1. Cell Biology
  2. Plant Biology

Two mechanisms regulate directional cell growth in Arabidopsis lateral roots

  1. Charlotte Kirchhelle  Is a corresponding author
  2. Daniel Garcia-Gonzalez
  3. Niloufer G Irani
  4. Antoine Jérusalem
  5. Ian Moore
  1. University of Oxford, United Kingdom
https://doi.org/10.7554/eLife.47988
Share this article
Cite this article
  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
  2. Download BibTeX
  3. Download .RIS

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.

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.

Metrics

  • 5,012
    views
  • 849
    downloads
  • 32
    citations

Views, downloads and citations are aggregated across all versions of this paper published by eLife.

Download links

A two-part list of links to download the article, or parts of the article, in various formats.

Downloads (link to download the article as PDF)

Open citations (links to open the citations from this article in various online reference manager services)

Cite this article (links to download the citations from this article in formats compatible with various reference manager tools)

  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

Share this article

https://doi.org/10.7554/eLife.47988

Categories and tags

Research organism

Further reading

    1. Cell Biology

    Small-molecule activation of TFEB alleviates Niemann–Pick disease type C via promoting lysosomal exocytosis and biogenesis

    Kaili Du, Hongyu Chen ... Dan Li
    Research Article

    Niemann–Pick disease type C (NPC) is a devastating lysosomal storage disease characterized by abnormal cholesterol accumulation in lysosomes. Currently, there is no treatment for NPC. Transcription factor EB (TFEB), a member of the microphthalmia transcription factors (MiTF), has emerged as a master regulator of lysosomal function and promoted the clearance of substrates stored in cells. However, it is not known whether TFEB plays a role in cholesterol clearance in NPC disease. Here, we show that transgenic overexpression of TFEB, but not TFE3 (another member of MiTF family) facilitates cholesterol clearance in various NPC1 cell models. Pharmacological activation of TFEB by sulforaphane (SFN), a previously identified natural small-molecule TFEB agonist by us, can dramatically ameliorate cholesterol accumulation in human and mouse NPC1 cell models. In NPC1 cells, SFN induces TFEB nuclear translocation via a ROS-Ca2+-calcineurin-dependent but MTOR-independent pathway and upregulates the expression of TFEB-downstream genes, promoting lysosomal exocytosis and biogenesis. While genetic inhibition of TFEB abolishes the cholesterol clearance and exocytosis effect by SFN. In the NPC1 mouse model, SFN dephosphorylates/activates TFEB in the brain and exhibits potent efficacy of rescuing the loss of Purkinje cells and body weight. Hence, pharmacological upregulating lysosome machinery via targeting TFEB represents a promising approach to treat NPC and related lysosomal storage diseases, and provides the possibility of TFEB agonists, that is, SFN as potential NPC therapeutic candidates.

    1. Cell Biology

    Stratification of enterochromaffin cells by single-cell expression analysis

    Yan Song, Linda J Fothergill ... Gene W Yeo
    Research Article

    Dynamic interactions between gut mucosal cells and the external environment are essential to maintain gut homeostasis. Enterochromaffin (EC) cells transduce both chemical and mechanical signals and produce 5-hydroxytryptamine to mediate disparate physiological responses. However, the molecular and cellular basis for functional diversity of ECs remains to be adequately defined. Here, we integrated single-cell transcriptomics with spatial image analysis to identify 14 EC clusters that are topographically organized along the gut. Subtypes predicted to be sensitive to the chemical environment and mechanical forces were identified that express distinct transcription factors and hormones. A Piezo2+ population in the distal colon was endowed with a distinctive neuronal signature. Using a combination of genetic, chemogenetic, and pharmacological approaches, we demonstrated Piezo2+ ECs are required for normal colon motility. Our study constructs a molecular map for ECs and offers a framework for deconvoluting EC cells with pleiotropic functions.

    1. Cell Biology
    2. Developmental Biology

    Lens Development: Bringing signaling complexity into focus

    Sarah Y Coomson, Salil A Lachke
    Insight

    A study in mice reveals key interactions between proteins involved in fibroblast growth factor signaling and how they contribute to distinct stages of eye lens development.