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Sugar transporters in Fabaceae, featuring SUT MST and SWEET families of the model plant Medicago truncatula and the agricultural crop Pisum sativum


Autoři: Joan Doidy aff001;  Ugo Vidal aff001;  Rémi Lemoine aff001
Působiště autorů: Université de Poitiers, UMR CNRS 7267, EBI "Ecologie et Biologie des Interactions", Poitiers, France aff001
Vyšlo v časopise: PLoS ONE 14(9)
Kategorie: Research Article
prolekare.web.journal.doi_sk: https://doi.org/10.1371/journal.pone.0223173

Souhrn

Sugar transporters play a crucial role for plant productivity, as they coordinate sugar fluxes from source leaf towards sink organs (seed, fruit, root) and regulate the supply of carbon resources towards the microorganisms of the rhizosphere (bacteria and fungi). Thus, sugar fluxes mediated by SUT (sucrose transporters), MST (monosaccharide transporters) and SWEET (sugar will eventually be exported transporters) families are key determinants of crop yield and shape the microbial communities living in the soil. In this work, we performed a systematic search for sugar transporters in Fabaceae genomes, focusing on model and agronomical plants. Here, we update the inventory of sugar transporter families mining the latest version of the Medicago truncatula genome and identify for the first time SUT MST and SWEET families of the agricultural crop Pisum sativum. The sugar transporter families of these Fabaceae species comprise respectively 7 MtSUT 7 PsSUT, 72 MtMST 59 PsMST and 26 MtSWEET 22 PsSWEET. Our comprehensive phylogenetic analysis sets a milestone for the scientific community, as we propose a new and simple nomenclature to correctly name SUT MST and SWEET families. Then, we searched for transcriptomic data available for our gene repertoire. We show that several clusters of homologous genes are co-expressed in different organs, suggesting that orthologous sugar transporters may have a conserved function. We focused our analysis on gene candidates that may be involved in remobilizing resources during flowering, grain filling and in allocating carbon towards roots colonized by arbuscular mycorrhizal fungi and Rhizobia. Our findings open new perspectives for agroecological applications in legume crops, as for instance improving the yield and quality of seed productions and promoting the use of symbiotic microorganisms.

Klíčová slova:

Plant genomics – Genomic medicine – Legumes – Arabidopsis thaliana – Fabaceae – Peas – Medicago – Sucrose


Zdroje

1. De Ron AM. Grain Legumes. Springer-Verlag New York ed: Springer-Verlag New York; 2015. 438 p.

2. Stagnari F, Maggio A, Galieni A, Pisante M. Multiple benefits of legumes for agriculture sustainability: an overview. Chemical and Biological Technologies in Agriculture. 2017;4(1):2.

3. Wezel A, Casagrande M, Celette F, Vian J-F, Ferrer A, Peigné J. Agroecological practices for sustainable agriculture. A review. Agronomy for Sustainable Development. 2014;34(1):1–20.

4. Duchene O, Vian J-F, Celette F. Intercropping with legume for agroecological cropping systems: Complementarity and facilitation processes and the importance of soil microorganisms. A review. Agriculture, Ecosystems & Environment. 2017;240:148–61.

5. Hennion N, Durand M, Vriet C, Doidy J, Maurousset L, Lemoine R, et al. Sugars en route to the roots. Transport, metabolism and storage within plant roots and towards microorganisms of the rhizosphere. Physiologia Plantarum. 2018;0(0).

6. Sosso D, Luo D, Li Q-B, Sasse J, Yang J, Gendrot G, et al. Seed filling in domesticated maize and rice depends on SWEET-mediated hexose transport. Nat Genet. 2015;47(12):1489–93. doi: 10.1038/ng.3422 26523777

7. Chen LQ, Hou BH, Lalonde S, Takanaga H, Hartung ML, Qu XQ, et al. Sugar transporters for intercellular exchange and nutrition of pathogens. Nature. 2010;468(7323):527–32. doi: 10.1038/nature09606 21107422

8. Eom J-S, Chen L-Q, Sosso D, Julius BT, Lin IW, Qu X-Q, et al. SWEETs, transporters for intracellular and intercellular sugar translocation. Current Opinion in Plant Biology. 2015;25:53–62. doi: 10.1016/j.pbi.2015.04.005 25988582

9. Jeena GS, Kumar S, Shukla RK. Structure, evolution and diverse physiological roles of SWEET sugar transporters in plants. Plant molecular biology. 2019.

10. Wang L, Patrick JW, Ruan Y-L. Live Long and Prosper: Roles of Sugar and Sugar Polymers in Seed Vigor. Molecular Plant. 2018;11(1):1–3. doi: 10.1016/j.molp.2017.12.012 29274385

11. Riesmeier JW, Willmitzer L, Frommer WB. Isolation and characterization of a sucrose carrier cDNA from spinach by functional expression in yeast. EMBO Journal. 1992;11(13):4705–13. 1464305

12. Peng D, Gu X, Xue L, Leebens-Mack JH, Tsai C-J. Bayesian phylogeny of sucrose transporters: Ancient origins, differential expansion and convergent evolution in monocots and dicots. Frontiers in Plant Science. 2014;5. doi: 10.3389/fpls.2014.00005

13. Buttner M. The monosaccharide transporter(-like) gene family in Arabidopsis. FEBS Letters. 2007;581(12):2318–24. doi: 10.1016/j.febslet.2007.03.016 17379213

14. Johnson DA, Thomas MA. The monosaccharide transporter gene family in Arabidopsis and rice: A history of duplications, adaptive evolution, and functional divergence. Molecular Biology and Evolution. 2007;24(11):2412–23. doi: 10.1093/molbev/msm184 17827171

15. Doidy J, Grace E, Kühn C, Simon-Plas F, Casieri L, Wipf D. Sugar transporters in plants and in their interactions with fungi. Trends in Plant Science. 2012;17(7):413–22. doi: 10.1016/j.tplants.2012.03.009 22513109

16. Patil G, Valliyodan B, Deshmukh R, Prince S, Nicander B, Zhao M, et al. Soybean (Glycine max) SWEET gene family: insights through comparative genomics, transcriptome profiling and whole genome re-sequence analysis. BMC Genomics. 2015;16(1):1–16.

17. Kryvoruchko IS, Sinharoy S, Torres-Jerez I, Sosso D, Pislariu CI, Guan D, et al. MtSWEET11, a Nodule-Specific Sucrose Transporter of Medicago truncatula. Plant Physiology. 2016;171(1):554–65. doi: 10.1104/pp.15.01910 27021190

18. Doidy J, van Tuinen D, Lamotte O, Corneillat M, Alcaraz G, Wipf D. The Medicago truncatula sucrose transporter family. Characterization and implication of key members in carbon partitioning towards arbuscular mycorrhizal fungi. Molecular Plant. 2012: doi: 10.1093/mp/sss079 22930732

19. Zhou YC, Qu HX, Dibley KE, Offler CE, Patrick JW. A suite of sucrose transporters expressed in coats of developing legume seeds includes novel pH-independent facilitators. The Plant Journal. 2007;49(4):750–64. doi: 10.1111/j.1365-313X.2006.03000.x 17253986

20. Zhou Y, Chan K, Wang TL, Hedley CL, Offler CE, Patrick JW. Intracellular sucrose communicates metabolic demand to sucrose transporters in developing pea cotyledons. Journal of experimental botany. 2009;60(1):71–85. doi: 10.1093/jxb/ern254 18931350

21. Dhandapani P, Song J, Novak O, Jameson PE. Infection by Rhodococcus fascians maintains cotyledons as a sink tissue for the pathogen. Annals of Botany. 2016;119(5):841–52.

22. Krishnakumar V, Kim M, Rosen BD, Karamycheva S, Bidwell SL, Tang H, et al. MTGD: The Medicago truncatula Genome Database. Plant and Cell Physiology. 2014;56(1):e1–e. doi: 10.1093/pcp/pcu179 25432968

23. Young ND, Debelle F, Oldroyd GED, Geurts R, Cannon SB, Udvardi MK, et al. The Medicago genome provides insight into the evolution of rhizobial symbioses. Nature. 2011;480:520–4. doi: 10.1038/nature10625 22089132

24. Alves-Carvalho S, Aubert G, Carrère S, Cruaud C, Brochot A-L, Jacquin F, et al. Full-length de novo assembly of RNA-seq data in pea (Pisum sativum L.) provides a gene expression atlas and gives insights into root nodulation in this species. The Plant Journal. 2015;84(1):1–19. doi: 10.1111/tpj.12967 26296678

25. 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(D1):D1178–D86.

26. Dash S, Campbell JD, Cannon EKS, Cleary AM, Huang W, Kalberer SR, et al. Legume information system (LegumeInfo.org): a key component of a set of federated data resources for the legume family. Nucleic Acids Res. 2016;44(D1):D1181–D8. doi: 10.1093/nar/gkv1159 26546515

27. Hall T. BioEdit: A User-Friendly Biological Sequence Alignment Editor and Analysis Program for Windows 95/98/NT1999. 95–8 p.

28. Kumar S, Stecher G, Tamura K. MEGA7: Molecular Evolutionary Genetics Analysis Version 7.0 for Bigger Datasets. Molecular Biology and Evolution. 2016;33(7):1870–4. doi: 10.1093/molbev/msw054 27004904

29. Jones DT, Taylor WR, Thornton JM. The rapid generation of mutation data matrices from protein sequences. Bioinformatics. 1992;8(3):275–82.

30. He J, Benedito VA, Wang M, Murray JD, Zhao PX, Tang Y, et al. The Medicago truncatula gene expression atlas web server. BMC Bioinformatics. 2009;10:441-. doi: 10.1186/1471-2105-10-441 20028527

31. Benedito VA, Torres-Jerez I, Murray JD, Andriankaja A, Allen S, Kakar K, et al. A gene expression atlas of the model legume Medicago truncatula. The Plant Journal. 2008;55(3):504–13. doi: 10.1111/j.1365-313X.2008.03519.x 18410479

32. Ruffel S, Freixes S, Balzergue S, Tillard P, Jeudy C, Martin-Magniette ML, et al. Systemic signaling of the plant nitrogen status triggers specific transcriptome responses depending on the nitrogen source in Medicago truncatula. Plant physiology. 2008;146(4):2020–35. doi: 10.1104/pp.107.115667 18287487

33. Hogekamp C, Arndt D, Pereira P, Becker JD, Hohnjec N, Küster H. Laser-microdissection unravels cell-type specific transcription in arbuscular mycorrhizal roots, including CAAT-box TF gene expression correlating with fungal contact and spread. Plant Physiology. 2011:published October 26, 2011, doi: 10.1104/pp.111.186635

34. Saeed A, Sharov V, White J, Li J, Liang W, Bhagabati N, et al. TM4: a free, open-source system for microarray data management and analysis. Biotechniques. 2003;34(2).

35. Kreplak J, Madoui M-A, Cápal P, Novák P, Labadie K, Aubert G, et al. A reference genome for pea provides insight into legume genome evolution. Nature Genetics. 2019;51(9):1411–22. doi: 10.1038/s41588-019-0480-1 31477930

36. Lalonde S, Frommer WB. SUT sucrose and MST monosaccharide transporter inventory of the Selaginella genome. Frontiers in Plant Science. 2012;3. doi: 10.3389/fpls.2012.00003

37. Overvoorde P, Frommer W, Grimes H. A Soybean Sucrose Binding Protein Independently Mediates Nonsaturable Sucrose Uptake in Yeast1996. 271–80 p.

38. Aldape MJ, Elmer AM, Chao WS, Grimes HD. Identification and characterization of a sucrose transporter isolated from the developing cotyledons of soybean. Archives of Biochemistry and Biophysics. 2003;409(2):243–50. doi: 10.1016/s0003-9861(02)00631-8 12504891

39. Weber H, Borisjuk L, Heim U, Sauer N, Wobus U. A role for sugar transporters during seed development: molecular characterization of a hexose and a sucrose carrier in fava bean seeds. The Plant Cell. 1997;9(6):895–908. doi: 10.1105/tpc.9.6.895 9212465

40. Tegeder M, Wang XD, Frommer WB, Offler CE, Patrick JW. Sucrose transport into developing seeds of Pisum sativum L. Plant Journal. 1999;18(2):151–61. doi: 10.1046/j.1365-313x.1999.00439.x 10363367

41. Flemetakis E, Dimou M, Cotzur D, Efrose RC, Aivalakis G, Colebatch G, et al. A sucrose transporter, LjSUT4, is up‐regulated during Lotus japonicus nodule development*. Journal of experimental botany. 2003;54(388):1789–91. doi: 10.1093/jxb/erg179 12754265

42. Reinders A, Sivitz A, Starker C, Gantt J, Ward J. Functional analysis of LjSUT4, a vacuolar sucrose transporter from Lotus japonicus. Plant molecular biology. 2008;68(3):289–99. doi: 10.1007/s11103-008-9370-0 18618272

43. Zhang C, Turgeon R. Downregulating the sucrose transporter VpSUT1 in Verbascum phoeniceum does not inhibit phloem loading. Proceedings of the National Academy of Sciences of the United States of America. 2009;106(44):18849–54. doi: 10.1073/pnas.0904189106 19846784

44. Gottwald JR, Krysan PJ, Young JC, Evert RF, Sussman MR. Genetic evidence for the in planta role of phloem-specific plasma membrane sucrose transporters. Proceedings of the National Academy of Sciences of the United States of America. 2000;97(25):13979–84. doi: 10.1073/pnas.250473797 11087840

45. Rennie EA, Turgeon R. A comprehensive picture of phloem loading strategies. Proceedings of the National Academy of Sciences of the United States of America. 2009;106(33):14162–7. doi: 10.1073/pnas.0902279106 19666555

46. Barker L, Kuhn C, Weise A, Schulz A, Gebhardt C, Hirner B, et al. SUT2, a putative sucrose sensor in sieve elements. Plant Cell. 2000;12(7):1153–64. doi: 10.1105/tpc.12.7.1153 10899981

47. Hackel A, Schauer N, Carrari F, Fernie A, Grimm B, Kühn C. Sucrose transporter LeSUT1 and LeSUT2 inhibition affects tomato fruit development in different ways. The Plant Journal. 2006;45(2):180–92. doi: 10.1111/j.1365-313X.2005.02572.x 16367963

48. Bitterlich M, Krügel U, Boldt-Burisch K, Franken P, Kühn C. The sucrose transporter SlSUT2 from tomato interacts with brassinosteroid functioning and affects arbuscular mycorrhiza formation. The Plant Journal. 2014;78(5):877–89. doi: 10.1111/tpj.12515 24654931

49. Schneider S, Hulpke S, Schulz A, Yaron I, Höll J, Imlau A, et al. Vacuoles release sucrose via tonoplast-localised SUC4-type transporters. Plant Biology. 2011;14(2):325–36. doi: 10.1111/j.1438-8677.2011.00506.x 21972845

50. Komarova NY, Meier S, Meier A, Grotemeyer MS, Rentsch D. Determinants for Arabidopsis peptide transporter targeting to the tonoplast or plasma membrane. Traffic. 2012: doi: 10.1111/j.600-0854.2012.01370.x

51. Léran S, Varala K, Boyer J-C, Chiurazzi M, Crawford N, Daniel-Vedele F, et al. A unified nomenclature of NITRATE TRANSPORTER 1/PEPTIDE TRANSPORTER family members in plants. Trends in Plant Science. 2014;19(1):5–9. doi: 10.1016/j.tplants.2013.08.008 24055139

52. Harrison MJ. A sugar transporter from Medicago truncatula: Altered expression pattern in roots during vesicular-arbuscular (VA) mycorrhizal associations. The Plant Journal. 1996;9(4):491–503. doi: 10.1046/j.1365-313x.1996.09040491.x 8624512

53. An J, Zeng T, Ji C, de Graaf S, Zheng Z, Xiao TT, et al. A Medicago truncatula SWEET transporter implicated in arbuscule maintenance during arbuscular mycorrhizal symbiosis. New Phytologist. 2019;0(ja).

54. Sugiyama A, Saida Y, Yoshimizu M, Takanashi K, Sosso D, Frommer WB, et al. Molecular Characterization of LjSWEET3, a Sugar Transporter in Nodules of Lotus japonicus. Plant and Cell Physiology. 2016;58(2):298–306.

55. Sun MX, Huang XY, Yang J, Guan YF, Yang ZN. Arabidopsis RPG1 is important for primexine deposition and functions redundantly with RPG2 for plant fertility at the late reproductive stage. Plant reproduction. 2013;26(2):83–91. doi: 10.1007/s00497-012-0208-1 23686221

56. Chen L-Q, Lin IW, Qu X-Q, Sosso D, McFarlane HE, Londoño A, et al. A Cascade of Sequentially Expressed Sucrose Transporters in the Seed Coat and Endosperm Provides Nutrition for the Arabidopsis Embryo. The Plant Cell. 2015;27(3):607–19. doi: 10.1105/tpc.114.134585 25794936

57. 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. doi: 10.1126/science.1213351 22157085

58. Klemens PAW, Patzke K, Deitmer J, Spinner L, Le Hir R, Bellini C, et al. Overexpression of the Vacuolar Sugar Carrier AtSWEET16 Modifies Germination, Growth, and Stress Tolerance in Arabidopsis. Plant Physiology. 2013;163(3):1338–52. doi: 10.1104/pp.113.224972 24028846

59. Guo W-J, Nagy R, Chen H-Y, Pfrunder S, Yu Y-C, Santelia D, et al. SWEET17, a facilitative transporter, mediates fructose transport across the tonoplast of Arabidopsis roots and leaves. Plant physiology. 2014;164(2):777–89. doi: 10.1104/pp.113.232751 24381066

60. Ainsworth E, Bush D. Carbohydrate export from the leaf—A highly regulated process and target to enhance photosynthesis and productivity. Plant Physiology. 2010;155:64–9. doi: 10.1104/pp.110.167684 20971857

61. 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. Proceedings of the National Academy of Sciences. 2013;110(39):E3685–E94.

62. Ma Q-J, Sun M-H, Kang H, Lu J, You C-X, Hao Y-J. A CIPK protein kinase targets sucrose transporter MdSUT2.2 at Ser254 for phosphorylation to enhance salt tolerance. Plant, Cell & Environment. 2019;42(3):918–30.

63. Kalliampakou KI, Kouri ED, Boleti H, Pavli O, Maurousset L, Udvardi MK, et al. Cloning and functional characterization of LjPLT4, a plasma membrane xylitol H+- symporter from Lotus japonicus. Molecular Membrane Biology. 2011;28(1):1–13. doi: 10.3109/09687688.2010.500626 21219252

64. Slewinski TL. Diverse Functional Roles of Monosaccharide Transporters and their Homologs in Vascular Plants: A Physiological Perspective. Molecular Plant. 2011;4(4):641–62. doi: 10.1093/mp/ssr051 21746702

65. Lin IW, Sosso D, Chen L-Q, Gase K, Kim S-G, Kessler D, et al. Nectar secretion requires sucrose phosphate synthases and the sugar transporter SWEET9. Nature. 2014;508:546. doi: 10.1038/nature13082 24670640

66. Aluri S, Buttner M. Identification and functional expression of the Arabidopsis thaliana vacuolar glucose transporter 1 and its role in seed germination and flowering. Proceedings of the National Academy of Sciences of the United States of America. 2007;104(7):2537–42. doi: 10.1073/pnas.0610278104 17284600

67. Patzke K, Prananingrum P, Klemens PAW, Trentmann O, Rodrigues CM, Keller I, et al. The Plastidic Sugar Transporter pSuT Influences Flowering and Affects Cold Responses. Plant Physiology. 2019;179(2):569–87. doi: 10.1104/pp.18.01036 30482788

68. Yang J, Luo D, Yang B, Frommer WB, Eom J-S. SWEET11 and 15 as key players in seed filling in rice. New Phytologist. 2018;218(2):604–15. doi: 10.1111/nph.15004 29393510

69. Wang S, Yokosho K, Guo R, Whelan J, Ruan Y-L, Ma JF, et al. The Soybean Sugar Transporter GmSWEET15 Mediates Sucrose Export from Endosperm to Early Embryo. Plant Physiology. 2019;180(4):2133–41. doi: 10.1104/pp.19.00641 31221732

70. Gomez SK, Javot H, Deewatthanawong P, Torres-Jerez I, Tang Y, Blancaflor E, et al. Medicago truncatula and Glomus intraradices gene expression in cortical cells harboring arbuscules in the arbuscular mycorrhizal symbiosis. BMC Plant Biology. 2009;9(1):10.

71. Gaude N, Bortfeld S, Duensing N, Lohse M, Krajinski F. Arbuscule-containing and non-colonized cortical cells of mycorrhizal roots undergo a massive and specific reprogramming during arbuscular mycorrhizal development. The Plant Journal. 2011;69(3):510–28. doi: 10.1111/j.1365-313X.2011.04810.x 21978245

72. Lemonnier P, Gaillard C, Veillet F, Verbeke J, Lemoine R, Coutos-Thévenot P, et al. Expression of Arabidopsis sugar transport protein STP13 differentially affects glucose transport activity and basal resistance to Botrytis cinerea. Plant molecular biology. 2014;85(4):473–84.

73. Yamada K, Saijo Y, Nakagami H, Takano Y. Regulation of sugar transporter activity for antibacterial defense in Arabidopsis. Science. 2016;354(6318):1427–30. doi: 10.1126/science.aah5692 27884939

74. Gamas P, Niebel FDC, Lescure N, Cullimore JV. Use of a subtractive hybridization approach to identify new Medicago truncatula genes induced during root nodule development. Molecular Plant-Microbe Interactions. 1996;9(4):233–42. 8634476

75. Manck-Götzenberger J, Requena N. Arbuscular mycorrhiza symbiosis induces a major transcriptional reprogramming of the potato SWEET sugar transporter family. Frontiers in Plant Science. 2016;7.

76. Kafle A, Garcia K, Wang X, Pfeffer PE, Strahan GD, Bücking H. Nutrient demand and fungal access to resources control the carbon allocation to the symbiotic partners in tripartite interactions of Medicago truncatula. Plant, Cell & Environment. 2019;42(1):270–84.

77. Oldroyd GED. Speak, friend, and enter: signalling systems that promote beneficial symbiotic associations in plants. Nature Reviews Microbiology. 2013;11:252. doi: 10.1038/nrmicro2990 23493145

78. Gianinazzi S, Gollotte A, Binet M-N, van Tuinen D, Redecker D, Wipf D. Agroecology: the key role of arbuscular mycorrhizas in ecosystem services. Mycorrhiza. 2010;20(8):519–30. doi: 10.1007/s00572-010-0333-3 20697748

79. Chaintreuil C, Rivallan R, Bertioli DJ, Klopp C, Gouzy J, Courtois B, et al. A gene-based map of the Nod factor-independent Aeschynomene evenia sheds new light on the evolution of nodulation and legume genomes. DNA Research. 2016;23(4):365–76. doi: 10.1093/dnares/dsw020 27298380

80. Bruneau A, J. Doyle J, Herendeen P, Hughes C, Kenicer G, Lewis G, et al. Legume phylogeny and classification in the 21st century: Progress, prospects and lessons for other species-rich clades2013. 217–48 p.

81. Schmid M, Davison TS, Henz SR, Pape UJ, Demar M, Vingron M, et al. A gene expression map of Arabidopsis thaliana development. Nature Genetics. 2005;37(5):501–6. doi: 10.1038/ng1543 15806101


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