Molecular Mechanism of Substrate Recognition and Transport by the AtSWEET13 Sugar Transporter

Overview

Journal Proc Natl Acad Sci U S A

Specialty Science

Date 2017 Sep 8

PMID 28878024

Citations 49

Authors

Lei Han

Yongping Zhu

Min Liu

Ye Zhou

Guangyuan Lu

Lan Lan

Xianping Wang

Yongfang Zhao

Xuejun C Zhang

Affiliations

Soon will be listed here.

Abstract

Sugar Will Eventually be Exported Transporters (SWEETs) are recently identified sugar transporters that can discriminate and transport di- or monosaccharides across a membrane following the concentration gradient. SWEETs play key roles in plant biological processes, such as pollen nutrition, nectar secretion, seed filling, and phloem loading. SWEET13 from (AtSWEET13) is an important sucrose transporter in pollen development. Here, we report the 2.8-Å resolution crystal structure of AtSWEET13 in the inward-facing conformation with a substrate analog, 2'-deoxycytidine 5'-monophosphate, bound in the central cavity. In addition, based on the results of an in-cell transport activity assay and single-molecule Förster resonance energy transfer analysis, we suggest a mechanism for substrate selectivity based on the size of the substrate-binding pocket. Furthermore, AtSWEET13 appears to form a higher order structure presumably related to its function.

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References

Xuan Y, Hu Y, Chen L, Sosso D, Ducat D, Hou B . Functional role of oligomerization for bacterial and plant SWEET sugar transporter family. Proc Natl Acad Sci U S A. 2013; 110(39):E3685-94. PMC: 3785766. DOI: 10.1073/pnas.1311244110. View

Gault J, Donlan J, Liko I, Hopper J, Gupta K, Housden N . High-resolution mass spectrometry of small molecules bound to membrane proteins. Nat Methods. 2016; 13(4):333-6. PMC: 4856209. DOI: 10.1038/nmeth.3771. View

Hallworth R, Nichols M . Single molecule imaging approach to membrane protein stoichiometry. Microsc Microanal. 2012; 18(4):771-80. PMC: 3786598. DOI: 10.1017/S1431927612001195. View

Jardetzky O . Simple allosteric model for membrane pumps. Nature. 1966; 211(5052):969-70. DOI: 10.1038/211969a0. View

Hou B, Takanaga H, Grossmann G, Chen L, Qu X, Jones A . Optical sensors for monitoring dynamic changes of intracellular metabolite levels in mammalian cells. Nat Protoc. 2011; 6(11):1818-33. DOI: 10.1038/nprot.2011.392. View

Chen L, Cheung L, Feng L, Tanner W, Frommer W . Transport of sugars. Annu Rev Biochem. 2015; 84:865-94. DOI: 10.1146/annurev-biochem-060614-033904. View

Eom J, Chen L, Sosso D, Julius B, Lin I, Qu X . SWEETs, transporters for intracellular and intercellular sugar translocation. Curr Opin Plant Biol. 2015; 25:53-62. DOI: 10.1016/j.pbi.2015.04.005. View

Terwilliger T, Grosse-Kunstleve R, Afonine P, Moriarty N, Zwart P, Hung L . Iterative model building, structure refinement and density modification with the PHENIX AutoBuild wizard. Acta Crystallogr D Biol Crystallogr. 2007; 64(Pt 1):61-9. PMC: 2394820. DOI: 10.1107/S090744490705024X. View

Kanno Y, Oikawa T, Chiba Y, Ishimaru Y, Shimizu T, Sano N . AtSWEET13 and AtSWEET14 regulate gibberellin-mediated physiological processes. Nat Commun. 2016; 7:13245. PMC: 5095183. DOI: 10.1038/ncomms13245. View

10.

McCoy A, Grosse-Kunstleve R, Adams P, Winn M, Storoni L, Read R . Phaser crystallographic software. J Appl Crystallogr. 2009; 40(Pt 4):658-674. PMC: 2483472. DOI: 10.1107/S0021889807021206. View

11.

Zhao Y, Mao G, Liu M, Zhang L, Wang X, Zhang X . Crystal structure of the E. coli peptide transporter YbgH. Structure. 2014; 22(8):1152-1160. DOI: 10.1016/j.str.2014.06.008. View

12.

Afonine P, Grosse-Kunstleve R, Echols N, Headd J, Moriarty N, Mustyakimov M . Towards automated crystallographic structure refinement with phenix.refine. Acta Crystallogr D Biol Crystallogr. 2012; 68(Pt 4):352-67. PMC: 3322595. DOI: 10.1107/S0907444912001308. View

13.

Lin I, Sosso D, Chen L, Gase K, Kim S, Kessler D . Nectar secretion requires sucrose phosphate synthases and the sugar transporter SWEET9. Nature. 2014; 508(7497):546-9. DOI: 10.1038/nature13082. View

14.

Chen L, Lin I, Qu X, Sosso D, McFarlane H, Londono A . A cascade of sequentially expressed sucrose transporters in the seed coat and endosperm provides nutrition for the Arabidopsis embryo. Plant Cell. 2015; 27(3):607-19. PMC: 4558658. DOI: 10.1105/tpc.114.134585. View

15.

Xu Y, Tao Y, Cheung L, Fan C, Chen L, Xu S . Structures of bacterial homologues of SWEET transporters in two distinct conformations. Nature. 2014; 515(7527):448-452. PMC: 4300204. DOI: 10.1038/nature13670. View

16.

Deng D, Sun P, Yan C, Ke M, Jiang X, Xiong L . Molecular basis of ligand recognition and transport by glucose transporters. Nature. 2015; 526(7573):391-6. DOI: 10.1038/nature14655. View

17.

Chun E, Thompson A, Liu W, Roth C, Griffith M, Katritch V . Fusion partner toolchest for the stabilization and crystallization of G protein-coupled receptors. Structure. 2012; 20(6):967-76. PMC: 3375611. DOI: 10.1016/j.str.2012.04.010. View

18.

Chen L, Hou B, Lalonde S, Takanaga H, Hartung M, Qu X . Sugar transporters for intercellular exchange and nutrition of pathogens. Nature. 2010; 468(7323):527-32. PMC: 3000469. DOI: 10.1038/nature09606. View

19.

Heng J, Zhao Y, Liu M, Liu Y, Fan J, Wang X . Substrate-bound structure of the E. coli multidrug resistance transporter MdfA. Cell Res. 2015; 25(9):1060-73. PMC: 4559816. DOI: 10.1038/cr.2015.94. View

20.

Chen L, Qu X, Hou B, Sosso D, Osorio S, Fernie A . Sucrose efflux mediated by SWEET proteins as a key step for phloem transport. Science. 2011; 335(6065):207-11. DOI: 10.1126/science.1213351. View