Rapid transporter regulation prevents substrate flow traffic jams in boron transport

  1. Naoyuki Sotta
  2. Susan Duncan
  3. Mayuki Tanaka
  4. Sato Takafumi
  5. Athanasius FM Marée  Is a corresponding author
  6. Toru Fujiwara  Is a corresponding author
  7. Verônica A. Grieneisen  Is a corresponding author
  1. The University of Tokyo, Japan
  2. John Innes Centre, United Kingdom
  3. University of Tokyo, Japan

Abstract

Nutrient uptake by roots often involves substrate-dependent regulated nutrient transporters. For robust uptake, the system requires a regulatory circuit within cells and a collective, coordinated behaviour across the tissue. A paradigm for such systems is boron uptake, known for its directional transport and homeostasis, as boron is essential for plant growth but toxic at high concentrations. In Arabidopsis thaliana Boron up- take occurs via diffusion facilitators (NIPs) and exporters (BORs), each presenting distinct polarity. Intriguingly, although boron soil concentrations are homogenous and stable, both transporters manifest strikingly swift boron-dependent regulation. Through mathematical modelling, we demonstrate that slower regulation of these transporters leads to physiologically detrimental oscillatory behaviour. Cells become periodically exposed to potentially cytotoxic boron levels, and nutrient throughput to the xylem becomes hampered. We conclude that, while maintaining homeostasis, swift transporter regulation within a polarised tissue context is critical to prevent intrinsic traffic-jam like behaviour of nutrient flow.

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Article and author information

Author details

  1. Naoyuki Sotta

    Graduate School of Agricultural and Life Sciences, The University of Tokyo, Tokyo, Japan
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0001-5558-5155
  2. Susan Duncan

    Department of Computational and Systems Biology, John Innes Centre, Norwich, United Kingdom
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0001-9581-1145
  3. Mayuki Tanaka

    Graduate School of Agricultural and Life Sciences, University of Tokyo, Tokyo, Japan
    Competing interests
    The authors declare that no competing interests exist.
  4. Sato Takafumi

    Graduate School of Agricultural and Life Sciences, University of Tokyo, Tokyo, Japan
    Competing interests
    The authors declare that no competing interests exist.
  5. Athanasius FM Marée

    Department of Computational and Systems Biology, John Innes Centre, Norwich, United Kingdom
    For correspondence
    Stan.Maree@jic.ac.uk
    Competing interests
    The authors declare that no competing interests exist.
  6. Toru Fujiwara

    Graduate School of Agricultural and Life Sciences, The University of Tokyo, Tokyo, Japan
    For correspondence
    atorufu@mail.ecc.u-tokyo.ac.jp
    Competing interests
    The authors declare that no competing interests exist.
  7. Verônica A. Grieneisen

    Department of Computational & Systems Biology, John Innes Centre, Norwich, United Kingdom
    For correspondence
    veronica.grieneisen@jic.ac.uk
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0001-6780-8301

Funding

Biotechnology and Biological Sciences Research Council (BB/J004553/1)

  • Athanasius FM Marée
  • Verônica A. Grieneisen

Japan Society for the Promotion of Science (25221202)

  • Toru Fujiwara

Engineering and Physical Sciences Research Council (BB/ L014130/1)

  • Susan Duncan

Japan Society for the Promotion of Science (15J11021)

  • Naoyuki Sotta

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

Reviewing Editor

  1. Maria J Harrison, Boyce Thompson Institute for Plant Research, United States

Version history

  1. Received: March 22, 2017
  2. Accepted: August 13, 2017
  3. Accepted Manuscript published: September 5, 2017 (version 1)
  4. Version of Record published: September 29, 2017 (version 2)

Copyright

© 2017, Sotta 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. Naoyuki Sotta
  2. Susan Duncan
  3. Mayuki Tanaka
  4. Sato Takafumi
  5. Athanasius FM Marée
  6. Toru Fujiwara
  7. Verônica A. Grieneisen
(2017)
Rapid transporter regulation prevents substrate flow traffic jams in boron transport
eLife 6:e27038.
https://doi.org/10.7554/eLife.27038

Share this article

https://doi.org/10.7554/eLife.27038

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