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SWEET family transporters act as water conducting carrier proteins in plants
Open accessPreprint — 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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Highly accurate protein structure prediction with AlphaFold
Jumper, J., Evans, R., Pritzel, A., Green, T., Figurnov, M., Ronneberger, O., Tunyasuvunakool, K., Bates, R., Žídek, A., Potapenko, A., et al. (2021) · Nature · doi:10.1038/s41586-021-03819-2 · Cited by 43,764
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Research works printed but not linked: 60
- Verkman, A. Aquaporins. Current Biology 2013, 23, R 52–R55. · DOI
- 10.1146/annurev.arplant.59.032607.092734 · DOI
- 10.1104/pp.113.233791 · DOI
- 2024, Functional regulation of aquaporin dynamics by lipid bilayer composition, Nature Communications, 15, 1848, 10.1038/s41467-024-46027-y · DOI · Paper page
- 2014, How does water pass through a sugar transporter?, Biophysical Journal, 106, 1229, 10.1016/j.bpj.2014.02.003 · DOI
- 10.1021/bi101454f · DOI
- Huang, B. ; Wang, H. ; Yang, B . Water transport mediated by other membrane proteins. Aquaporins 2017, 251–261. · DOI
- 10.1073/pnas.93.23.13367 · DOI
- 10.1073/pnas.1613744113 · DOI
- 1996, Sodium-glucose cotransporters display sodium-and phlorizin-dependent water permeability, American Journal of Physiology-Cell Physiology, 271, C1774, 10.1152/ajpcell.1996.271.5.C1774 · DOI
- 10.1074/jbc.M115.706986 · DOI
- 2021, Multiple interactions of glucose with the extra-membranous loops of GLUT1 aid transport, Journal of Chemical Information and Modeling, 61, 3559, 10.1021/acs.jcim.1c00310 · DOI
- 10.1113/jphysiol.2005.093526 · DOI
- 10.1016/S0014-4835(02)00329-9 · DOI
- 10.1016/j.bpj.2012.07.044 · DOI
- 10.1073/pnas.1218986110 · DOI
- 10.1038/nature15391 · DOI
- 10.1038/nature09606 · DOI
- 2022, When SWEETs Turn Tweens: Updates and Perspectives, Annual Review of Plant Biology, 73, 379, 10.1146/annurev-arplant-070621-093907 · DOI
- 2019, Molecular basis of the glucose transport mechanism in plants, ACS central science, 5, 1085, 10.1021/acscentsci.9b00252 · DOI
- 10.1101/2022.10.12.511964 · DOI
- 10.1101/2024.06.12.598708 · DOI
- 2021, Impact of Increased Membrane Realism on Conformational Sampling of Proteins, Journal of Chemical Theory and Computation, 17, 5342, 10.1021/acs.jctc.1c00276 · DOI
- 10.1016/j.cell.2017.03.010 · DOI
- 2019, Distinct substrate transport mechanism identified in homologous sugar transporters, The Journal of Physical Chemistry B, 123, 8411, 10.1021/acs.jpcb.9b08257 · DOI
- Chan, M. C. ; Shukla, D . Markov state modeling of membrane transport proteins. Journal of Structural Biology 2021, 213, 107800. · DOI
- 10.1021/jacs.7b12191 · DOI
- Nóe, F. ; Rosta, E. Markov Models of Molecular Kinetics. The Journal of Chemical Physics 2019, 151, 190401. · DOI
- 2021, Markov State Models to Study the Functional Dynamics of Proteins in the Wake of Machine Learning, JACS Au, 1, 1330, 10.1021/jacsau.1c00254 · DOI
- 10.1016/j.ymeth.2010.06.002 · DOI · Paper page
- 10.1021/ar5002999 · DOI
- 10.1073/pnas.87.8.3244 · DOI
- 10.1007/s00232-009-9216-y · DOI
- 2002, Conransporters as molecular water pumps, International review of cytology, 215, 259, 10.1016/S0074-7696(02)15012-1 · DOI
- 2012, Transport of water against its concentration gradient: fact or fiction?, Wiley Interdisciplinary Reviews: Membrane Transport and Signaling, 1, 373
- 2016, Comparative protein structure modeling using MODELLER, Current protocols in bioinformatics, 54, 5
- Lee, J. ; Cheng, X. ; Jo, S. ; MacKerell, A. D. ; Klauda, J. B. ; Im, W . CHARMM-GUI input generator for NAMD, GROMACS, AMBER, OpenMM, and CHARMM/OpenMM simulations using the CHARM M36 additive force field. Biophysical journal 2016, 110, 641a. · DOI
- 10.1021/acs.jctc.5b00255 · DOI
- 10.1002/1096-987X(20010415)22:5<501::AID-JCC1021>3.0.CO;2-V · DOI
- 10.1063/1.470117 · DOI
- 2013, PTRAJ and CPPTRAJ: software for processing and analysis of molecular dynamics trajectory data, Journal of chemical theory and computation, 9, 3084, 10.1021/ct400341p · DOI
- 10.1002/jcc.25382 · DOI
- 10.1016/j.bpj.2015.08.015 · DOI
- 10.1016/0263-7855(96)00018-5 · DOI · Paper page
- 10.1016/S0263-7855(97)00009-X · DOI
- 2022, Hexose transporter SWEET5 confers galactose sensitivity to Arabidopsis pollen germination via a galactokinase, Plant physiology, 189, 388, 10.1093/plphys/kiac068 · DOI
- 10.1038/nature13670 · DOI
- 2015, Structural basis for the facilitative diffusion mechanism by SemiSWEET transporter, Nature communications, 6, 6112, 10.1038/ncomms7112 · DOI
- 2021, Phosphorylation of SWEET sucrose transporters regulates plant root:shoot ratio under drought, Nature Plants, 8, 68, 10.1038/s41477-021-01040-7 · DOI
- 2020, SLC6 transporter oligomerization, Journal of Neurochemistry, 157, 919
- 10.1042/BST20160217 · DOI
- 10.1093/jxb/ern240 · DOI · Paper page
- Tang, R.-J. ; Luan, M. ; Wang, C. ; Lhamo, D. ; Yang, Y. ; Zhao, F.-G. ; Lan, W.-Z. ; Fu, A.-G. ; Luan, S . Plant Membrane Transport Research in the Post-genomic Era. Plant Communications 2020, 1, 100013. · DOI
- 2022, Structural Rearrangement of the Serotonin Transporter Intracellular Gate Induced by Thr276 Phosphorylation, ACS Chemical Neuroscience, 13, 933, 10.1021/acschemneuro.1c00714 · DOI · Paper page
- 10.1101/2022.10.17.512638 · DOI
- 2022, Thirty years of molecular dynamics simulations on posttranslational modifications of proteins, Physical Chemistry Chemical Physics, 24, 26371, 10.1039/D2CP02883B · DOI
- 10.1073/pnas.1311244110 · DOI
- 2020, Structural Consequences of Multisite Phosphorylation in the BAK1 Kinase Domain, Biophysical Journal, 118, 698, 10.1016/j.bpj.2019.12.026 · DOI
- Kuanyshev, N. ; Deewan, A. ; Jagtap, S. S. ; Liu, J. ; Selvam, B. ; Chen, L. ; Shukla, D. ; Rao, C. V. ; Jin, Y . Identification and analysis of sugar transporters capable of co-transporting glucose and xylose simultaneously. Biotechnology Journal 2021, 16, 2100238. · DOI
- 2023, Exploring the Substrate Specificity of a Sugar Transporter with Biosensors and Cheminformatics, ACS Synthetic Biology, 12, 565, 10.1021/acssynbio.2c00571 · DOI
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)
- PMC
- PMC11230166
- OpenAlex
- W4408967473
- Cited by
- 3
- References
- 1
- Citations by year
- 2025: 3
- FWCI
- 0.90
- Type
- journal article
- Language
- en
- Open access
- green
- doi.org
- 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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