Rapid transporter regulation prevents substrate flow traffic jams in boron transport

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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.

Data availability

The following data sets were generated

1. Grieneisen et al.
(2017) Data from: Rapid transporter regulation prevents substrate flow traffic jams in boron transport
Available at Dryad Digital Repository under a CC0 Public Domain Dedication.

https://doi.org/10.5061/dryad.9pq6k

Article and author information

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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.

"This ORCID iD identifies the author of this article:" 0000-0001-5558-5155
Susan Duncan

Department of Computational and Systems Biology, John Innes Centre, Norwich, United Kingdom

Competing interests
The authors declare that no competing interests exist.

"This ORCID iD identifies the author of this article:" 0000-0001-9581-1145
Mayuki Tanaka

Graduate School of Agricultural and Life Sciences, University of Tokyo, Tokyo, Japan

Competing interests
The authors declare that no competing interests exist.
Sato Takafumi

Graduate School of Agricultural and Life Sciences, University of Tokyo, Tokyo, Japan

Competing interests
The authors declare that no competing interests exist.
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.
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.
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.

"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.

Copyright

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.