Two mechanisms regulate directional cell growth in Arabidopsis lateral roots

Abstract

Morphogenesis in plants depends critically on directional (anisotropic) growth. This occurs principally perpendicular to the net orientation of cellulose microfibrils (CMFs), which is in turn controlled by cortical microtubules (CMTs). In young lateral roots of Arabidopsis thaliana, growth anisotropy also depends on RAB-A5c, a plant-specific small GTPase that specifies a membrane trafficking pathway to the geometric edges of cells. Here we investigate the functional relationship between structural anisotropy at faces and RAB-A5c activity at edges during lateral root development. We show that surprisingly, inhibition of RAB-A5c function is associated with increased CMT/CMF anisotropy. We present genetic, pharmacological, and modelling evidence that this increase in CMT/CMF anisotropy partially compensates for loss of an independent RAB-A5c-mediated mechanism that maintains anisotropic growth in meristematic cells. We show that RAB-A5c associates with CMTs at cell edges, indicating that CMTs act as an integration point for both mechanisms controlling cellular growth anisotropy in lateral roots.

Data availability

Source data files have been provided for Figure 1, Figure 4, Figure 5, Figure 3, Figure 1 - Figure Supplement 2, Figure 1 - Figure Supplement 3, and Figure 3 - Figure Supplement 1. The source code file has been provided for the computational model (Figure 2 and Fiugre 2 - Figure Supplements).

Article and author information

Author details

  1. Charlotte Kirchhelle

    Department of Plant Sciences, University of Oxford, Oxford, United Kingdom
    For correspondence
    charlotte.kirchhelle@plants.ox.ac.uk
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0001-8448-6906
  2. Daniel Garcia-Gonzalez

    Department of Engineering Science, University of Oxford, Oxford, United Kingdom
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0003-4692-3508
  3. Niloufer G Irani

    Department of Plant Sciences, University of Oxford, Oxford, United Kingdom
    Competing interests
    The authors declare that no competing interests exist.
  4. Antoine Jérusalem

    Department of Engineering Science, University of Oxford, Oxford, United Kingdom
    Competing interests
    The authors declare that no competing interests exist.
  5. Ian Moore

    Department of Plant Sciences, University of Oxford, Oxford, United Kingdom
    Competing interests
    The authors declare that no competing interests exist.

Funding

Biotechnology and Biological Sciences Research Council (BB/P01979X/1)

  • Charlotte Kirchhelle
  • Antoine Jérusalem
  • Ian Moore

Leverhulme Trust (RPG-2014-276)

  • Niloufer G Irani
  • Ian Moore

Leverhulme Trust (ECF-2017-483)

  • Charlotte Kirchhelle

John Fell Fund, University of Oxford

  • Charlotte Kirchhelle
  • Antoine Jérusalem
  • Ian Moore

Seventh Framework Programme (ERC Grant Agreement No. 306587)

  • Daniel Garcia-Gonzalez
  • Antoine Jérusalem

The funders had no role in study design, data collection and interpretation, or the decision to submit the work for publication.

Reviewing Editor

  1. Jürgen Kleine-Vehn, University of Natural Resources and Life Sciences, Austria

Publication history

  1. Received: April 26, 2019
  2. Accepted: July 27, 2019
  3. Accepted Manuscript published: July 29, 2019 (version 1)
  4. Version of Record published: September 17, 2019 (version 2)
  5. Version of Record updated: September 26, 2019 (version 3)

Copyright

© 2019, Kirchhelle et al.

This article is distributed under the terms of the Creative Commons Attribution License permitting unrestricted use and redistribution provided that the original author and source are credited.

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  1. Charlotte Kirchhelle
  2. Daniel Garcia-Gonzalez
  3. Niloufer G Irani
  4. Antoine Jérusalem
  5. Ian Moore
(2019)
Two mechanisms regulate directional cell growth in Arabidopsis lateral roots
eLife 8:e47988.
https://doi.org/10.7554/eLife.47988

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