, C.J. and Shimura, Y. 1991. Requirement of the auxin polar transport system in early stages of Arabidopsis floral bud formation. Plant Cell 3: 677–684.

    PubMed  CAS  Google Scholar 

  • Palme, K. and Galweiler, L. 1999. PIN-pointing the molecular basis of auxin transport. Curr. Opin. Plant Biol. 2: 375–381.

    Article  PubMed  CAS  Google Scholar 

  • Parry, G., Delbarre, A., Marchant, A., Swarup, R., Napier, R., Perrot-Rechenmann, C. and Bennett, M.J. 2001. Novel auxin transport inhibitors phenocopy the auxin influx carrier mutation auxL Plant J. 25:399–406.

    Article  PubMed  CAS  Google Scholar 

  • Przemeck, G.K., Mattsson, J., Hardtke, C.S., Sung, Z.R. and Berleth, T. 1996. Studies on the role of the Arabidopsis gene MONOPTEROS in vascular development and plant cell axialization. Planta 200: 229–237.

    Article  PubMed  CAS  Google Scholar 

  • Raven, J.A. 1975. Transport of indolacetic acid in plant cells in relation to pH and electrical potential gradients, and its significance for polar IAA transport. New Phytol. 74: 163–172.

    Article  CAS  Google Scholar 

  • Rashotte, A.M., Brady, S., Reed, R., Ante, S. and Muday, G.K. 2000. Basipetal auxin transport is required for gravitropism in roots of Arabidopsis. Plant Physiol. 122: 481–490.

    Article  PubMed  CAS  Google Scholar 

  • Rashotte, A.M., DeLong, A. and Muday, G.K. 2001. Genetic and chemical reductions in protein phosphatase activity alter auxin transport, gravity response, and lateral root growth. Plant Cell 13: 1683–1697.

    PubMed  CAS  Google Scholar 

  • Reinhardt, D., Mandel, T. and Kuhlemeier, C. 2000. Auxin regulates the initiation and radial position of plant lateral organs. Plant Cell 12:507–518.

    PubMed  CAS  Google Scholar 

  • Rubery, P.H. 1990. Phytotropins: receptors and endogenous ligands. Symp. Soc. Exp. Biol. 44: 119–146.

    PubMed  CAS  Google Scholar 

  • Rubery, P.H. und Sheldrake, A.R. 1974. Carrier-mediated auxin transport. Planta 118: 101–121.

    Article  CAS  Google Scholar 

  • Ruegger, M., Dewey, E., Hobbie, L., Brown, D., Bernasconi, P., Turner, J., Muday, G.K. and Estelle, M. 1997. 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.

    PubMed  CAS  Google Scholar 

  • Sabatini, S., Beis, D., Wolkenfelt, H., Murfett, J., Guilfoyle, T., Malamy, J., Benfey, P., Leyser, O., Bechtold, N., Weisbeek, P. and Scheres, B. 1999. An auxin-dependent distal organizer of pattern and polarity in the Arabidopsis root. Cell 99: 463–472.

    Article  PubMed  CAS  Google Scholar 

  • Sachs, T. 1989. The development of vascular networks during leaf development. Curr. Top. Plant Biochem. Physiol. 18: 168–183.

    Google Scholar 

  • Schiavone, F.M. and Cooke, T.J. 1987. Unusual patterns of somatic embryogenesis in the domesticated carrot developmental effects of exogenous auxins and auxin transport inhibitors. Cell Differ. 21:53–62.

    Article  PubMed  CAS  Google Scholar 

  • Steinmann, T., Geldner, N., Grebe, M., Mangold, S., Jackson, CL., Paris, S., Gälweiler, L., Palme, K. and Jürgens, G. 1999. Coordinated polar localization of auxin efflux carrier PIN1 by GNOM ARF GEE Science 286: 316–318.

    Article  PubMed  CAS  Google Scholar 

  • Swarup, R., Friml, J., Marchant, A., Ljung, K., Sandberg, G., Palme, K. and Bennett, M. 2001. Localisation of the auxin permease AUX1 suggests two functionally distinct hormone transport pathways operate in the Arabidopsis root apex. Genes Dev., in press.

    Google Scholar 

  • Uggia, C., Mellerowicz, E.J. and Sundberg, B. 1998. Indole-3-acetic acid controls cambial growth in scots pine by positional signalling. Plant Physiol. 117: 113–121.

    Article  Google Scholar 

  • Utsuno, K., Shikanai, T., Yamada, Y. and Hashimoto, T. 1998. AGR, an Agravitropic locus of Arabidopsis thaliana, encodes a novel membrane protein family member. Plant Cell Physiol. 39: 1111–1118.

    Article  PubMed  CAS  Google Scholar 

  • Went, F.W. 1974. Reflections and speculations. Annu. Rev. Plant Physiol. 25: 1–26.

    Article  CAS  Google Scholar 

  • Wetmore, R.H. and Rier, J.P. 1963. Experimental induction of vascular tissues in callus of angiosperms. Am. J. Bot. 50: 418–430.

    Article  CAS  Google Scholar 

  • Yamamoto, M. and Yamamoto, K.T. 1999. Effects of natural and synthetic auxins on the gravitropic growth habit of roots in two auxin-resistant mutants of Arabidopsis, axr1 and axr4: evidence for defects in the auxin influx mechanism of axr4. J. Plant Res. 112:391–396.

    Article  PubMed  CAS  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Editor information

Catherine Perrot-Rechenmann Gretchen Hagen

Rights and permissions

Reprints and permissions

Copyright information

© 2002 Kluwer Academic Publishers

About this chapter

Cite this chapter

Friml, J., Palme, K. (2002). Polar auxin transport — old questions and new concepts?. In: Perrot-Rechenmann, C., Hagen, G. (eds) Auxin Molecular Biology. Springer, Dordrecht. https://doi.org/10.1007/978-94-010-0377-3_2

Download citation

  • DOI: https://doi.org/10.1007/978-94-010-0377-3_2

  • Publisher Name: Springer, Dordrecht

  • Print ISBN: 978-94-010-3917-8

  • Online ISBN: 978-94-010-0377-3

  • eBook Packages: Springer Book Archive

Publish with us

Policies and ethics