Molecular Biology Reports

, Volume 46, Issue 2, pp 2327–2353 | Cite as

Further studies on sugar transporter (SWEET) genes in wheat (Triticum aestivum L.)

  • Tinku Gautam
  • Gautam Saripalli
  • Vijay Gahlaut
  • Anuj Kumar
  • P. K. Sharma
  • H. S. Balyan
  • P. K. GuptaEmail author
Original Article


SWEET proteins represent one of the largest sugar transporter family in the plant kingdom and play crucial roles in plant development and stress responses. In the present study, a total of 108 TaSWEET genes distributed on all the 21 wheat chromosomes were identified using the latest whole genome sequence (as against 59 genes reported in an earlier report). These 108 genes included 14 of the 17 types reported in Arabidopsis and also included three novel types. Tandem duplications (22) and segmental duplications (5) played a significant role in the expansion of TaSWEET family. A number of cis-elements were also identified in the promoter regions of TaSWEET genes, indicating response of TaSWEET genes during development and also during biotic/abiotic stresses. The TaSWEET proteins carried 4–7 trans-membrane helices (TMHs) showing diversity in structure. Phylogenetic analysis using SWEET proteins of wheat and 8 other species gave four well-known clusters. Expression analysis involving both in silico and in planta indicated relatively higher expression of TaSWEET genes in water/heat sensitive and leaf rust resistant genotypes. The results provided insights into the functional role of TaSWEETs in biotic and abiotic stresses, which may further help in planning strategies to develop high yielding wheat varieties tolerant to environmental stresses.


Sugar transporter TaSWEET Sucrose Drought Leaf rust Wheat 



The work was carried out, when TG and GS held JRF/SRF positions under a research project funded under NASF-ICAR program of Government of India. PKG was awarded Hony Scientist position and HSB was awarded Senior Scientist position both from Indian National Science Academy (INSA). For qRT-PCR, RNA for a pair of NILs was available from another collaborative project funded by NASF-ICAR. Bioinformatics Infrastructure Facility (BIF) laboratory was used for carrying out a part of the bioinformatics work. Head, Department of Genetics and Plant Breeding, CCS University, Meerut, provided the necessary infrastructure.

Author contributions

PKG, HSB and PKS conceived the experiment and also edited and finalized the manuscript. TG conducted most of the experiments including qRT-PCR with the help of GS. AK conducted molecular dynamics analysis and VG helped in chromosome mapping.

Compliance with ethical standards

Conflict of interest

All the authors declare that there is no conflict of interest.

Ethical approval

This article does not contain any studies with human participants or animals performed by any of the authors.

Supplementary material

11033_2019_4691_MOESM1_ESM.docx (1.4 mb)
Supplementary material 1 (DOCX 1437 KB)
11033_2019_4691_MOESM2_ESM.docx (116 kb)
Supplementary material 2 (DOCX 116 KB)


  1. 1.
    Aoki N, Hirose T, Scofield GN, Whitfeld PR, Furbank RT (2003) The sucrose transporter gene family in rice. Plant Cell Physiol 44:223–232CrossRefPubMedGoogle Scholar
  2. 2.
    Lemoine R, Camera SL, Atanassova R et al (2013) Source-to sink transport of sugar and regulation by environmental factors. Front Plant Sci 4:272CrossRefPubMedPubMedCentralGoogle Scholar
  3. 3.
    Sauer N (2007) Molecular physiology of higher plant sucrose transporters. FEBS Lett 581:2309–2317CrossRefPubMedGoogle Scholar
  4. 4.
    Srivastava AC, Ganesan S, Ismail IO, Ayre BG (2008) 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 148:200–211CrossRefPubMedPubMedCentralGoogle Scholar
  5. 5.
    Chen LQ, Hou BH, Lalonde S et al (2010) Sugar transporters for intercellular exchange and nutrition of pathogens. Nature 468:527–532CrossRefPubMedPubMedCentralGoogle Scholar
  6. 6.
    Gamas P, Niebel FC, Lescure N, Cullimore J (1996) Use of a subtractive hybridization approach to identify new Medicago truncatula genes induced during root nodule development. Mol Plant Microbe Interact 9:233–242CrossRefPubMedGoogle Scholar
  7. 7.
    Arteron DR, Terol-Alcayde J, Paricio N, Ring J, Bargues M, Torres A, Perez-Alonso M (1998) Saliva, a new Drosophila gene expressed in the embryonic salivary glands with homologues in plants and vertebrates. Mech Dev 75:159–162CrossRefGoogle Scholar
  8. 8.
    Yuan M, Wang S (2013) Rice MtN3/saliva/SWEET family genes and their homologs in cellular organisms. Mol Plant 6:665–674CrossRefPubMedGoogle Scholar
  9. 9.
    Jia B, Zhu XF, Pu ZJ, Duan YX, Hao LJ, Zhang J, Chen LQ, Jeon CO, Xuan YH (2017) Integrative view of the diversity and evolution of SWEET and SemiSWEET sugar transporters. Front Plant Sci 8:2178CrossRefPubMedPubMedCentralGoogle Scholar
  10. 10.
    Patil G, Valliyodan B, Deshmukh R et al (2015) Soybean (Glycine max) SWEET gene family: insights through comparative genomics, transcriptome profiling and whole genome re-sequence analysis. BMC Genom 16:520CrossRefGoogle Scholar
  11. 11.
    Jian H, Lu K, Yang B et al (2016) Genome-wide analysis and expression profiling of the SUC and SWEET gene families of sucrose transporters in oilseed rape (Brassica napus L.). Front. Plant Sci 7:1464Google Scholar
  12. 12.
    Li H, Li X, Xuan Y, Jiang J, Wei Y, Piao Z (2018) Genome wide identification and expression profiling of SWEET genes family reveals its role during Plasmodiophora brassicae-induced formation of clubroot in Brassica rapa. Front Plant Sci 9:207CrossRefPubMedPubMedCentralGoogle Scholar
  13. 13.
    Mizuno H, Kasuga S, Kawahigashi H (2016) The sorghum SWEET gene family: stem sucrose accumulation as revealed through transcriptome profiling. Biotechnol Biofuels 9:127CrossRefPubMedPubMedCentralGoogle Scholar
  14. 14.
    Manck-Gotzenberger J, Requena N (2016) Arbuscular mycorrhiza symbiosis induces a major transcriptional reprogramming of the potato SWEET sugar transporter family. Front Plant Sci 7:487CrossRefPubMedPubMedCentralGoogle Scholar
  15. 15.
    Feng L, Frommer WB (2015) Structure and function of SemiSWEET and SWEET sugar transporters. Trends Biochem Sci 40:480–486CrossRefPubMedGoogle Scholar
  16. 16.
    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. Front Plant Sci 5:569CrossRefPubMedPubMedCentralGoogle Scholar
  17. 17.
    Chong J, Piron MC, 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. J Exp Bot 65:6589–6601CrossRefPubMedGoogle Scholar
  18. 18.
    Miao H, Sun P, Liu Q et al (2017) Genome-wide analyses of SWEET family proteins reveal involvement in fruit development and abiotic/biotic stress responses in banana. Sci Rep 7:3536CrossRefPubMedPubMedCentralGoogle Scholar
  19. 19.
    Miao L, Lv Y, Kong L et al (2018) Genome-wide identification, phylogeny, evolution, and expression patterns of MtN3/saliva/SWEET genes and functional analysis of BcNS in Brassica rapa. BMC Genom 19:174CrossRefGoogle Scholar
  20. 20.
    Gao Y, Wang ZY, Kumar V, Xu XF, Yuan P, Zhu XF, Li TY, Jia B, Xuan YH (2018) Genome-wide identification of the SWEET gene family in wheat. Gene 642:284–292CrossRefPubMedGoogle Scholar
  21. 21.
    Chen LQ, Qu XQ, Hou BH, Sosso D, Osorio S, Fernie AR, Frommer WB (2012) Sucrose efflux mediated by SWEET proteins as a key step for phloem transport. Science 335:207–211CrossRefPubMedGoogle Scholar
  22. 22.
    Chen LQ, Lin IW, Qu XQ, Sosso D, McFarlane HE, Londoño A, Samuels AL, Frommer WB (2015) A cascade of sequentially expressed sucrose transporters in the seed coat and endosperm provides nutrition for the Arabidopsis embryo. Plant Cell 27:607–619CrossRefPubMedPubMedCentralGoogle Scholar
  23. 23.
    Durand M, Porcheron B, Hennion N, Maurousset L, Lemoine R, Pourtau N (2016) Water deficit enhances C export to the roots in A. thaliana plants with contribution of sucrose transporters in both shoot and roots. Plant Physiol 170:1460–1479CrossRefPubMedPubMedCentralGoogle Scholar
  24. 24.
    Seo PJ, Park JM, Kang SK, Kim SG, Park CM (2011) An Arabidopsis senescence-associated protein SAG29 regulates cell viability under high salinity. Planta 233:189–200CrossRefPubMedGoogle Scholar
  25. 25.
    Sosso D, Luo D, Li QB et al (2015) Seed filling in domesticated maize and rice depends on SWEET-mediated hexose transport. Nat Genet 47:1489–1493CrossRefPubMedGoogle Scholar
  26. 26.
    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 9:94210CrossRefGoogle Scholar
  27. 27.
    Le Hir R, Spinner L, Klemens PA et al (2015) Disruption of the sugar transporters AtSWEET11 and AtSWEET12 affects vascular development and freezing tolerance in Arabidopsis. Mol Plant 8:1687–1690CrossRefPubMedGoogle Scholar
  28. 28.
    Chen LQ (2014) SWEET sugar transporters for phloem transport and pathogen nutrition. New Phytol 201:1150–1155CrossRefPubMedGoogle Scholar
  29. 29.
    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. Plant Cell 22:3864–3876CrossRefPubMedPubMedCentralGoogle Scholar
  30. 30.
    Hutin M, Perez-Quintero AL, Lopez C, Szurek B (2015) MorTAL kombat: the story of defense against TAL effectors through loss-of-susceptibility. Front Plant Sci 6:535PubMedPubMedCentralGoogle Scholar
  31. 31.
    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 Phytol 200:808–819CrossRefPubMedGoogle Scholar
  32. 32.
    Yang B, Sugio A, White FF (2006) Os8N3 is a host disease-susceptibility gene for bacterial blight of rice. Proc Natl Acad Sci 103:10503–10508CrossRefPubMedGoogle Scholar
  33. 33.
    Keating BA, Herrero M, Carberry PS, Gardner J, Cole MB (2014) Food wedges: framing the global food demand and supply challenge towards 2050. Glob Food Sec 3:125–132CrossRefGoogle Scholar
  34. 34.
    Akter N, Rafiqul IM (2017) Heat stress effects and management in wheat: a review. Agron Sustain Dev 37:37CrossRefGoogle Scholar
  35. 35.
    Gupta PK, Balyan HS, Gahlaut V (2017) QTL analysis for drought tolerance in wheat: present status and future possibilities. Agronomy 7:5CrossRefGoogle Scholar
  36. 36.
    Mwadzingeni L, Shimelis H, Dube E, Laing MD, Tsilo TJ (2016) Breeding wheat for drought tolerance: progress and technologies. J Integr Agric 15:935–943CrossRefGoogle Scholar
  37. 37.
    Finn RD, Coggill P, Eberhardt RY et al (2016) The Pfam protein families database: towards a more sustainable future. Nucleic Acids Res 44:279–285CrossRefGoogle Scholar
  38. 38.
    Marchler-Bauer A, Bo Y, Han L et al (2017) CDD/SPARCLE: functional classification of proteins via subfamily domain architectures. Nucleic Acids Res 45:200–203CrossRefGoogle Scholar
  39. 39.
    Ning P, Liu C, Kang J, Lv J (2017) Genome-wide analysis of WRKY transcription factors in wheat (Triticum aestivum L.) and differential expression under water deficit condition. Peer J 5:3232CrossRefGoogle Scholar
  40. 40.
    Hu B, Jin J, Guo AY, Zhang H, Luo J, Gao G (2015) GSDS 2.0: an upgraded gene feature visualization server. Bioinformatics 31:1296–1297CrossRefPubMedGoogle Scholar
  41. 41.
    Rombauts S, Dehais P, Van Montagu M, Rouze P (1999) PlantCARE, a plant cis-acting regulatory element database. Nucleic Acids Res 27:295–296CrossRefPubMedPubMedCentralGoogle Scholar
  42. 42.
    Batra R, Saripalli G, Mohan A, Gupta S, Gill KS, Varadwaj PK, Balyan HS, Gupta PK (2017) Comparative analysis of AGPase genes and encoded proteins in eight monocots and three dicots with emphasis on wheat. Front Plant Sci 8:19CrossRefPubMedPubMedCentralGoogle Scholar
  43. 43.
    Dai X, Zhao PX (2011) psRNATarget: a plant small RNA target analysis server. Nucleic Acids Res 39:155–159 (Web Server Issue)CrossRefGoogle Scholar
  44. 44.
    Cheong W, Tan Y, Yap S, Ng KP (2015) Genome analysis ClicO FS: an interactive web-based service of Circos. Bioinformatics 31:3685–3687CrossRefPubMedPubMedCentralGoogle Scholar
  45. 45.
    Gasteiger E, Hoogland C, Gattiker A, Duvaud S, Wilkins MR, Appel RD, Bairoch A (2005) Protein identification and analysis tools on the ExPASy Server. In: Walker JM (ed) The proteomics protocols handbook. Humana Press, New York, pp 571–607CrossRefGoogle Scholar
  46. 46.
    Krogh A, Larsson B, Von HG, Sonnhammer EL (2001) Predicting transmembrane protein topology with a hidden Markov model: application to complete genomes. J Mol Biol 305:567–580CrossRefPubMedGoogle Scholar
  47. 47.
    Robert X, Gouet P (2014) Deciphering key features in protein structures with the new ENDscript server. Nucl Acids Res 42:320–324CrossRefGoogle Scholar
  48. 48.
    Bailey TL, Boden M, Buske FA, Frith M, Grant CE, Clementi L, Ren J, Li WW, Noble WS (2009) MEME suite: tools for motif discovery and searching. Nucleic Acids Res 37:202–208CrossRefGoogle Scholar
  49. 49.
    Tao Y, Cheung LS, Li S, Eom JS (2015) Structure of a eukaryotic SWEET transporter in a homo-trimeric complex. Nature 527:259–263CrossRefPubMedPubMedCentralGoogle Scholar
  50. 50.
    Simonetti FL, Teppa E, Chernomoretz A, Nielsen M, Marino Buslje C (2013) MISTIC: Mutual information server to infer coevolution. Nucleic Acids Res 41:8–14CrossRefGoogle Scholar
  51. 51.
    Kumar A, Kumar S, Kumar U, Suravajhala P, Gajula MN (2016) Functional and structural insights into novel DREB1A transcription factors in common wheat (Triticum aestivum L.): a molecular modeling approach. Comput Biol Chem 64:217–226CrossRefPubMedGoogle Scholar
  52. 52.
    Waterhouse A, Bertoni M, Bienert S et al (2018) SWISS-MODEL: homology modelling of protein structures and complexes. Nucleic Acids Res 46:296–303CrossRefGoogle Scholar
  53. 53.
    Pettersen EF, Goddard TD, Huang CC, Couch GS, Greenblatt DM, Meng EC, Ferrin TE (2004) UCSF Chimera--A visualization system for exploratory research and analysis. J Comput Chem 25:1605–1612CrossRefGoogle Scholar
  54. 54.
    Kim S, Thiessen PA, Bolton EE et al (2016) PubChem substance and compound databases. Nucleic Acid Res 44:1202–1213CrossRefGoogle Scholar
  55. 55.
    Kumar A, Kumar S, Kumar A, Sharma N (2017) Homology modeling, molecular docking and molecular dynamics based functional insights into rice urease bound to urea. Proc Natl Acad Sci 88:1539–1548Google Scholar
  56. 56.
    Schneidman-duhovny D, Inbar Y, Nussinov R, Wolfson HJ (2005) PatchDock and SymmDock: servers for rigid and symmetric docking. Nucleic Acids Res 33:363–367CrossRefGoogle Scholar
  57. 57.
    Abraham MJ, Murtola T, Schulz R, Páll S, Smith JC, Hess B, Lindahl E (2015) GROMACS: high performance molecular simulations through multi-level parallelism from laptops to supercomputers. SoftwareX 1-2:19-25CrossRefGoogle Scholar
  58. 58.
    Jorgensen WL, Maxwell DS, Tirado-rives J, Haven N (1996) Development and testing of the OPLS all-atom force field on conformational energetics and properties of organic liquids. J Am Chem Soc 118:11225–11236CrossRefGoogle Scholar
  59. 59.
    Kaminski GA, Friesner RA (2001) Evaluation and reparametrization of the OPLS-AA force field for proteins via comparison with accurate quantum chemical calculations on peptides. Phys Chem B 105:6474–6487CrossRefGoogle Scholar
  60. 60.
    Gahlaut V, Mathur S, Dhariwal R, Khurana JP, Tyagi AK, Balyan HS, Gupta PK (2014) A multi-step phosphorelay two-component system impacts on tolerance against dehydration stress in common wheat. Funct Integr Genomics 14:707–716CrossRefPubMedGoogle Scholar
  61. 61.
    Sharma C, Saripalli G, Kumar S et al (2018) A study of transcriptome in leaf rust infected bread wheat involving seedling resistance gene Lr28. Funct Plant Biol 45:1046–1064CrossRefGoogle Scholar
  62. 62.
    Conant CG, Wolfe HK (2008) Turning a hobby into a job: how duplicated genes find new functions. Nat Rev Genet 9:938–950CrossRefPubMedGoogle Scholar
  63. 63.
    Glover NM, Daron J, Pingault L, Vandepoele K, Paux E, Feuillet C, Choulet F (2015) Small-scale gene duplications played a major role in the recent evolution of wheat chromosome 3B. Genome Biol 16:1–13CrossRefGoogle Scholar
  64. 64.
    Ma J, Yang Y, Luo W et al (2017) Genome-wide identification and analysis of the MADS-box gene family in bread wheat (Triticum aestivum L.). Plos One 12:181443Google Scholar
  65. 65.
    Magadum S, Banerjee U, Murugan P, Gangapur D, Ravikesavan R (2013) Gene duplication as a major force in evolution. J Genet 92:155–161CrossRefPubMedGoogle Scholar
  66. 66.
    Roulin A, Auer PL, Libault M, Schlueter J, Farmer A, May G, Stacey G, Doerge RW, Jackson SA (2013) The fate of duplicated genes in a polyploid plant genome. Plant J 73:143–153CrossRefPubMedGoogle Scholar
  67. 67.
    Cannon SB, Mitra A, Baumgarten A, Young ND, May G (2004) The roles of segmental and tandem gene duplication in the evolution of large gene families in Arabidopsis thaliana. BMC Plant Biol 4:1–21CrossRefGoogle Scholar
  68. 68.
    Liu J, Li Y, Wang W, Gai J, Li Y (2016) Genome-wide analysis of MATE transporters and expression patterns of a subgroup of MATE genes in response to aluminum toxicity in soybean. BMC Genom 17:223CrossRefGoogle Scholar
  69. 69.
    Kumar S, Mohan A, Balyan HS, Gupta PK (2009) Orthology between genomes of Brachypodium, wheat and rice. BMC Res Notes 2:93CrossRefPubMedPubMedCentralGoogle Scholar
  70. 70.
    Pfeifer M, Kugler KG, Sandve SR et al (2014) Genome interplay in the grain transcriptome of hexaploid bread wheat. Science 345:1250091–1250091CrossRefPubMedGoogle Scholar
  71. 71.
    Ikai A (1980) Thermostability and aliphatic index of globular proteins. J Biochem 88:1895–1898Google Scholar
  72. 72.
    Chandran D (2015) Co-option of developmentally regulated plant SWEET transporters for pathogen nutrition and abiotic stress tolerance. IUBMB Life 67:461–471CrossRefPubMedGoogle Scholar
  73. 73.
    Eom JS, Chen LQ, Sosso D, Julius BT (2015) SWEETs, transporters for intracellular and intercellular sugar translocation. Curr Opin Plant Biol 25:53–62CrossRefPubMedGoogle Scholar
  74. 74.
    Chardon F, Bedu M, Calenge F et al (2013) Leaf fructose content is controlled by the vacuolar transporter SWEET17 in Arabidopsis. Curr Biol 23:697–702CrossRefPubMedGoogle Scholar
  75. 75.
    Lee Y, Nishizawa T, Yamashita K, Ishitani R, Nureki O (2015) Structural basis for the facilitative diffusion mechanism by SemiSWEET transporter. Nat Commun 6:6112CrossRefPubMedPubMedCentralGoogle Scholar
  76. 76.
    Xuan YH, Hu YB, Chen LQ, Sosso D, Ducat DC, Hou BH, Frommer WB (2013) Functional role of oligomerization for bacterial and plant SWEET sugar transporter family. Proc Natl Acad Sci 110:3685–3694CrossRefGoogle Scholar
  77. 77.
    Gray WM (2004) Hormonal regulation of plant growth and development. Plos Biol 2:311CrossRefGoogle Scholar
  78. 78.
    Jameson PE, Dhandapani P, Novak O, Song J (2016) Cytokinins and expression of SWEET, SUT, CWINV and AAP genes increase as pea seeds germinate. Int J Mol Sci 17:12CrossRefGoogle Scholar
  79. 79.
    Engel ML, Holmes-Davis R, McCormick S (2005) Green sperm. Identification of male gamete promoters in Arabidopsis. Plant Physiol 138:2124–2133CrossRefPubMedPubMedCentralGoogle Scholar
  80. 80.
    Baker RF, Leach KA, Braun DM (2012) SWEET as sugar: new sucrose effluxers in plants. Mol Plant 5:766–768CrossRefPubMedGoogle Scholar
  81. 81.
    Li T, Liu B, Spalding MH, Weeks DP, Yang B (2012) High-efficiency TALEN-based gene editing produces disease-resistant rice. Nat Biotechnol 30:390–392CrossRefPubMedGoogle Scholar

Copyright information

© Springer Nature B.V. 2019

Authors and Affiliations

  • Tinku Gautam
    • 1
  • Gautam Saripalli
    • 1
  • Vijay Gahlaut
    • 2
  • Anuj Kumar
    • 3
  • P. K. Sharma
    • 1
  • H. S. Balyan
    • 1
  • P. K. Gupta
    • 1
    Email author
  1. 1.Department of Genetics and Plant BreedingCh. Charan Singh UniversityMeerutIndia
  2. 2.Department of Plant Molecular BiologyUniversity of Delhi South CampusNew DelhiIndia
  3. 3.Advance Center for Computational & Applied BiotechnologyUttarakhand Council for Biotechnology (UCB)DehradunIndia

Personalised recommendations