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Root gravitropism requires lateral root cap and epidermal cells for transport and response to a mobile auxin signal

Nature Cell Biology volume 7, pages 1057–1065 (2005)Cite this article

Abstract

Re-orientation of Arabidopsis seedlings induces a rapid, asymmetric release of the growth regulator auxin from gravity-sensing columella cells at the root apex. The resulting lateral auxin gradient is hypothesized to drive differential cell expansion in elongation-zone tissues. We mapped those root tissues that function to transport or respond to auxin during a gravitropic response. Targeted expression of the auxin influx facilitator AUX1 demonstrated that root gravitropism requires auxin to be transported via the lateral root cap to all elongating epidermal cells. A three-dimensional model of the root elongation zone predicted that AUX1 causes the majority of auxin to accumulate in the epidermis. Selectively disrupting the auxin responsiveness of expanding epidermal cells by expressing a mutant form of the AUX/IAA17 protein, axr3-1, abolished root gravitropism. We conclude that gravitropic curvature in Arabidopsis roots is primarily driven by the differential expansion of epidermal cells in response to an influx-carrier-dependent auxin gradient.

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Figure 1: Mapping Arabidopsis root tissues that transport auxin during a gravitropic response.
Figure 2: Modelling carrier-mediated transport of the lateral auxin gradient in the elongation zone.
Figure 3: Auxin-responsive IAA2:uidA reporter expression.
Figure 4: Kinematic analysis of AUX1-dependent root growth.
Figure 5: Root gravitropism requires AUX1 expression in all expanding epidermal cells.
Figure 6: Mapping root tissues that respond to the lateral auxin gradient using axr3-1.
Figure 7: A schematic model for auxin-regulated root gravitropism.

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Acknowledgements

We would like to thank the Nottingham Arabidopsis Stock Centre (NASC) for providing selected GAL4 enhancer trap lines used in this study and D. Weijers for the GAL4-related constructs. We also thank M. Broadley, J. Friml, D. Grierson, C. Hodgman, M. Holdsworth, L. Laplaze, J. Roberts, P.J. White, Z. Wilson and anonymous referees for helpful comments about the manuscript. The work was supported by the Biotechnology and Biological Sciences Research Council (R.S., P.P., K.K., H.M.O.L. and M.J.B.); European Space Agency (R.S. and M.J.B.); EU Training site grant HTMC-CT-2000-00088 awarded to P.P.; Gatsby Charitable Foundation (J.H. and M.J.B.); Formas and V.R. (R.B.).

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Authors and Affiliations

  1. School of Biosciences, University of Nottingham, Nottingham, LE12 5RD, UK

    Ranjan Swarup, Paula Perry & Malcolm J. Bennett

  2. Physics Department, Simon's Rock College, Great Barrington, 01230, MA, USA

    Eric M. Kramer

  3. Department of Biology, University of York, York, YO10 5YW, UK

    Kirsten Knox & H. M. Ottoline Leyser

  4. Department of Plant Sciences, University of Cambridge, Cambridge, CB2 3EA, UK

    Jim Haseloff

  5. Plant Systems Biology, Flemish Institute of Biotechnology (VIB)/University of Ghent, Ghent, B-9052, Belgium

    Gerrit T. S. Beemster

  6. Umeå Plant Science Centre, SLU, Umeå, SE-90183, Sweden

    Rishikesh Bhalerao

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Correspondence to Malcolm J. Bennett.

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Supplementary information

Supplementary Information

Supplementary text providing additional details of the computer model and References plus Supplementary tables S1, S2, S3 and S4 plus Supplementary figures S1, S2, S3, S4 and S5 (PDF 375 kb)

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Swarup, R., Kramer, E., Perry, P. 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). https://doi.org/10.1038/ncb1316

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