期刊论文详细信息
BMC Genomics
Soybean (Glycine max) SWEET gene family: insights through comparative genomics, transcriptome profiling and whole genome re-sequence analysis
Henry T. Nguyen4  Dong Xu2  Trupti Joshi2  Yang Liu2  Juhi Chaudhary4  Li Lin4  Li Song4  Humira Sonah4  Mingzhe Zhao1  Bjorn Nicander3  Silvas Prince4  Rupesh Deshmukh4  Babu Valliyodan4  Gunvant Patil4 
[1] Current address: Agronomy College of Shenyang Agricultural University, Shenyang, China;Department of Computer Science, Informatics Institute, and Christopher S. Bond Life Sciences Center, University of Missouri, Columbia 65211, MO, USA;Department of Plant Biology and Forest Genetics and Linnean Center for Plant Biology, Swedish University of Agricultural Sciences, Uppsala, Sweden;National Center for Soybean Biotechnology and Division of Plant Sciences, University of Missouri, Columbia 65211, MO, USA
关键词: Soybean;    Whole genome re-sequencing;    Sink;    Sugar transport;    Effluxer;    SWEET;   
Others  :  1222466
DOI  :  10.1186/s12864-015-1730-y
 received in 2014-12-29, accepted in 2015-06-26,  发布年份 2015
【 摘 要 】

Background

SWEET (MtN3_saliva) domain proteins, a recently identified group of efflux transporters, play an indispensable role in sugar efflux, phloem loading, plant-pathogen interaction and reproductive tissue development. The SWEET gene family is predominantly studied in Arabidopsis and members of the family are being investigated in rice. To date, no transcriptome or genomics analysis of soybean SWEET genes has been reported.

Results

In the present investigation, we explored the evolutionary aspect of the SWEET gene family in diverse plant species including primitive single cell algae to angiosperms with a major emphasis on Glycine max. Evolutionary features showed expansion and duplication of the SWEET gene family in land plants. Homology searches with BLAST tools and Hidden Markov Model-directed sequence alignments identified 52 SWEET genes that were mapped to 15 chromosomes in the soybean genome as tandem duplication events. Soybean SWEET (GmSWEET) genes showed a wide range of expression profiles in different tissues and developmental stages. Analysis of public transcriptome data and expression profiling using quantitative real time PCR (qRT-PCR) showed that a majority of the GmSWEET genes were confined to reproductive tissue development. Several natural genetic variants (non-synonymous SNPs, premature stop codons and haplotype) were identified in the GmSWEET genes using whole genome re-sequencing data analysis of 106 soybean genotypes. A significant association was observed between SNP-haplogroup and seed sucrose content in three gene clusters on chromosome 6.

Conclusion

Present investigation utilized comparative genomics, transcriptome profiling and whole genome re-sequencing approaches and provided a systematic description of soybean SWEET genes and identified putative candidates with probable roles in the reproductive tissue development. Gene expression profiling at different developmental stages and genomic variation data will aid as an important resource for the soybean research community and can be extremely valuable for understanding sink unloading and enhancing carbohydrate delivery to developing seeds for improving yield.

【 授权许可】

   
2015 Patil et al.

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【 参考文献 】
  • [1]Rolland F, Moore B, Sheen J. Sugar sensing and signaling in plants. Plant Cell. 2002; 14 Supplement:S185-205.
  • [2]Wind J, Smeekens S, Hanson J. Sucrose: metabolite and signaling molecule. Phytochem. 2010; 71(14):1610-4.
  • [3]Ayre BG. Membrane-transport systems for sucrose in relation to whole-plant carbon partitioning. Mol Plant. 2011; 4:ssr014.
  • [4]Sauer N. Molecular physiology of higher plant sucrose transporters. FEBS Lett. 2007; 581(12):2309-17.
  • [5]Ruan Y-L. Sucrose metabolism: gateway to diverse carbon use and sugar signaling. Annu Rev Plant Biol. 2014; 65:33-67.
  • [6]Baker RF, Leach KA, Braun DM. SWEET as sugar: new sucrose effluxers in plants. Mol Plant. 2012; 5(4):766-8.
  • [7]Turgeon R, Wolf S. Phloem transport: cellular pathways and molecular trafficking. Annu Rev Plant Biol. 2009; 60:207-21.
  • [8]Lemoine R, La Camera S, Atanassova R, Dedaldechamp F, Allario T, Pourtau N, et al. Source-to-sink transport of sugar and regulation by environmental factors. Front Plant Sci. 2013;4:272.
  • [9]Braun DM, Slewinski TL. Genetic control of carbon partitioning in grasses: roles of sucrose transporters and tie-dyed loci in phloem loading. Plant Physiol. 2009; 149(1):71-81.
  • [10]Rennie EA, Turgeon R. A comprehensive picture of phloem loading strategies. Proc Natl Acad Sci U S A. 2009; 106(33):14162-7.
  • [11]Lohaus G, Burba M, Heldt H. Comparison of the contents of sucrose and amino acids in the leaves, phloem sap and taproots of high and low sugar-producing hybrids of sugar beet (Beta vulgaris L.). J Exp Bot. 1994; 45(8):1097-101.
  • [12]Slewinski TL, Meeley R, Braun DM. Sucrose transporter1 functions in phloem loading in maize leaves. J Exp Bot. 2009; 60(3):881-92.
  • [13]Srivastava AC, Ganesan S, Ismail IO, Ayre BG. Functional characterization of the Arabidopsis AtSUC2 sucrose/H+ symporter by tissue-specific complementation reveals an essential role in phloem loading but not in long-distance transport. Plant Physiol. 2008; 148(1):200-11.
  • [14]Aoki N, Hirose T, Scofield GN, Whitfeld PR, Furbank RT. The sucrose transporter gene family in rice. Plant Cell Physiol. 2003; 44(3):223-32.
  • [15]Chen L-Q, Hou B-H, Lalonde S, Takanaga H, Hartung ML, Qu X-Q, et al. Sugar transporters for intercellular exchange and nutrition of pathogens. Nature. 2010;468(7323):527–32.
  • [16]Sonnewald U. SWEETS–the missing sugar efflux carriers. Front Plant Sci. 2011; 2:1-2.
  • [17]Kühn C. A comparison of the sucrose transporter systems of different plant species. Plant Biol. 2003; 5(3):215-32.
  • [18]Contim LAS, Waclawovsky AJ, Delú‐Filho N, Pirovani CP, Clarindo WR, Loureiro ME, et al. The soybean sucrose binding protein gene family: genomic organization, gene copy number and tissue‐specific expression of the SBP2 promoter. J Exp Bot. 2003;54(393):2643–53.
  • [19]Guan Y-F, Huang X-Y, Zhu J, Gao J-F, Zhang H-X, Yang Z-N. 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 Physiol. 2008; 147(2):852-63.
  • [20]Yuan M, Wang S. Rice MtN3/saliva family genes and their homologues in cellular organisms. Mol Plant. 2013; 6:sst035.
  • [21]Gamas P, de Carvalho NF, Lescure N, Cullimore JV. Use of a subtractive hybridization approach to identify new Medicago truncatula genes induced during root nodule development. MPMI. 1996; 9(4):233-42.
  • [22]Artero RD, Terol-Alcayde J, Paricio N, Ring J, Bargues M, Torres A, et al. Saliva, a new Drosophila gene expressed in the embryonic salivary glands with homologues in plants and vertebrates. Mech Dev. 1998;75(1):159–62.
  • [23]Slewinski TL. Diverse functional roles of monosaccharide transporters and their homologs in vascular plants: a physiological perspective. Mol Plant. 2011; 4(4):641-62.
  • [24]Braun DM. SWEET! The pathway is complete. Science. 2012; 335(6065):173-4.
  • [25]Chen LQ. SWEET sugar transporters for phloem transport and pathogen nutrition. New Phytol. 2014; 201(4):1150-5.
  • [26]Chen L-Q, Qu X-Q, Hou B-H, Sosso D, Osorio S, Fernie AR, et al. Sucrose efflux mediated by SWEET proteins as a key step for phloem transport. Science. 2012;335(6065):207–11.
  • [27]Streubel J, Pesce C, Hutin M, Koebnik R, Boch J, Szurek B. Five phylogenetically close rice SWEET genes confer TAL effector‐mediated susceptibility to Xanthomonas oryzae pv. oryzae. New Phytol. 2013; 200(3):808-19.
  • [28]Denancé N, Szurek B, Noël LD. Emerging functions of nodulin-like proteins in non-nodulating plant species. Plant Cell Physiol. 2014; 55(3):469-74.
  • [29]Doidy J, Grace E, Kühn C, Simon-Plas F, Casieri L, Wipf D. Sugar transporters in plants and in their interactions with fungi. Trends Plant Sci. 2012; 17(7):413-22.
  • [30]Patrick JW. PHLOEM UNLOADING: sieve element unloading and post-sieve element transport. Annu Rev Plant Physiol Plant Mol Biol. 1997; 48(1):191-222.
  • [31]Baud S, Dubreucq B, Miquel M, Rochat C, Lepiniec L. Storage reserve accumulation in Arabidopsis: metabolic and developmental control of seed filling. Am Soc Plant Biologists. 2008; 6:e0113.
  • [32]Weber H, Borisjuk L, Wobus U. Molecular physiology of legume seed development. Annu Rev Plant Biol. 2005; 56:253-79.
  • [33]Zhang W-H, Zhou Y, Dibley KE, Tyerman SD, Furbank RT, Patrick JW. Review: Nutrient loading of developing seeds. Funct Plant Biol. 2007; 34(4):314-31.
  • [34]Lalonde S, Tegeder M, Throne‐Holst M, Frommer W, Patrick J. Phloem loading and unloading of sugars and amino acids. Plant Cell Environ. 2003; 26(1):37-56.
  • [35]Marschner H, Marschner P. Marschner’s mineral nutrition of higher plants. Academic press, London; 2012.
  • [36]Zhou Y, Qu H, Dibley KE, Offler CE, Patrick JW. A suite of sucrose transporters expressed in coats of developing legume seeds includes novel pH‐independent facilitators. Plant J. 2007; 49(4):750-64.
  • [37]Ludewig F, Flügge U-I. Role of metabolite transporters in source-sink carbon allocation. Front Plant Sci. 2013; 4:231.
  • [38]Weschke W, Panitz R, Gubatz S, Wang Q, Radchuk R, Weber H, et al. The role of invertases and hexose transporters in controlling sugar ratios in maternal and filial tissues of barley caryopses during early development. Plant J. 2003;33(2):395–411.
  • [39]Wei X, Liu F, Chen C, Ma F, Li M. The Malus domestica sugar transporter gene family: identifications based on genome and expression profiling related to the accumulation of fruit sugars. Front Plant Sci. 2014; 5:569.
  • [40]Yang B, Sugio A, White FF. Os8N3 is a host disease-susceptibility gene for bacterial blight of rice. Proc Natl Acad Sci U S A. 2006; 103(27):10503-8.
  • [41]Punta M, Coggill PC, Eberhardt RY, Mistry J, Tate J, Boursnell C, et al. The Pfam protein families database. Nucleic Acids Res. 2011;40:gkr1065.
  • [42]Van Bel M, Proost S, Wischnitzki E, Movahedi S, Scheerlinck C, Van De Peer Y, et al. Dissecting plant genomes with the PLAZA comparative genomics platform. Plant Physiol. 2011;111:189514.
  • [43]Xuan YH, Hu YB, Chen L-Q, Sosso D, Ducat DC, Hou B-H, et al. Functional role of oligomerization for bacterial and plant SWEET sugar transporter family. Proc Natl Acad Sci U S A. 2013;110(39):E3685–94.
  • [44]Severin AJ, Cannon SB, Graham MM, Grant D, Shoemaker RC. Changes in twelve homoeologous genomic regions in soybean following three rounds of polyploidy. Plant Cell. 2011; 23(9):3129-36.
  • [45]Soltis DE, Visger CJ, Soltis PS. The polyploidy revolution then… and now: Stebbins revisited. Am J Bot. 2014; 101(7):1057-78.
  • [46]Schmutz J, Cannon SB, Schlueter J, Ma J, Mitros T, Nelson W, et al. Genome sequence of the palaeopolyploid soybean. Nature. 2010;463(7278):178–83.
  • [47]Roulin A, Auer PL, Libault M, Schlueter J, Farmer A, May G, et al. The fate of duplicated genes in a polyploid plant genome. Plant J. 2013;73(1):143–53.
  • [48]Li W-H, Gojobori T, Nei M. Pseudogenes as a paradigm of neutral evolution. Nature. 1981; 292(5820):237-9.
  • [49]Lynch M, Conery JS. The evolutionary fate and consequences of duplicate genes. Science. 2000; 290(5494):1151-5.
  • [50]Xu Y, Tao Y, Cheung LS, Fan C, Chen L-Q, Xu S, et al. Structures of bacterial homologues of SWEET transporters in two distinct conformations. Nature. 2014;515:448–52.
  • [51]Geer LY, Domrachev M, Lipman DJ, Bryant SH. CDART: protein homology by domain architecture. Genome Res. 2002; 12(10):1619-23.
  • [52]Afoufa-Bastien D, Medici A, Jeauffre J, Coutos-Thevenot P, Lemoine R, Atanassova R, et al. The Vitis vinifera sugar transporter gene family: phylogenetic overview and macroarray expression profiling. BMC Plant Biol. 2010;10(1):245.
  • [53]Thijs G, Moreau Y, De Smet F, Mathys J, Lescot M, Rombauts S, et al. INCLUSive: integrated clustering, upstream sequence retrieval and motif sampling. Bioinformatics. 2002;18(2):331–2.
  • [54]Klepek YS, Volke M, Konrad KR, Wippel K, Hoth S, Hedrich R, et al. Arabidopsis thaliana POLYOL/MONOSACCHARIDE TRANSPORTERS 1 and 2: fructose and xylitol/H+ symporters in pollen and young xylem cells. J Exp Bot. 2009;61:erp322.
  • [55]Smalle J, Kurepa J, Haegman M, Gielen J, Van Montagu M, Van Der Straeten D. The trihelix DNA-binding motif in higher plants is not restricted to the transcription factors GT-1 and GT-2. Proc Natl Acad Sci U S A. 1998; 95(6):3318-22.
  • [56]Zhou D-X. Regulatory mechanism of plant gene transcription by GT-elements and GT-factors. Trends Plant Sci. 1999; 4(6):210-4.
  • [57]Severin AJ, Woody JL, Bolon Y-T, Joseph B, Diers BW, Farmer AD, et al. RNA-Seq Atlas of Glycine max: a guide to the soybean transcriptome. BMC Plant Biol. 2010;10(1):160.
  • [58]Antony G, Zhou J, Huang S, Li T, Liu B, White F, et al. Rice xa13 recessive resistance to bacterial blight is defeated by induction of the disease susceptibility gene Os-11 N3. Plant Cell. 2010;22(11):3864–76.
  • [59]Chu Z, Yuan M, Yao J, Ge X, Yuan B, Xu C, et al. Promoter mutations of an essential gene for pollen development result in disease resistance in rice. Genes Dev. 2006;20(10):1250–5.
  • [60]Lauter ANM, Peiffer GA, Yin T, Whitham SA, Cook D, Shoemaker RC, et al. Identification of candidate genes involved in early iron deficiency chlorosis signaling in soybean (Glycine max) roots and leaves. BMC Genomics. 2014;15(1):702.
  • [61]Lam H-M, Xu X, Liu X, Chen W, Yang G, Wong F-L, et al. Resequencing of 31 wild and cultivated soybean genomes identifies patterns of genetic diversity and selection. Nat Genet. 2010;42(12):1053–9.
  • [62]Qi X, Li M-W, Xie M, Liu X, Ni M, Shao G, et al. Identification of a novel salt tolerance gene in wild soybean by whole-genome sequencing. Nat Comm. 2014;5:4340.
  • [63]Patil G. Identification of sequence variants in candidate genes for Oil content using whole genome Re-sequencing of soybean germplasm. In: Plant and animal genome XXII conference. San Diego, CA Plant and Animal Genome; 2014.
  • [64]Chardon F, Bedu M, Calenge F, Klemens PA, Spinner L, Clement G, et al. Leaf fructose content is controlled by the vacuolar transporter SWEET17 in Arabidopsis. Curr Biol. 2013;23(8):697–702.
  • [65]Zimmermann MH, Ziegler H. List of sugars and sugar alcohols in sieve-tube exudates. Encycl Plant Physiol, New Ser; 1975.
  • [66]Ayre BG, Keller F, Turgeon R. Symplastic continuity between companion cells and the translocation stream: long-distance transport is controlled by retention and retrieval mechanisms in the phloem. Plant Physiol. 2003; 131(4):1518-28.
  • [67]Patil G, Nicander B. Identification of two additional members of the tRNA isopentenyltransferase family in Physcomitrella patens. Plant Mol Biol. 2013; 82(4–5):417-26.
  • [68]Liu Y-J, Han X-M, Ren L-L, Yang H-L, Zeng Q-Y. Functional divergence of the glutathione S-transferase supergene family in Physcomitrella patens reveals complex patterns of large gene family evolution in land plants. Plant Physiol. 2013; 161(2):773-86.
  • [69]McCarthy TW, Der JP, Honaas LA, Anderson CT. Phylogenetic analysis of pectin-related gene families in Physcomitrella patens and nine other plant species yields evolutionary insights into cell walls. BMC Plant Biol. 2014; 14(1):79.
  • [70]Rensing SA, Lang D, Zimmer AD, Terry A, Salamov A, Shapiro H, et al. The Physcomitrella genome reveals evolutionary insights into the conquest of land by plants. Science. 2008;319(5859):64–9.
  • [71]Keller R, Ziegler C, Schneider D. When two turn into one: evolution of membrane transporters from half modules. Biol Chem. 2014; 395(12):1379-88.
  • [72]Talbot NJ. Cell biology: Raiding the sweet shop. Nature. 2010; 468(7323):510-1.
  • [73]Wang J-L, Liu C-Y, Wang J, Qi Z-M, Li H, Hu G-H, et al. An integrated QTL Map of fungal disease resistance in soybean (glycine max L. Merr): a method of meta-analysis for mining R genes. Agric Sci China. 2010;9(2):223–32.
  • [74]Yuan M, Chu Z, Li X, Xu C, Wang S. The bacterial pathogen Xanthomonas oryzae overcomes rice defenses by regulating host copper redistribution. Plant Cell. 2010; 22(9):3164-76.
  • [75]van Ooij C. Pathogenesis: The SWEET life of pathogens. Nat Rev Microb. 2011; 9(1):4-5.
  • [76]Patrick J, Offler C. Post-sieve element transport of sucrose in developing seeds. Funct Plant Biol. 1995; 22(4):681-702.
  • [77]Antos M, Wiebold W. Abscission, total soluble sugars, and starch profiles within a soybean canopy. Agron J. 1984; 76(5):715-9.
  • [78]Nagel L, Brewster R, Riedell W, Reese R. Cytokinin regulation of flower and pod set in soybeans (Glycine max (L.) Merr.). Ann Bot. 2001; 88(1):27-31.
  • [79]Dybing CD, Reese ZN. Nitrogen and carbohydrate nutrient concentrations and flower Set in soybean glycine max (L.) merr.). J Biol Sci. 2008; 8(1):24-33.
  • [80]Li C, Wei J, Lin Y, Chen H. Gene silencing using the recessive rice bacterial blight resistance gene xa13 as a new paradigm in plant breeding. Plant Cell Rep. 2012; 31(5):851-62.
  • [81]Fernandez L, Le Cunff L, Tello J, Lacombe T, Boursiquot JM, Fournier Level A, et al. This P: Haplotype diversity of VvTFL1A gene and association with cluster traits in grapevine (V. vinifera). BMC Plant Biol. 2014;14(1):209.
  • [82]Langewisch T, Zhang H, Vincent R, Joshi T, Xu D, Bilyeu K. Major soybean maturity gene haplotypes revealed by SNPViz analysis of 72 sequenced soybean genomes. PLoS One. 2014; 9(4):e94150.
  • [83]Prince SJ, Song L, Qiu D, Maldonado Dos Santos JV, Chai C, Joshi T, et al. Genetic variants in root architecture-related genes in a Glycine soja accession, a potential resource to improve cultivated soybean. BMC Genomics. 2015;16(1):132.
  • [84]Goodstein DM, Shu S, Howson R, Neupane R, Hayes RD, Fazo J, et al. Phytozome: a comparative platform for green plant genomics. Nucleic Acids Res. 2012;40(Database issue):D1178–86.
  • [85]Edgar RC. MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res. 2004; 32(5):1792-7.
  • [86]Apweiler R, Attwood TK, Bairoch A, Bateman A, Birney E, Biswas M, et al. The InterPro database, an integrated documentation resource for protein families, domains and functional sites. Nucleic Acids Res. 2001;29(1):37–40.
  • [87]Tamura K, Nei M, Kumar S. Prospects for inferring very large phylogenies by using the neighbor-joining method. Proc Natl Acad Sci U S A. 2004; 101(30):11030-5.
  • [88]Tamura K, Peterson D, Peterson N, Stecher G, Nei M, Kumar S. MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Mol Biol Evol. 2011; 28(10):2731-9.
  • [89]Thijs G, Lescot M, Marchal K, Rombauts S, De Moor B, Rouze P, et al. A higher-order background model improves the detection of promoter regulatory elements by Gibbs sampling. Bioinformatics. 2001;17(12):1113–22.
  • [90]Bülow L, Brill Y, Hehl R. AthaMap-assisted transcription factor target gene identification in Arabidopsis thaliana. Database. 2010; 2010:034.
  • [91]Joshi T, Fitzpatrick MR, Chen S, Liu Y, Zhang H, Endacott RZ, et al. Soybean knowledge base (SoyKB): a web resource for integration of soybean translational genomics and molecular breeding. Nucleic Acids Res. 2014;42(Database issue):D1245–52.
  • [92]Cannon EK, Cannon SB. Chromosome visualization tool: a whole genome viewer. Int J Plant Geno. 2011; 2011:373875.
  • [93]Suyama M, Torrents D, Bork P. PAL2NAL: robust conversion of protein sequence alignments into the corresponding codon alignments. Nucleic Acids Res. 2006; 34(suppl 2):W609-12.
  • [94]Page RD. Visualizing phylogenetic trees using TreeView. Curr protoc bioinformatics. 2002.6.2. 1-6.2. 15. vol. Chapter 6
  • [95]Liu C-M, Wong T, Wu E, Luo R, Yiu S-M, Li Y, et al. SOAP3: ultra-fast GPU-based parallel alignment tool for short reads. Bioinformatics. 2012;28(6):878–9.
  • [96]Van Dongen JT, Ammerlaan AM, Wouterlood M, Van Aelst AC, Borstlap AC. Structure of the developing pea seed coat and the post-phloem transport pathway of nutrients. Ann Bot. 2003; 91(6):729-37.
  • [97]Bradbury PJ, Zhang Z, Kroon DE, Casstevens TM, Ramdoss Y, Buckler ES. TASSEL: software for association mapping of complex traits in diverse samples. Bioinformatics. 2007; 23(19):2633-5.
  • [98]Milne I, Shaw P, Stephen G, Bayer M, Cardle L, Thomas WT, et al. Flapjack—graphical genotype visualization. Bioinformatics. 2010;26(24):3133–4.
  • [99]Krogh A, Larsson B, Von Heijne G, Sonnhammer EL. Predicting transmembrane protein topology with a hidden Markov model: application to complete genomes. J Mol Biol. 2001; 305(3):567-80.
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