Co-option of developmentally regulated plant SWEET transporters for pathogen nutrition and abiotic stress tolerance

IUBMB Life

Volumn 67, Issue 7, 2015, Pages 461-471

  Chandran, Divya ^a  

^a REGIONAL CENTRE FOR BIOTECHNOLOGY   (India)

Author keywords

biotrophy; Medicago truncatula; necrotrophy; sugar transporter; symbiosis; TAL effectors

Indexed keywords

ABIOTIC STRESS; BARREL MEDIC; GENE ACTIVATION; GENE EXPRESSION; GLUCOSE TRANSPORT; HEXOSE TRANSPORT; LEAF SENESCENCE; NONHUMAN; NUTRITION; PHYLOGENY; PLANT DEVELOPMENT; PLANT GROWTH; POLLEN DEVELOPMENT; REVIEW; SUGAR TRANSPORT; GENE EXPRESSION REGULATION; GENETICS; GROWTH, DEVELOPMENT AND AGING; HOST PATHOGEN INTERACTION; METABOLISM; PHYSIOLOGICAL STRESS; PHYSIOLOGY; PLANT DISEASE; POLLEN;

MEDICAGO TRUNCATULA;

ARABIDOPSIS PROTEIN; CARBOHYDRATE; CARRIER PROTEIN; SWEET11 PROTEIN, ARABIDOPSIS; SWEET12 PROTEIN, ARABIDOPSIS; VEGETABLE PROTEIN;

ARABIDOPSIS PROTEINS; CARBOHYDRATES; GENE EXPRESSION REGULATION, PLANT; HOST-PATHOGEN INTERACTIONS; MEMBRANE TRANSPORT PROTEINS; PLANT DEVELOPMENT; PLANT DISEASES; PLANT PROTEINS; POLLEN; STRESS, PHYSIOLOGICAL;

EID: 84937966992     PISSN: 15216543     EISSN: 15216551     Source Type: Journal    
DOI: 10.1002/iub.1394     Document Type: Review

References (56)

1. Talbot, N. J., (2010) Cell biology: raiding the sweet shop. Nature. 468, 510-511.
2. Chen, L. Q., (2014) SWEET sugar transporters for phloem transport and pathogen nutrition. New Phytol. 201, 1150-1155.
3. Chen, L. Q., Hou, B. H., Lalonde, S., Takanaga, H., Hartung, M. L., et al., (2010) Sugar transporters for intercellular exchange and nutrition of pathogens. Nature. 468, 527-532.
4. Chen, L. Q., Qu, X. Q., Hou, B. H., Sosso, D., Osorio, S., et al., (2012) Sucrose efflux mediated by SWEET proteins as a key step for phloem transport. Science. 335, 207-211.
5. Gamas, P., Niebel Fde, C., Lescure, N., and, 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, 233-242.
6. Artero, R. D., Terol-Alcayde, J., Paricio, N., Ring, J., Bargues, M., et al., (1998) Saliva, a new Drosophila gene expressed in the embryonic salivary glands with homologues in plants and vertebrates. Mech Dev. 75, 159-162.
7. Xuan, Y. H., Hu, Y. B., Chen, L. Q., Sosso, D., Ducat, D. C., et al., (2013) Functional role of oligomerization for bacterial and plant SWEET sugar transporter family. Proc. Natl. Acad. Sci. USA 110, E3685-E3694.
8. Xu, Y., Tao, Y., Cheung, L. S., Fan, C., Chen, L. Q., et al., (2014) Structures of bacterial homologues of SWEET transporters in two distinct conformations. Nature. 515, 448-452.
9. Wang, J., Yan, C., Li, Y., Hirata, K., Yamamoto, M., et al., (2014) Crystal structure of a bacterial homologue of SWEET transporters. Cell Res. 24, 1486-1489.
10. Chandran, D., Reinders, A., and, Ward, J. M., (2003) Substrate specificity of the Arabidopsis thaliana sucrose transporter AtSUC2. J. Biol. Chem. 278, 44320-44325.
11. Schwacke, R., Schneider, A., van der Graaff, E., Fischer, K., Catoni, E., et al., (2003) ARAMEMNON, a novel database for Arabidopsis integral membrane proteins. Plant Physiol. 131, 16-26.
12. Tang, H., Krishnakumar, V., Bidwell, S., Rosen, B., Chan, A., et al., (2014) An improved genome release (version Mt4.0) for the model legume Medicago truncatula. BMC Genomics 15, 312.
13. Zhou, Y., Liu, L., Huang, W., Yuan, M., Zhou, F., et al., (2014) Overexpression of OsSWEET5 in rice causes growth retardation and precocious senescence. PLoS One 9, e94210.
14. Chardon, F., Bedu, M., Calenge, F., Klemens, P. A., Spinner, L., et al., (2013) Leaf fructose content is controlled by the vacuolar transporter SWEET17 in Arabidopsis. Curr Biol. 23, 697-702.
15. Klemens, P. A., Patzke, K., Deitmer, J., Spinner, L., Le Hir, R., et al., (2013) Overexpression of the vacuolar sugar carrier AtSWEET16 modifies germination, growth, and stress tolerance in Arabidopsis. Plant Physiol. 163, 1338-1352.
16. Guo, W. J., Nagy, R., Chen, H. Y., Pfrunder, S., Yu, Y. C., et al., (2014) SWEET17, a facilitative transporter, mediates fructose transport across the tonoplast of Arabidopsis roots and leaves. Plant Physiol. 164, 777-789.
17. Chu, Z., Fu, B., Yang, H., Xu, C., Li, Z., et al., (2006) Targeting xa13, a recessive gene for bacterial blight resistance in rice. Theor. Appl. Genet. 112, 455-461.
18. Lin, I. W., Sosso, D., Chen, L. Q., Gase, K., Kim, S. G., et al., (2014) Nectar secretion requires sucrose phosphate synthases and the sugar transporter SWEET9. Nature. 508, 546-549.
19. Ge, Y. X., Angenent, G. C., Wittich, P. E., Peters, J., Franken, J., et al., (2000) NEC1, a novel gene, highly expressed in nectary tissue of Petunia hybrida. Plant J. 24, 725-734.
20. Chen, L. Q., Lin, W. I., Qu, X. Q., Sosso, D., McFarlane, H. E., et al., (2015) A cascade of sequentially expressed sucrose transporters in the seed coat and endosperm provides nutrition for the Arabidopsis embryo. Plant Cell, epub ahead of print March 20.
21. Guan, Y. F., Huang, X. Y., Zhu, J., Gao, J. F., Zhang, H. X., et al., (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 Physiol. 147, 852-863.
22. Sun, M. X., Huang, X. Y., Yang, J., Guan, Y. F., and, 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 Reprod. 26, 83-91.
23. Yang, B., Sugio, A., and, White, F. F., (2006) Os8N3 is a host disease-susceptibility gene for bacterial blight of rice. Proc. Natl. Acad. Sci. USA 103, 10503-10508.
24. Engel, M. L., Holmes-Davis, R., and, McCormick, S., (2005) Green sperm. Identification of male gamete promoters in Arabidopsis. Plant Physiol. 138, 2124-2133.
25. Chakraborty, S., and, Newton, A. C., (2011) Climate change, plant diseases and food security: an overview. Plant Pathol. 60, 2-14.
26. Liu, Q., Yuan, M., Zhou, Y., Li, X., Xiao, J., et al., (2011) A paralog of the MtN3/saliva family recessively confers race-specific resistance to Xanthomonas oryzae in rice. Plant Cell Environ. 34, 1958-1969.
27. Yu, Y., Streubel, J., Balzergue, S., Champion, A., Boch, J., et al., (2011) Colonization of rice leaf blades by an African strain of Xanthomonas oryzae pv. oryzae depends on a new TAL effector that induces the rice nodulin-3 Os11N3 gene. Mol. Plant Microbe Interact. 24, 1102-1113.
28. Antony, G., Zhou, J., Huang, S., Li, T., Liu, B., et al., (2010) Rice xa13 recessive resistance to bacterial blight is defeated by induction of the disease susceptibility gene Os-11N3. Plant Cell 22, 3864-3876.
29. Bogdanove, A. J., (2014) Principles and applications of TAL effectors for plant physiology and metabolism. Curr. Opin. Plant Biol. 19, 99-104.
30. Römer, P., Recht, S., Strauss, T., Elsaesser, J., Schornack, S., et al., (2010) Promoter elements of rice susceptibility genes are bound and activated by specific TAL effectors from the bacterial blight pathogen, Xanthomonas oryzae pv. oryzae. New Phytol. 187, 1048-1057.
31. Verdier, V., Triplett, L. R., Hummel, A. W., Corral, R., Cernadas, R. A., et al., (2012) Transcription activator-like (TAL) effectors targeting OsSWEET genes enhance virulence on diverse rice (Oryza sativa) varieties when expressed individually in a TAL effector-deficient strain of Xanthomonas oryzae. New Phytol. 196, 1197-1207.
32. Li, T., Huang, S., Zhou, J., and, Yang, B., (2013) Designer TAL effectors induce disease susceptibility and resistance to Xanthomonas oryzae pv. oryzae in rice. Mol. Plant. 6, 781-789.
33. Streubel, J., Pesce, C., Hutin, M., Koebnik, R., Boch, J., et al., (2013) Five phylogenetically close rice SWEET genes confer TAL effector-mediated susceptibility to Xanthomonas oryzae pv. oryzae. New Phytol. 200, 808-819.
34. Cohn, M., Bart, R. S., Shybut, M., Dahlbeck, D., Gomez, M., et al., (2014) Xanthomonas axonopodis virulence is promoted by a transcription activator-like effector-mediated induction of a SWEET sugar transporter in Cassava. Mol. Plant Microbe Interact. 27, 1186-1198.
35. Hu, Y., Zhang, J., Jia, H., Sosso, D., Li, T., et al., (2014) Lateral organ boundaries 1 is a disease susceptibility gene for citrus bacterial canker disease. Proc. Natl. Acad. Sci. USA 111, E521-E529.
36. Chong, J., Piron, M. C., Meyer, S., Merdinoglu, D., Bertsch, C., et al., (2014) The SWEET family of sugar transporters in grapevine: VvSWEET4 is involved in the interaction with Botrytis cinerea. J. Exp. Bot. 65, 6589-6601.
37. Perotto, S., Rodda, M., Benetti, A., Sillo, F., Ercole, E., et al., (2014) Gene expression in mycorrhizal orchid protocorms suggests a friendly plant-fungus relationship. Planta 239, 1337-1349.
38. Oliver, R. P., and, Ipcho, S. V., (2004) Arabidopsis pathology breathes new life into the necrotrophs-vs.-biotrophs classification of fungal pathogens. Mol. Plant Pathol. 5, 347-352.
39. Lee, S. J., and, Rose, J. K., (2010) Mediation of the transition from biotrophy to necrotrophy in hemibiotrophic plant pathogens by secreted effector proteins. Plant Signal Behav. 5, 769-772.
40. Micali, C., Göllner, K., Humphry, M., Consonni, C., and, Panstruga, R., (2008) The powdery mildew disease of Arabidopsis: a paradigm for the interaction between plants and biotrophic fungi. Arabidopsis Book. 6, e0115.
41. Chandran, D., Inada, N., Hather, G., Kleindt, C. K., and, Wildermuth, M. C., (2010) Laser microdissection of Arabidopsis cells at the powdery mildew infection site reveals site-specific processes and regulators. Proc. Natl. Acad. Sci. USA 107, 460-465.
42. Morkunas, I., and, Ratajczak, L., (2014) The role of sugar signaling in plant defense responses against fungal pathogens. Acta Physiol Plant 36, 1607-1619.
43. Ferrari, S., Galletti, R., Denoux, C., De Lorenzo, G., Ausubel, F. M., et al., (2007) Resistance to Botrytis cinerea induced in Arabidopsis by elicitors is independent of salicylic acid, ethylene, or jasmonate signaling but requires PHYTOALEXIN DEFICIENT3. Plant Physiol. 144, 367-379.
44. Yuan, M., Zhao, J., Huang, R., Li, X., Xiao, J., et al., (2014) Rice MtN3/saliva/SWEET gene family: evolution, expression profiling, and sugar transport. J. Int. Plant Biol. 56, 559-570.
45. Wildermuth, M. C., (2010) Modulation of host nuclear ploidy: a common mechanism of obligate plant biotrophs. Curr. Opin. Plant Biol. 13, 449-458.
46. Benedito, V. A., Torres-Jerez, I., Murray, J. D., Andriankaja, A., Allen, S., et al., (2008) A gene expression atlas of the model legume Medicago truncatula. Plant J. 55, 504-513.
47. He, J., Benedito, V. A., Wang, M., Murray, J. D., Zhao, P. X., et al., (2009) The Medicago truncatula gene expression atlas web server. BMC Bioinformatics 10, 441.
48. Yuanyuan, M., Yali, Z., Jiang, L., and, Hongbo, S., (2009) Roles of plant soluble sugars and their responses to plant cold stress. Afr. J. Biotechnol. 8, 2004-2010.
49. Seo, P. J., Park, J. M., Kang, S. K., Kim, S. G., and, Park, C. M., (2011) An Arabidopsis senescence-associated protein SAG29 regulates cell viability under high salinity. Planta 233, 189-200.
50. Fotopoulos, V., Gilbert, M. J., Pittman, J. K., Marvier, A. C., Buchanan, A. J., et al., (2003) The monosaccharide transporter gene, AtSTP4, and the cell-wall invertase, Atbetafruct1, are induced in Arabidopsis during infection with the fungal biotroph Erysiphe cichoracearum. Plant Physiol. 132, 821-829.
51. Hall, J. L., and, Williams, L. E., (2000) Assimilate transport and partitioning in fungal biotrophic interactions. Funct. Plant Biol. 27, 549-560.
52. Frugoli, J., and, Harris, J., (2001) Medicago truncatula on the move!. Plant Cell. 13, 458-463.
53. Akibode, S., and, Maredia, M., (2011). Global and regional trends in production, trade and consumption of food legume crops. Report.
54. Schroeder, J. I., Delhaize, E., Frommer, W. B., Guerinot, M. L., Harrison, M. J., et al., (2013) Using membrane transporters to improve crops for sustainable food production. Nature. 497, 60-66.
55. Li, C., Wei, J., Lin, Y., and, Chen, H., (2012) Gene silencing using the recessive rice bacterial blight resistance gene xa13 as a new paradigm in plant breeding. Plant Cell Rep. 31, 851-862.
56. Li, T., Liu, B., Spalding, M. H., Weeks, D. P., and, Yang, B., (2012) High-efficiency TALEN-based gene editing produces disease-resistant rice. Nat. Biotechnol. 30, 390-392.