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Title: Structure of a eukaryotic SWEET transporter in a homotrimeric complex

Abstract

Eukaryotes rely on efficient distribution of energy and carbon skeletons between organs in the form of sugars. Glucose in animals and sucrose in plants serve as the dominant distribution forms. Cellular sugar uptake and release require vesicular and/or plasma membrane transport proteins. Humans and plants use proteins from three superfamilies for sugar translocation: the major facilitator superfamily (MFS), the sodium solute symporter family (SSF; only in the animal kingdom), and SWEETs. SWEETs carry mono- and disaccharides across vacuolar or plasma membranes. Plant SWEETs play key roles in sugar translocation between compartments, cells, and organs, notably in nectar secretion, phloem loading for long distance translocation, pollen nutrition, and seed filling. Plant SWEETs cause pathogen susceptibility possibly by sugar leakage from infected cells. The vacuolar Arabidopsis thaliana AtSWEET2 sequesters sugars in root vacuoles; loss-of-function mutants show increased susceptibility to Pythium infection. In this paper, we show that its orthologue, the vacuolar glucose transporter OsSWEET2b from rice (Oryza sativa), consists of an asymmetrical pair of triple-helix bundles, connected by an inversion linker transmembrane helix (TM4) to create the translocation pathway. Structural and biochemical analyses show OsSWEET2b in an apparent inward (cytosolic) open state forming homomeric trimers. TM4 tightly interacts with the first triple-helixmore » bundle within a protomer and mediates key contacts among protomers. Structure-guided mutagenesis of the close paralogue SWEET1 from Arabidopsis identified key residues in substrate translocation and protomer crosstalk. Finally, insights into the structure–function relationship of SWEETs are valuable for understanding the transport mechanism of eukaryotic SWEETs and may be useful for engineering sugar flux.« less

Authors:
 [1];  [2];  [3];  [2];  [2];  [1];  [4];  [2];  [1]
  1. Stanford Univ., CA (United States). School of Medicine. Dept. of Molecular and Cellular Physiology
  2. Carnegie Inst. of Science, Stanford, CA (United States). Dept. of Plant Biology
  3. Stanford Univ., CA (United States). School of Medicine. Dept. of Molecular and Cellular Physiology; Sichuan Univ., Chengdu (China). College of Life Sciences. Key Lab. of Bio-Resource and Eco-Environment of Ministry of Education. Center of Growth, Metabolism and Aging
  4. Argonne National Lab. (ANL), Argonne, IL (United States). NE-CAT. Dept. of Chemistry and Chemical Biology
Publication Date:
Research Org.:
Stanford Univ., CA (United States); Carnegie Inst. of Science, Stanford, CA (United States)
Sponsoring Org.:
USDOE Office of Science (SC), Basic Energy Sciences (BES) (SC-22); National Science Foundation (NSF); National Inst. of Health (NIH) (United States); Stanford Univ. (United States); Harold and Leila Y. Mathers Charitable Foundation (United States); Alfred P. Sloan Foundation (United States); National Natural Science Foundation of China (NNSFC)
Contributing Org.:
Sichuan Univ., Chengdu (China); Argonne National Lab. (ANL), Argonne, IL (United States)
OSTI Identifier:
1226370
Grant/Contract Number:  
FG02-04ER15542; AC02-06CH11357; IOS-1258018; 1401855; P41 GM103403; 31300618
Resource Type:
Accepted Manuscript
Journal Name:
Nature (London)
Additional Journal Information:
Journal Name: Nature (London); Journal Volume: 527; Journal Issue: 7577; Journal ID: ISSN 0028-0836
Publisher:
Nature Publishing Group
Country of Publication:
United States
Language:
ENGLISH
Subject:
59 BASIC BIOLOGICAL SCIENCES; X-ray crystallography; Transporters

Citation Formats

Tao, Yuyong, Cheung, Lily S., Li, Shuo, Eom, Joon-Seob, Chen, Li-Qing, Xu, Yan, Perry, Kay, Frommer, Wolf B., and Feng, Liang. Structure of a eukaryotic SWEET transporter in a homotrimeric complex. United States: N. p., 2015. Web. doi:10.1038/nature15391.
Tao, Yuyong, Cheung, Lily S., Li, Shuo, Eom, Joon-Seob, Chen, Li-Qing, Xu, Yan, Perry, Kay, Frommer, Wolf B., & Feng, Liang. Structure of a eukaryotic SWEET transporter in a homotrimeric complex. United States. doi:10.1038/nature15391.
Tao, Yuyong, Cheung, Lily S., Li, Shuo, Eom, Joon-Seob, Chen, Li-Qing, Xu, Yan, Perry, Kay, Frommer, Wolf B., and Feng, Liang. Mon . "Structure of a eukaryotic SWEET transporter in a homotrimeric complex". United States. doi:10.1038/nature15391. https://www.osti.gov/servlets/purl/1226370.
@article{osti_1226370,
title = {Structure of a eukaryotic SWEET transporter in a homotrimeric complex},
author = {Tao, Yuyong and Cheung, Lily S. and Li, Shuo and Eom, Joon-Seob and Chen, Li-Qing and Xu, Yan and Perry, Kay and Frommer, Wolf B. and Feng, Liang},
abstractNote = {Eukaryotes rely on efficient distribution of energy and carbon skeletons between organs in the form of sugars. Glucose in animals and sucrose in plants serve as the dominant distribution forms. Cellular sugar uptake and release require vesicular and/or plasma membrane transport proteins. Humans and plants use proteins from three superfamilies for sugar translocation: the major facilitator superfamily (MFS), the sodium solute symporter family (SSF; only in the animal kingdom), and SWEETs. SWEETs carry mono- and disaccharides across vacuolar or plasma membranes. Plant SWEETs play key roles in sugar translocation between compartments, cells, and organs, notably in nectar secretion, phloem loading for long distance translocation, pollen nutrition, and seed filling. Plant SWEETs cause pathogen susceptibility possibly by sugar leakage from infected cells. The vacuolar Arabidopsis thaliana AtSWEET2 sequesters sugars in root vacuoles; loss-of-function mutants show increased susceptibility to Pythium infection. In this paper, we show that its orthologue, the vacuolar glucose transporter OsSWEET2b from rice (Oryza sativa), consists of an asymmetrical pair of triple-helix bundles, connected by an inversion linker transmembrane helix (TM4) to create the translocation pathway. Structural and biochemical analyses show OsSWEET2b in an apparent inward (cytosolic) open state forming homomeric trimers. TM4 tightly interacts with the first triple-helix bundle within a protomer and mediates key contacts among protomers. Structure-guided mutagenesis of the close paralogue SWEET1 from Arabidopsis identified key residues in substrate translocation and protomer crosstalk. Finally, insights into the structure–function relationship of SWEETs are valuable for understanding the transport mechanism of eukaryotic SWEETs and may be useful for engineering sugar flux.},
doi = {10.1038/nature15391},
journal = {Nature (London)},
number = 7577,
volume = 527,
place = {United States},
year = {2015},
month = {10}
}

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