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Journal of Integrative Agriculture  2022, Vol. 21 Issue (10): 2848-2864    DOI: 10.1016/j.jia.2022.07.034
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Genome-wide identification, expression and functional analysis of sugar transporters in sorghum (Sorghum bicolor L.) 

XIAO Qian-lin1*, LI Zhen1*, WANG Ya-yun2, HOU Xian-bin3, WEI Xi-mei1, ZHAO Xiao1, HUANG Lei1, GUO Yan-jun4, LIU Zhi-zhai1

1 College of Agronomy and Biotechnology, Southwest University, Chongqing 400715, P.R.China

2 State Key Laboratory of Crop Gene Exploration and Utilization in Southwest China, Sichuan Agricultural University, Chengdu 611130, P.R.China

3 College of Agriculture and Food Engineering, Baise University, Baise 533000, P.R.China

4 College of Animal Science and Technology, Southwest University, Chongqing 400715, P.R.China

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摘要  糖转运蛋白在植物渗透调节、信号途径以及植物的生长发育过程中具有重要的作用。然而,目前高粱糖转运蛋白(Sorghum Sugar Transporter,SST)的功能研究却相对较少。本研究通过BLASTP在全基因组鉴定得到98个SST。分析结果显示,这98个SST被划分成3个家族,其中6个被划分为蔗糖转运蛋白家族(sucrose transporters,SUT),23个被划分为SWEET蛋白家族(sugars will eventually be exported transporters,SWEET),69个被划分为单糖转运蛋白家族(monosaccharide transporters,MST)。并且这69个高粱MST可进一步分为7个亚家族,其中24个蛋白属于sugar transporter protein(STP),23个属于polyol/monosaccharide transporter(PLT),2个属于vacuolar glucose transporter(VGT),4个属于inositol transporter(INT),3个属于plastidic glucose transporter/suppressor of G protein beta1(pGlcT/SBG1),5个属于tonoplastic monosaccharide transporter(TMT),8个属于early response to dehydration (ERD6)-like(ERD)。研究结果还发现,SST的编码基因在染色体上随机分布,但却呈现成簇分布的特性,SWEET、ERD、STP和PLT的27个编码基因聚集形成8个串联重复区,其中22个编码基因形成了11对旁系同源基因,占SST编码基因的22.4%。此外,SST家族具有相似的保守结构域,但其保守基序与跨膜结构域(TMH)的特征却有所不同。进一步的分析结果显示,SST编码基因表现出明显的组织特异性;有7个SST主要分布在细胞膜以及膜细胞器上;而选取的14个SST则均能在酵母中转运不同类型的单糖。通过以上研究,我们揭示了SST的序列特征和蛋白的初步功能,研究结果为解析SST在高粱的糖转运及糖信号通路中的作用奠定了基础。

Abstract  

Sugar transporters are essential for osmotic process regulation, various signaling pathways and plant growth and development.  Currently, few studies are available on the function of sugar transporters in sorghum (Sorghum bicolor L.).  In this study, we performed a genome-wide survey of sugar transporters in sorghum.  In total, 98 sorghum sugar transporters (SSTs) were identified via BLASTP.  These SSTs were classified into three families based on the phylogenetic and conserved domain analysis, including six sucrose transporters (SUTs), 23 sugars will eventually be exported transporters (SWEETs), and 69 monosaccharide transporters (MSTs).  The sorghum MSTs were further divided into seven subfamilies, including 24 STPs, 23 PLTs, two VGTs, four INTs, three pGlcT/SBG1s, five TMTs, and eight ERDs.  Chromosomal localization of the SST genes showed that they were randomly distributed on 10 chromosomes, and substantial clustering was evident on the specific chromosomes.  Twenty-seven SST genes from the families of SWEET, ERD, STP, and PLT were found to cluster in eight tandem repeat event regions.  In total, 22 SSTs comprising 11 paralogous pairs and accounting for 22.4% of all the genes were located on the duplicated blocks.  The different subfamilies of SST proteins possessed the same conserved domain, but there were some differences in features of the motif and transmembrane helices (TMH).  The publicly-accessible RNA-sequencing data and real-time PCR revealed that the SST genes exhibited distinctive tissue specific patterns.  Functional studies showed that seven SSTs were mainly located on the cell membrane and membrane organelles, and 14 of the SSTs could transport different types of monosaccharides in yeast.  These findings will help us to further elucidate their roles in the sorghum sugar transport and sugar signaling pathways.

Keywords:  sorghum (Sorghum bicolor L.)        sugar transporter        SUT        SWEET        MST        phylogenetic analysis  
Received: 10 March 2021   Accepted: 07 May 2021
Fund: This work was supported by the National Natural Science Foundation of China (32001607) and Fundamental Research Funds for the Central Universities of Southwest University (No: SWU118087).
About author:  Correspondence XIAO Qian-lin, Tel: +86-23-68251410, E-mail: xiaoql1853@swu.edu.cn; LIU Zhi-zhai, Tel: +86-23-68251410, E-mail: liu003@swu.edu.cn * These authors contributed equally to this study.

Cite this article: 

XIAO Qian-lin, LI Zhen, WANG Ya-yun, HOU Xian-bin, WEI Xi-mei, ZHAO Xiao, HUANG Lei, GUO Yan-jun, LIU Zhi-zhai. 2022. Genome-wide identification, expression and functional analysis of sugar transporters in sorghum (Sorghum bicolor L.) . Journal of Integrative Agriculture, 21(10): 2848-2864.

Aoki N, Scofield G N, Wang X D, Patrick J W, Offler C E, Furbank R T. 2004. Expression and localisation analysis of the wheat sucrose transporter TaSUT1 in vegetative tissues. Planta, 219, 176–184.
Aoki N, Whitfeld P, Hoeren F, Scofield G, Newell K, Patrick J, Offler C, Clarke B, Rahman S, Furbank R T. 2002. Three sucrose transporter genes are expressed in the developing grain of hexaploid wheat. Plant Molecular Biology, 50, 453–462.
Baker R F, Leach K A, Boyer N R, Swyers M J, Benitez-Alfonso Y, Skopelitis T, Luo A, Sylvester A, Jackson D, Braun D M. 2016. Sucrose transporter ZmSut1 expression and localization uncover new insights into sucrose phloem loading. Plant Physiology, 172, 1876–1898.
Baud S, Wuillème S, Lemoine R, Kronenberger J, Caboche M, Lepiniec L C, Rochat C. 2005. The AtSUC5 sucrose transporter specifically expressed in the endosperm is involved in early seed development in Arabidopsis. Plant Journal, 43, 824–836.
Bihmidine S, Baker R F, Hoffner C, Braun D M. 2015. Sucrose accumulation in sweet sorghum stems occurs by apoplasmic phloem unloading and does not involve differential Sucrose transporter expression. BMC Plant Biology, 15, 1–22.
Bihmidine S, Julius B T, Dweikat I, Braun D M. 2016. Tonoplast sugar transporters (SbTSTs) putatively control sucrose accumulation in sweet sorghum stems. Plant Signaling & Behavior, 11, doi: 10.1080/15592324.2015.1117721.
Boorer K J, Loo D D, Wright E M. 1994. Steady-state and presteady-state kinetics of the H+/hexose cotransporter (STP1) from Arabidopsis thaliana expressed in Xenopus oocytes. Journal of Biological Chemistry, 269, 20417–20424.
Braun D M, Slewinski T L. 2009. Genetic control of carbon partitioning in grasses: Roles of sucrose transporters and tie-dyed loci in phloem loading. Plant Physiology, 149, 71–81.
Braun D M, Wang L, Ruan Y L. 2014. Understanding and manipulating sucrose phloem loading, unloading, metabolism, and signalling to enhance crop yield and food security. Journal of Experimental Botany, 65, 1713–1735.
Büttner M. 2007. The monosaccharide transporter(-like) gene family in Arabidopsis. FEBS Letters, 581, 2318–2324.
Büttner M. 2010. The Arabidopsis sugar transporter (AtSTP) family: An update. Plant Biology, 12, 35–41.
Büttner M, Sauer N. 2000. Monosaccharide transporters in plants: Structure, function and physiology. Biochimica et Biophysica Acta (BBA)-Biomembranes, 1465, 263–274.
Carpaneto A, Geiger D, Bamberg E, Sauer N, Fromm J, Hedrich R. 2005. Phloem-localized, proton-coupled sucrose carrier ZmSUT1 mediates sucrose efflux under the control of the sucrose gradient and the proton motive force. Journal of Biological Chemistry, 280, 21437–21443.
Chandran D, Reinders A, Ward J M. 2003. Substrate specificity of the Arabidopsis thaliana sucrose transporter AtSUC2. Journal of Biological Chemistry, 278, 44320–44325.
Chen C, Chen H, Zhang Y, Thomas H R, Frank M H, He Y, Xia R. 2020. TBtools - An integrative toolkit developed for interactive analyses of big biological data. Molecular Plant, 13, 1194–1202.
Chen H Y, Huh J H, Yu Y C, Ho L H, Chen L Q, Tholl D, Frommer W B, Guo W J. 2015. The Arabidopsis vacuolar sugar transporter SWEET2 limits carbon sequestration from roots and restricts Pythium infection. Plant Journal, 83, 1046–1058.
Chen J, Yi Q, Cao Y, Wei B, Zheng L, Xiao Q, Xie Y, Gu Y, Li Y, Huang H, Wang Y, Hou X, Long T, Zhang J, Liu H, Liu Y, Yu G, Huang Y. 2016. ZmbZIP91 regulates expression of starch synthesis-related genes by binding to ACTCAT elements in their promoters. Journal of Experimental Botany, 67, 1327–1338.
Chen L Q. 2014. SWEET sugar transporters for phloem transport and pathogen nutrition. New Phytologist, 201, 1150–1155.
Chen L Q, Cheung L S, Feng L, Tanner W, Frommer W B. 2015. Transport of sugars. Annual Review of Biochemistry, 84, 865–894.
Chen L Q, Hou B H, Lalonde S, Takanaga H, Hartung M L, Qu X Q, Guo W J, Kim J G, Underwood W, Chaudhuri B, Chermak D, Antony G, White F F, Somerville S C, Mudgett M B, Frommer W B. 2010. Sugar transporters for intercellular exchange and nutrition of pathogens. Nature, 468, 527–532.
Chen L Q, Qu X Q, Hou B H, Sosso D, Osorio S, Fernie A R, Frommer W B. 2012. Sucrose efflux mediated by SWEET proteins as a key step for phloem transport. Science, 335, 207–211.
Davidson R M, Gowda M, Moghe G, Lin H, Vaillancourt B, Shiu S H, Jiang N, Buell C R. 2012. Comparative transcriptomics of three Poaceae species reveals patterns of gene expression evolution. Plant Journal, 71, 492–502.
Diderich J A, Schuurmans M, Van Gaalen M C, Kruckeberg A L, Van Dam K. 2001. Functional analysis of the hexose transporter homologue HXT5 in Saccharomyces cerevisiae. Yeast, 18, 1515–1524.
Divya C, Anke R, Ward J M. 2003. Substrate specificity of the Arabidopsis thaliana sucrose transporter AtSUC2. Journal of Biological Chemistry, 278, 44320–44325.
Feng C Y, Han J X, Han X X, Jiang J. 2015. Genome-wide identification, phylogeny, and expression analysis of the SWEET gene family in tomato. Gene, 573, 261–272.
Guan Y F, Huang X Y, Zhu J, Gao J F, Zhang H X, Yang Z N. 2008. RUPTURED POLLEN GRAIN1, a member of the MtN3/saliva gene family, is crucial for exine pattern formation and cell integrity of microspores in Arabidopsis. Plant Physiology, 147, 852–863.
Guo A Y, Zhu Q H, Chen X, Luo J C. 2007. GSDS: A gene structure display server. Hereditas, 29, 1023–1026.
Guo W J, Nagy R, Chen H Y, Pfrunder S, Yu Y C, Santelia D, Frommer W B, Martinoia E. 2014. SWEET17, a facilitative transporter, mediates fructose transport across the tonoplast of Arabidopsis roots and leaves. Plant Physiology, 164, 777–789.
Hirose T, Imaizumi N, Scofield G N, Furbank R T, Ohsugi R. 1997. cDNA cloning and tissue specific expression of a gene for sucrose transporter from rice (Oryza sativa L.). Plant and Cell Physiology, 38, 1389–1396.
Hu Y F, Li Y P, Zhang J, Liu H, Tian M, Huang Y. 2012. Binding of ABI4 to a CACCG motif mediates the ABA-induced expression of the ZmSSI gene in maize (Zea mays L.) endosperm. Journal of Experimental Botany, 63, 5979–5989.
Ishimaru K, Hirose T, Aoki N, Takahashi S, Ono K, Yamamoto S, Wu J, Saji S, Baba T, Ugaki M, Matsumoto T, Ohsugi R. 2001. Antisense expression of a rice sucrose transporter OsSUT1 in rice (Oryza sativa L.). Plant and Cell Physiology, 42, 1181–1185.
Johnson D A, Hill J P, Thomas M A. 2006. The monosaccharide transporter gene family in land plants is ancient and shows differential subfamily expression and expansion across lineages. BMC Evolutionary Biology, 6, doi: 10.1186/1471-2148-6-64.
Johnson D A, Thomas M A. 2007. The monosaccharide transporter gene family in Arabidopsis and rice: a history of duplications, adaptive evolution, and functional divergence. Molecular Biology & Evolution, 24, 2412–2423.
Julius B T, Leach K A, Tran T M, Mertz R A, Braun D M. 2017. Sugar transporters in plants: New insights and discoveries. Plant and Cell Physiology, 58, 1442–1460.
Klepek Y S, Geiger D, Stadler R, Klebl F, Landouar-Arsivaud L, Lemoine R, Hedrich R, Sauer N. 2005. Arabidopsis POLYOL TRANSPORTER5, a new member of the monosaccharide transporter-like superfamily, mediates H+-symport of numerous substrates, including myo-inositol, glycerol, and ribose. Plant Cell, 17, 204–218.
Klepek Y S, Volke M, Kai R K, Wippel K, Hoth S, Hedrich R, Sauer N. 2010. Arabidopsis thaliana POLYOL/MONOSACCHARIDE TRANSPORTERS 1 and 2: Fructose and xylitol/H+ symporters in pollen and young xylem cells. Journal of Experimental Botany, 61, 537–550.
Krzywindski M, Schein J, Birol I, Connors J, Gascoyne R, Horsman D, Hones S J, Marra M A. 2009. Circos: An information aesthetic for comparative genomics. Genome Research, 19, 1639–1645.
Kühn C, Grof C P L. 2010. Sucrose transporters of higher plants. Current Opinion in Plant Biology, 13, 288–298.
Lastdrager J, Hanson J, Smeekens S. 2014. Sugar signals and the control of plant growth and development. Journal of Experimental Botany, 65, 799–807.
Lemonnier P, Gaillard C, Veillet F, Verveke J, Lemoine R, Coutos-Thevenot P, Camera S L. 2014. Expression of Arabidopsis sugar transport protein STP13 differentially affects glucose transport activity and basal resistance to Botrytis cinerea. Plant Molecular Biology, 85, 473–484
Li Y, Li L L, Fan R C, Peng C C, Sun H L, Zhu S Y, Wang X F, Zhang L Y, Zhang D P. 2012. Arabidopsis sucrose transporter SUT4 interacts with cytochrome b5–2 to regulate seed germination in response to sucrose and glucose. Molecular Plant, 5, 1029–1041.
Lynch M, Conery J S. 2000. The evolutionary fate and consequences of duplicate genes. Science, 290, 1151–1155.
Ma L, Zhang D, Miao Q, Yang J, Xuan Y, Hu Y. 2017. Essential role of sugar transporter OsSWEET11 during the early stage of rice grain filling. Plant and Cell Physiology, 58, 863–873.
Makita Y, Shimada S, Kawashima M, Kondoukuriyama T, Toyoda T, Matsui M. 2015. MOROKOSHI: transcriptome database in Sorghum bicolor. Plant and Cell Physiology, 56, doi: 10.1093/pcp/pcu187.
Matsukura C, Saitoh T, Hirose T, Ohsugi R, Perata P, Yamaguchi J. 2000. Sugar uptake and transport in rice embryo. Expression of companion cell-specific sucrose transporter (OsSUT1) induced by sugar and light. Plant Physiology, 124, 85–93.
Meyer S, Melzer M, Truernit E, Hümmer C, Besenbeck R, Stadler R, Sauer N. 2001. AtSUC3, a gene encoding a new Arabidopsis sucrose transporter, is expressed in cells adjacent to the vascular tissue and in a carpel cell layer. Plant Journal, 24, 869–882.
Milne R J, Byrt C S, Patrick J W, Grof C P L. 2013. Are sucrose transporter expression profiles linked with patterns of biomass partitioning in Sorghum phenotypes? Frontiers in Plant Science, 4, doi: 10.3389/fpls.2013.00223.
Milne R J, Perroux J M, Rae A L, Reinders A, Ward J M, Offler C E, Patrick J W, Grof C P L. 2017. Sucrose transporter localization and function in phloem unloading in developing stems. Plant Physiology, 173, 1330–1341.
Mizuno H, Kasuga S, Kawahigashi H. 2016. The sorghum SWEET gene family: stem sucrose accumulation as revealed through transcriptome profiling. Biotechnology for Biofuels, 9, doi: 10.1186/s13068-016-0546-6.
De Moliner F, Knox K, Reinders A, Ward J M, McLaughlin P J, Oparka K, Vendrell M. 2018. Probing binding specificity of the sucrose transporter AtSUC2 with fluorescent coumarin glucosides. Journal of Experimental Botany, 69, 2473–2482.
Paterson A, Bowers J, Bruggmann R, Dubchak I, Grimwood J, Gundlach H, Haberer G, Hellsten U, Mitros T, Poliakov A, Schmutz J, Spannagl M, Tang H, Wang X, Wicker T, Bharti A, Chapman J, Feltus F, Gowik U, Grigoriev I, et al. 2009. The Sorghum bicolor genome and the diversification of grasses. Nature, 457, 551–556.
Patil G, Valliyodan B, Deshmukh R, Prince S, Nicander B, Zhao M, Sonah H, Song L, Lin L, Chaudhary J, Liu Y, Joshi T, Xu D, Nguyen H T. 2015. Soybean (Glycine max) SWEET gene family: insights through comparative genomics, transcriptome profiling and whole genome re-sequence analysis. BMC Genomics, 16, doi: 10.1186/s12864-015-1730-y.
Pommerrenig B, Popko J, Heilmann M, Schulmeister S, Dietel K, Schmitt B, Stadler R, Feussner I, Sauer N. 2013. SUCROSE TRANSPORTER 5 supplies Arabidopsis embryos with biotin and affects triacylglycerol accumulation. Plant Journal, 73, 392–404.
Quirino B F, Normanly J, Amasino R M. 1999. Diverse range of gene activity during Arabidopsis thaliana leaf senescence includes pathogen-independent induction of defense-related genes. Plant Molecular Biology, 40, 267–278.
Riesmeier J W, Hirner B, Frommer W B. 1993. Potato sucrose transporter expression in minor veins indicates a role in phloem loading. Plant Cell, 5, 1591–1598.
Riesmeier J W, Willmitzer L, Frommer W B. 1992. Isolation and characterization of a sucrose carrier cDNA from spinach by functional expression in yeast. EMBO Journal, 11, 4705–4713.
Ruan Y L. 2014. Sucrose metabolism: gateway to diverse carbon use and sugar signaling. Annual Review of Plant Biology, 65, 33–67.
Sauer N, Friedländer K, Grämlwicke U. 1990. Primary structure, genomic organization and heterologous expression of a glucose transporter from Arabidopsis thaliana. EMBO Journal, 9, 3045–3050.
Schneider S, Schneidereit A S, Konrad K R, Hajirezaei M R, Gramann M, Hedrich R, Sauer N. 2006. Arabidopsis INOSITOL TRANSPORTER4 mediates high-affinity H+ symport of myoinositol across the plasma membrane. Plant Physiology, 141, 565–577.
Scofield G N, Hirose T, Aoki N, Furbank R T. 2007. Involvement of the sucrose transporter, OsSUT1, in the long-distance pathway for assimilate transport in rice. Journal of Experimental Botany, 58, 3155–3169.
Shiratake K. 2007. Genetics of sucrose transporter in plants. Genes, Genomes and Genomics, 1, 73–80.
Sivitz A B, Reinders A, Johnson M E, Krentz A D, Grof C P L, Perroux J M, Ward J M. 2006. Arabidopsis sucrose transporter AtSUC9. High-affinity transport activity, intragenic control of expression, and early flowering mutant phenotype. Plant Physiology, 143, 188–198.
Sivitz A B, Reinders A, Ward J M. 2008. Arabidopsis sucrose transporter AtSUC1 is important for pollen germination and sucrose-induced anthocyanin accumulation. Plant Physiology, 147, 92–100.
Slewinski T L. 2011. Diverse functional roles of monosaccharide transporters and their homologs in vascular plants: A physiological perspective. Molecular Plant, 4, 641–662.
Slewinski T L, Garg A, Johal G S, Braun D M. 2010. Maize SUT1 functions in phloem loading. Plant Signaling & Behavior, 5, 687–690.
Slewinski T L, Meeley R, Braun D M. 2009. Sucrose transporter1 functions in phloem loading in maize leaves. Journal of Experimental Botany, 60, 881–892.
Sosso D, Luo D, Li Q B, Sasse J, Yang J, Gendrot G, Suzuki M, Koch K E, McCarty D R, Chourey P S, Rogowsky P M, Ross-Ibarra J, Yang B, Frommer W B. 2015. Seed filling in domesticated maize and rice depends on SWEET-mediated hexose transport. Nature Genetics, 47, 1489–1493.
Sun M X, Huang X Y, Yang J, Guan Y F, Yang Z N. 2013. Arabidopsis RPG1 is important for primexine deposition and functions redundantly with RPG2 for plant fertility at the late reproductive stage. Plant Reproduction, 26, 83–91.
Tamura K, Peterson D, Peterson N, Stecher G, Nei M, Kumar S. 2011. MEGA5: Molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Molecular Biology & Evolution, 28, 2731–2739.
Tian L, Liu L, Yin Y, Huang M, Chen Y, Xu X, Wu P, Li M, Wu G, Jiang H, Chen Y. 2017. Heterogeneity in the expression and subcellular localization of POLYOL/MONOSACCHARIDE TRANSPORTER genes in Lotus japonicus. PLoS ONE, 12, e0185269.
Wang Y, Tang H, Debarry J D, Tan X, Li J, Wang X, Lee T H, Jin H, Marler B, Guo H, Kissinger J C, Paterson A H. 2012. MCScanX: A toolkit for detection and evolutionary analysis of gene synteny and collinearity. Nucleic Acids Research, 40, e49.
Weise A, Barker L, Kühn C, Lalonde S, Buschmann H, Frommer W B, Ward J M. 2000. A new subfamily of sucrose transporters, SUT4, with low affinity/high capacity localized in enucleate sieve elements of plants. Plant Cell, 12, 1345–1355.
Wormit A, Trentmann O, Feifer I, Lohr C, Tjaden J, Meyer S, Schmidt U, Martinoia E, Neuhaus H E. 2006. Molecular identification and physiological characterization of a novel monosaccharide transporter from Arabidopsis involved in vacuolar sugar transport. Plant Cell, 18, 3476–3490.
Wu F H, Shen S C, Lee L Y, Lee S H, Chan M T, Lin C S. 2009. Tape-Arabidopsis Sandwich - A simpler Arabidopsis protoplast isolation method. Plant Methods, 5, doi: 10.1186/1746-4811-5-16.
Xuan Y H, Hu Y B, Chen L Q, Sosso D, Ducat D C, Hou B H, Frommer W B. 2013. Functional role of oligomerization for bacterial and plant SWEET sugar transporter family. Proceedings of the National Academy of Sciences of the United States of America, 110, E3685–E3694.
Yang B, Sugio A, White F F. 2006. Os8N3 is a host disease-susceptibility gene for bacterial blight of rice. Proceedings of the National Academy of Sciences of the United States of America, 103, 10503–10508.
Yu X, Wang X, Wang C, Chen X, Qu Z, Yu X, Han Q, Zhao J, Guo J, Huang L, Kang Z. 2010. Wheat defense genes in fungal (Puccinia striiformis) infection. Functional & Integrative Genomics, 10, 227–239.
Yuan M, Wang S. 2013. Rice MtN3/saliva/SWEET family genes and their homologues in cellular organisms. Molecular Plant, 6, 665–674.
Yuan M, Zhao J, Huang R, Li X, Xiao J, Wang S. 2014. Rice MtN3/saliva/SWEET gene family: Evolution, expression profiling, and sugar transport. Journal of Integrative Plant Biology, 56, 559–570.
Zeng L, Yi Y, Tang H, Wang J. 2014. VvpGLT, a grapevine gene encoding for a plastidic localized glucose transporter. In: Zhang T C, Ouyang P, Kaplan S, Skarnes B, eds., Proceedings of the 2012 International Conference on Applied Biotechnology, Lecture Notes in Electrical Engineering. vol., 251. Springer, Berlin, Heidelberg. https://doi.org/10.1007/978–3–642–37925–3_160.

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