Rapid transporter regulation prevents substrate flow traffic jams in boron transport
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 tran...
| Main Authors: | , , , , , , |
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| Format: | Article |
| Language: | English |
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eLife Sciences Publications Ltd
2017-09-01
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| Series: | eLife |
| Subjects: | |
| Online Access: | https://elifesciences.org/articles/27038 |
| _version_ | 1811236799974998016 |
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| author | Naoyuki Sotta Susan Duncan Mayuki Tanaka Takafumi Sato Athanasius FM Marée Toru Fujiwara Verônica A Grieneisen |
| author_facet | Naoyuki Sotta Susan Duncan Mayuki Tanaka Takafumi Sato Athanasius FM Marée Toru Fujiwara Verônica A Grieneisen |
| author_sort | Naoyuki Sotta |
| collection | DOAJ |
| description | 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 uptake 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. |
| first_indexed | 2024-04-12T12:15:27Z |
| format | Article |
| id | doaj.art-36c678da7a2f4dc38ff0bba16a8c7104 |
| institution | Directory Open Access Journal |
| issn | 2050-084X |
| language | English |
| last_indexed | 2024-04-12T12:15:27Z |
| publishDate | 2017-09-01 |
| publisher | eLife Sciences Publications Ltd |
| record_format | Article |
| series | eLife |
| spelling | doaj.art-36c678da7a2f4dc38ff0bba16a8c71042022-12-22T03:33:27ZengeLife Sciences Publications LtdeLife2050-084X2017-09-01610.7554/eLife.27038Rapid transporter regulation prevents substrate flow traffic jams in boron transportNaoyuki Sotta0https://orcid.org/0000-0001-5558-5155Susan Duncan1https://orcid.org/0000-0001-9581-1145Mayuki Tanaka2Takafumi Sato3Athanasius FM Marée4https://orcid.org/0000-0003-2689-2484Toru Fujiwara5https://orcid.org/0000-0002-5363-6040Verônica A Grieneisen6https://orcid.org/0000-0001-6780-8301Graduate School of Agricultural and Life Sciences, The University of Tokyo, Tokyo, JapanDepartment of Computational and Systems Biology, John Innes Centre, Norwich, United KingdomGraduate School of Agricultural and Life Sciences, The University of Tokyo, Tokyo, JapanGraduate School of Agricultural and Life Sciences, The University of Tokyo, Tokyo, JapanDepartment of Computational and Systems Biology, John Innes Centre, Norwich, United KingdomGraduate School of Agricultural and Life Sciences, The University of Tokyo, Tokyo, JapanDepartment of Computational and Systems Biology, John Innes Centre, Norwich, United KingdomNutrient 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 uptake 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.https://elifesciences.org/articles/27038polar transportboroncell polaritytraffic jamsnutrient uptakeroots |
| spellingShingle | Naoyuki Sotta Susan Duncan Mayuki Tanaka Takafumi Sato Athanasius FM Marée Toru Fujiwara Verônica A Grieneisen Rapid transporter regulation prevents substrate flow traffic jams in boron transport eLife polar transport boron cell polarity traffic jams nutrient uptake roots |
| title | Rapid transporter regulation prevents substrate flow traffic jams in boron transport |
| title_full | Rapid transporter regulation prevents substrate flow traffic jams in boron transport |
| title_fullStr | Rapid transporter regulation prevents substrate flow traffic jams in boron transport |
| title_full_unstemmed | Rapid transporter regulation prevents substrate flow traffic jams in boron transport |
| title_short | Rapid transporter regulation prevents substrate flow traffic jams in boron transport |
| title_sort | rapid transporter regulation prevents substrate flow traffic jams in boron transport |
| topic | polar transport boron cell polarity traffic jams nutrient uptake roots |
| url | https://elifesciences.org/articles/27038 |
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