PreprintCited by 3Ion Transport and Channel RegulationPlant nutrient uptake and metabolismNanopore and Nanochannel Transport Studies

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SWEET family transporters act as water conducting carrier proteins in plants

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Selvam, Balaji, Paul, Arnav, Yu, Ya-Chi, Chen, Li-Qing, Shukla, Diwakar·2024·Journal of Chemical Information and Modeling

Preprint — published as 10.1021/acs.jcim.5c00110 · Paper page

Abstract

Dedicated water channels are involved in the facilitated diffusion of water molecules across the cell membrane in plants. Transporter proteins are also known to transport water molecules along with substrates, however the molecular mechanism of water permeation is not well understood in plant transporters. Here, we show plant sugar transporters from the SWEET ( S ugar W ill E ventually be E xported T ransporter) family act as water-conducting carrier proteins via a variety of passive and active mechanisms that allow diffusion of water molecules from one side of the membrane to the other. This study provides a molecular perspective on how plant membrane transporters act as water carrier proteins, a topic that has not been extensively explored in literature. Water permeation in membrane transporters could occur via four distinct mechanisms which form our hypothesis for water transport in SWEETs. These hypothesis are tested using molecular dynamics simulations of the outward-facing, occluded, and inward-facing state of AtSWEET1 to identify the water permeation pathways and the flux associated with them. The hydrophobic gates at the center of the transport tunnel act as a barrier that restricts water permeation. We have performed in silico single and double mutations of the hydrophobic gate residues to examine the changes in the water conductivity. Surprisingly, the double mutant allows the water permeation to the intracellular half of the membrane and forms a continuous water channel. These computational results are validated by experimentally examining the transport of hydrogen peroxide molecules by the AtSWEET family of transporters. We have also shown that the transport of hydrogen peroxide follows the similar mechanism as water transport in AtSWEET1. Finally, we conclude that similar water-conduction states are also present in other SWEET transporters due to the high sequence and structure conservation exhibited by this transporter family.

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Metadata

Authors
Selvam, B., Paul, A., Yu, Y.-C., Chen, L.-Q., & Shukla, D.
Affiliations
University of Illinois Urbana-Champaign (US)
Corresponding author
Shukla, Diwakar
Venue
Journal of Chemical Information and Modeling
Publisher
openRxiv
Published
2024-06-25
Volume
65
Issue
7
Pages
3697-3705
ISSN
1549-9596 (ISSN-L)
OpenAlex
W4408967473
Cited by
3
References
1
Citations by year
2025: 3
FWCI
0.90
Type
journal article
Language
en
Open access
Licence
cc-by-nc-nd
Locations
  • Journal of Chemical Information and Modeling (publishedVersion)
  • bioRxiv (Cold Spring Harbor Laboratory) (acceptedVersion, cc-by-nc-nd)
  • PubMed (publishedVersion)
  • PubMed Central (submittedVersion, cc-by-nc-nd)
Funders
  • National Institute of General Medical Sciences (R35GM142745)
  • Division of Molecular and Cellular Biosciences (MCB1845606)
Topics
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Ion Transport and Channel Regulation
  • Life Sciences › Agricultural and Biological Sciences › Plant Science › Plant nutrient uptake and metabolism
  • Physical Sciences › Engineering › Biomedical Engineering › Nanopore and Nanochannel Transport Studies
Keywords
SWEET transporters, water permeation, plant membrane transporters, sugar transporters, hydrogen peroxide transport, facilitated diffusion, molecular dynamics simulation

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