|
|
|
|
|
| Genome-wide identification, characterization, and expression analysis of the SWEET gene family in cucumber |
| HU Li-ping1, 2, ZHANG Feng1, SONG Shu-hui1, TANG Xiao-wei1, XU Hui1, LIU Guang-min1, WANG Ya-qin1, HE Hong-ju1, 2 |
1 Beijing Vegetable Research Center, Beijing Academy of Agriculture and Forestry Sciences, Beijing 100097, P.R.China
2 Key Laboratory of Biology and Genetic Improvement of Horticultural Crops (North China), Ministry of Agriculture, Beijing 100097, P.R.China |
|
|
|
|
Abstract SWEETs (sugars will eventually be exported transporters) are a novel class of recently identified sugar transporters that play important roles in diverse physiological processes. However, only a few species of the plant SWEET gene family have been functionally identified. Up till now, there has been no systematic analysis of the SWEET gene family in Cucurbitaceae crops. Here, a genome-wide characterization of this family was conducted in cucumber (Cucumis sativus L.). A total of 17 CsSWEET genes were identified, which are not evenly distributed over the seven cucumber chromosomes. Cucumber SWEET protein sequences possess seven conserved domains and two putative serine phosphorylation sites. The phylogenetic tree of the SWEET genes in cucumber, Arabidopsis thaliana, and Oryza sativa was constructed, and all the SWEET genes were divided into four clades. In addition, a number of putative cis-elements were identified in the promoter regions of these CsSWEET genes: nine types involved in phytohormone responses and eight types involved in stress responses. Moreover, the transcript levels of CsSWEET genes were analyzed in various tissues using quantitative real-time polymerase chain reaction. A majority (70.58%) of the CsSWEET genes were confined to reproductive tissue development. Finally, 18 putative watermelon ClaSWEET genes and 18 melon CmSWEET genes were identified that showed a high degree of similarity with CsSWEET genes. The results from this study provided a basic understanding of the CsSWEET genes and may also facilitate future research to elucidate the function of SWEET genes in cucumber and other Cucurbitaceae crops.
|
|
Received: 25 July 2016
Accepted:
|
| Fund: This research was supported by the National Natural Science Foundation of China (31301792), the Beijing Natural Science Foundation, China (6142010) and the Youth Scientific Research Funds of the Beijing Academy of Agriculture and Forestry Sciences, China (QNJJ201401). |
|
Corresponding Authors:
Correspondence HE Hong-ju, Tel: +86-10-51503068, Fax: +86-10-51505002, E-mail: hehongju@nercv.org
|
| About author: HU Li-ping E-mail: huliping@nercv.org |
Cite this article:
HU Li-ping, ZHANG Feng, SONG Shu-hui, TANG Xiao-wei, XU Hui, LIU Guang-min, WANG Ya-qin, HE Hong-ju .
2017.
Genome-wide identification, characterization, and expression analysis of the SWEET gene family in cucumber. Journal of Integrative Agriculture, 16(07): 1486-1501.
|
| Antony G, Zhou J, Huang S, Li T, Liu B, White F, Yang B. 2010. Rice xa13 recessive resistance to bacterial blight is defeated by induction of the disease susceptibility gene Os-11N3. The Plant Cell, 22, 3864–3876.Ayre B G. 2011. Membrane-transport systems for sucrose in relation to whole-plant carbon partitioning. Molecular Plant, 4, 377–394. Bachmann M, Matile P, Keller F. 1994. Metabolism of the raffinose family oligosaccharides in leaves of Ajuga reptans L: Cold acclimation, translocation, and sink to source transition: Discovery of chain elongation enzyme. Plant Physiology, 105, 1335–1345.Chandran D. 2015. Co-option of developmentally regulated plant SWEET transporters for pathogen nutrition and abiotic stress tolerance. IUBMB Life, 67, 461–471.Chardon F, Bedu M, Calenge F, Klemens P A W, Spinner L, Clement G, Chietera G, Leran S, Ferrand M, Lacombe B, Loudet O, Dinant S, Bellini C, Neuhaus H E, Daniel-Vedele F, Krapp A. 2013. Leaf fructose content is controlled by the vacuolar transporter SWEET17 in Arabidopsis. Current Biology, 23, 697–702.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. The Plant Journal, 83, 1046–1058.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. 2015a. 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, Lin I W, Qu X Q, Sosso D, McFarlane H E, Londono A, Samuels A L, Frommer W B. 2015b. A cascade of sequentially expressed sucrose transporters in the seed coat and endosperm provides nutrition for the Arabidopsis embryo. The Plant Cell, 27, 607–619.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.Cheng J T, Li X, Yao F Z, Shan N, Li Y H, Zhang Z X, Sui X L. 2015. Functional characterization and expression analysis of cucumber (Cucumis sativus L.) hexose transporters, involving carbohydrate partitioning and phloem unloading in sink tissues. Plant Science, 237, 46–56.Chong J, Piron M C, Meyer S, Merdinoglu D, Bertsch C, Mestre P. 2014. The SWEET family of sugar transporters in grapevine: VvSWEET4 is involved in the interaction with Botrytis cinerea. Journal of Experimental Botany, 65, 6589–6601.Chu Z, Yuan M, Yao J, Ge X, Yuan B, Xu C, Li X, Fu B, Li Z, Bennetzen J L, Zhang Q, Wang S. 2006. Promoter mutations of an essential gene for pollen development result in disease resistance in rice. Genes & Development, 20, 1250–1255.Cohn M, Bart R S, Shybut M, Dahlbeck D, Gomez M, Morbitzer R, Hou B H, Frommer W B, Lahaye T, Staskawicz B J. 2014. Xanthomonas axonopodis virulence is promoted by a transcription activator-like effector-mediated induction of a SWEET sugar transporter in cassava. Molecular Plant-Microbe Interactions, 27, 1186–1198.Durand M, Porcheron B, Hennion N, Maurousset L, Lemoine R, Pourtau N. 2016. Water deficit enhances C export to the roots in Arabidopsis thaliana plants with contribution of sucrose transporters in both shoot and roots. Plant Physiology, 170, 1460–1479. Engel M L, Holmes-Davis R, McCormick S. 2005. Green sperm. Identification of male gamete promoters in Arabidopsis. Plant Physiology, 138, 2124–2133.Eom J S, Chen L Q, Sosso D, Julius B T, Lin I W, Qu X Q, Braun D M, Frommer W B. 2015. SWEETs, transporters for intracellular and intercellular sugar translocation. Current Opinion Plant Biology, 25, 53–62.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.Finn R D, Coggill P, Eberhardt R Y, Eddy S R, Mistry J, Mitchell A L, Potter S C, Punta M, Qureshi M, Sangrador-Vegas A, Salazar G A, Tate J, Bateman A. 2016. The Pfam protein families database: Towards a more sustainable future. Nucleic Acids Research, 44, D279–D285.Garcia-Mas J, Benjak A, Sanseverino W, Bourgeois M, Mir G, González V M, Hénaff E, Câmara F, Cozzuto L, Lowy E, Alioto T, Capella-Gutiérrez S, Blanca J, Cañizares J, Ziarsolo P, Gonzalez-Ibeas D, Rodríguez-Moreno L, Droege M, Du L, Alvarez-Tejado M, et al. 2012. The genome of melon (Cucumis melo L.). Proceedings of the National Academy of Sciences of the United States of America, 109, 11872–11877.Ge Y X, Angenent G C, Dahlhaus E, Franken J, Peters J, Wullems G J, Creemers-Molenaar J. 2001. Partial silencing of the NEC1 gene results in early opening of anthers in Petunia hybrida. Molecular Genetics and Genomics, 265, 414–423. Ge Y X, Angenent G C, Wittich P E, Peters J, Franken J, Busscher M, Zhang L M, Dahlhaus E, Kater M M, Wullems G J, Creemers-Molenaar T. 2000. NEC1, a novel gene, highly expressed in nectary tissue of Petunia hybrida. The Plant Journal, 24, 725–734.Gross K C, Pharr D M. 1982. A potential pathway for galactose metabolism in Cucumis sativus L., a stachyose transporting species. Plant Physiology, 69, 117–121.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 S, Zhang J, Sun H, Salse J, Lucas W J, Zhang H, Zheng Y, Mao L, Ren Y, Wang Z, Min J, Guo X, Murat F, Ham B K, Zhang Z, Gao S, Huang M, Xu Y, Zhong S, Bombarely A, et al. 2013. The draft genome of watermelon (Citrullus lanatus) and resequencing of 20 diverse accessions. Nature Genetics, 45, 51–58. 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.Handley L W, Pharr D M, McFeeters R F. 1983. Carbohydrate changes during maturation of cucumber fruit: implications for sugar metabolism and transport. Plant Physiology, 72, 498–502.Hir R, Spinner L, Klemens P A W, Chakraborti D, de Marco F, Vilaine F, Wolff N, Lemoine R, Porcheron B, Géry C, Téoulé E, Chabout S, Mouille G, Neuhaus H E, Dinant S, Bellini C. 2015. Disruption of the sugar transporters AtSWEET11 and AtSWEET12 affects vascular development and freezing tolerance in Arabidopsis. Molecular Plant, 8, 1687–1690. Hu B, Jin J, Guo A Y, Zhang H, Luo J, Gao G. 2015. GSDS 2.0: An upgraded gene feature visualization server. Bioinformatics, 31, 1296–1297.Hu L, Liu S. 2012. Genome-wide analysis of the MADS-box gene family in cucumber. Genome, 55, 245–256. Hu L, Sun H, Li R, Zhang L, Wang S, Sui X, Zhang Z. 2011. Phloem unloading follows an extensive apoplasmic pathway in cucumber (Cucumis sativus L.) fruit from anthesis to marketable maturing stage. Plant, Cell and Environment, 34, 1835–1848.Hu L P, Meng F Z, Wang S H, Sui X L, Li W, Wei Y X, Sun J L, Zhang Z X. 2009. Changes in carbohydrate levels and their metabolic enzymes in leaves, phloem sap and mesocarp during cucumber (Cucumis sativus L.) fruit development. Scientia Horticulturae, 121, 131–137.Hu Y, Zhang J, Jia H, Sosso D, Li T, Frommer W B, Yang B, White F F, Wang N, Jones J B. 2014. Lateral organ boundaries 1 is a disease susceptibility gene for citrus bacterial canker disease. Proceedings of the National Academy of Sciences of the United States of America, 111, E521–E529.Huang S, Li R, Zhang Z, Li L, Gu X, Fan W, Lucas W J, Wang X, Xie B, Ni P, Ren Y, Zhu H, Li J, Lin K, Jin W, Fei Z, Li G, Staub J, Kilian A, van der Vossen E A, et al. 2009. The genome of the cucumber, Cucumis sativus L. Nature Genetics, 41, 1275–1281.Klemens P A W, Patzke K, Deitmer J, Spinner L, Le Hir R, Bellini C, Bedu M, Chardon F, Krapp A, Neuhaus H E. 2013. Overexpression of the vacuolar sugar carrier AtSWEET16 modifies germination, growth, and stress tolerance in Arabidopsis. Plant Physiology, 163, 1338–1352.Kühn C, Grof C P. 2010. Sucrose transporters of higher plants. Current Opinion in Plant Biology, 13, 288–298.Lalonde S, Wipf D, Frommer W B. 2004. Transport mechanisms for organic forms of carbon and nitrogen between source and sink. Annual Review of Plant Biology, 55, 341–372.Lescot M, Déhais P, Thijs G, Marchal K, Moreau Y, Van de Peer Y, Rouzé P, Rombauts S. 2002. PlantCARE, a database of plant cis-acting regulatory elements and a portal to tools for in silico analysis of promoter sequences. Nucleic Acids Research, 30, 325–327.Letunic I, Doerks T, Bork P. 2015. SMART: Recent updates, new developments and status in 2015. Nucleic Acids Research, 43, D257–D260.Lin I W, Sosso D, Chen L Q, Gase K, Kim S G, Kessler D, Klinkenberg P M, Gorder M K, Hou B H, Qu X Q, Carter C J, Baldwin I T, Frommer W B. 2014. Nectar secretion requires sucrose phosphate synthases and the sugar transporter SWEET9. Nature, 508, 546–549.Livak K J, Schmittgen T D. 2001. Analysis of relative gene expression data using real-time quantitative PCR and the 2-??CT method. Methods, 25, 402–408.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, 520.Rennie E A, Turgeon R. 2009. A comprehensive picture of phloem loading strategies. Proceedings of the National Academy of Sciences of the United States of America, 106, 14162–14167.Ruan Y L. 2014. Sucrose metabolism: Gateway to diverse carbon use and sugar signaling. Annual Review of Plant Biology, 65, 33–67.Schultz J, Milpetz F, Bork P, Ponting C P. 1998. SMART, a simple modular architecture research tool: identification of signaling domains. Proceedings of the National Academy of Sciences of the United States of America, 95, 5857–5864.Seo P J, Park J M, Kang S K, Kim S G, Park C M. 2011. An Arabidopsis senescence-associated protein SAG29 regulates cell viability under high salinity. Planta, 233, 189–200.Slewinski T L. 2011. Diverse functional roles of monosaccharide transporters and their homologs in vascular plants: A physiological perspective. Molecular Plant, 4, 641–662. 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.Streubel J, Pesce C, Hutin M, Koebnik R, Boch J, Szurek B. 2013. Five phylogenetically close rice SWEET genes confer TAL effector-mediated susceptibility to Xanthomonas oryzae pv. oryzae. New Phytologist, 200, 808–819.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 and Evolution, 28, 2731–2739.Wei X, Liu F, Chen C, Ma F, Li M. 2014. The Malus domestica sugar transporter gene family: Identifications based on genome and expression profiling related to the accumulation of fruit sugars. Frontiers in Plant Science, 5, 569.Xu G, Guo C, Shan H, Kong H. 2012. Divergence of duplicate genes in exon-intron structure. Proceedings of the National Academy of Sciences of the United States of America, 109, 1187–1192.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.Yadav U P, Ayre B G, Bush D R. 2015. Transgenic approaches to altering carbon and nitrogen partitioning in whole plants: Assessing the potential to improve crop yields and nutritional quality. Frontiers in Plant Science, 6, 275. Yuan M, Chu Z, Li X, Xu C, Wang S. 2009. Pathogen-induced expressional loss of function is the key factor in race-specific bacterial resistance conferred by a recessive R gene xa13 in rice. Plant, Cell and Environment, 50, 947–955.Yuan M, Wang S. 2013. Rice MtN3/saliva/SWEET family genes and their homologs 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.Zheng Q, Tang Z, Xu Q, Deng X. 2014. Isolation, phylogenetic relationship and expression profiling of sugar transporter genes in sweet orange (Citrus sinensis). Plant Cell, Tissue and Organ Culture, 119, 609–624.Zhou Y, Liu L, Huang W, Yuan M, Zhou F, Li X, Lin Y. 2014. Overexpression of OsSWEET5 in rice causes growth retardation and precocious senescence. PLOS ONE, 9, e94210. |
| No Suggested Reading articles found! |
|
|
Viewed |
|
|
|
Full text
|
|
|
|
|
Abstract
|
|
|
|
|
Cited |
|
|
|
|
| |
Shared |
|
|
|
|
| |
Discussed |
|
|
|
|
