Rapid transporter regulation prevents substrate flow traffic jams in boron transport.
Rapid transporter regulation prevents substrate flow traffic jams in boron transport.
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DOI:
10.7554/elife.27038
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发表时间:
2017-09-05
期刊:
影响因子:
7.7
通讯作者:
Grieneisen VA
中科院分区:
文献类型:
--
作者:
Sotta N;Duncan S;Tanaka M;Sato T;Marée AF;Fujiwara T;Grieneisen VA
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. Every multicellular organism, including all plants and animals, faces the challenge of taking up the nutrients it needs and distributing them throughout its body. Plants absorb many nutrients including nitrogen and boron from the soil into their roots, often using tightly controlled processes that require energy to work. Plant roots contain several distinct layers of cells and the nutrients need to cross these layers to reach a channel at the centre of the root known as the xylem, which transports the nutrients to other parts of the plant. Plants need boron to grow. However, high levels of this nutrient are toxic so plants have evolved to change the rate at which they absorb boron to optimize growth in different environments. When there is little boron in the soil, certain transporter proteins move to the surface of root cells to bring boron into the root more effectively. On the other hand, when plants grow in soils with high boron, their root cells have fewer of these transporters on their surfaces to prevent too much boron entering the plant. This regulation of boron uptake appears logical, except for one detail: at any given location, the amount of boron in the soil is relatively stable and changes only very slowly. Why do plants invest energy in responding rapidly to the supply of a nutrient that changes so slowly in nature? Sotta et al. used mathematics and experimental approaches to study boron uptake in a plant known as Arabidopsis. The work reveals that the plants ability to rapidly alter how efficiently boron moves into root cells actually serves to avoid internal “traffic jams” in boron transport. If the numbers of transporter proteins on the surface of root cells changed more slowly, individual cells would occasionally experience high levels of boron that would interfere with the movement of boron further into the root, causing a jam. Furthermore, these ‘peaks’ of boron could damage the individual cells they affect. The findings of Sotta et al. reveal that, by being able to rapidly change the numbers of certain transporter proteins on the surface of root cells, plants can ensure they receive a steady supply of boron. This work suggests that to develop artificial systems that can adapt to changing surroundings, researchers will need to engineer solutions like those found in plants in order to avoid similar traffic jams in the systems. Along with considering how plants interact with their environment, studying how they avoid internal traffic jams in nutrient uptake may help efforts to alter plants, including crops, so that they grow better in harsh environments.