Sugar homeostasis mediated by cell wall invertase GRAIN INCOMPLETE FILLING 1 (GIF1) plays a role in pre-existing and induced defence in rice

Molecular Plant Pathology

Volumn 15, Issue 2, 2014, Pages 161-173

  Sun, Li ^a,b   Yang, Dong lei ^b,c   Kong, Yu ^b   Chen, Ying ^b   Li, Xiao Zun ^b   Zeng, Long Jun ^b   Li, Qun ^b   Wang, Er Tao ^b   He, Zu Hua ^a,b  

^a ZHEJIANG UNIVERSITY   (China)

^b INSTITUTE OF PLANT PHYSIOLOGY AND ECOLOGY   (China)

^c INSTITUTE OF GEOLOGY AND GEOPHYSICS   (China)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIA (MICROORGANISMS); MAGNAPORTHE ORYZAE; XANTHOMONAS ORYZAE PV. ORYZAE;

BETA FRUCTOFURANOSIDASE; REACTIVE OXYGEN METABOLITE;

ARTICLE; CARBOHYDRATE METABOLISM; CELL WALL; ENZYMOLOGY; GENE EXPRESSION REGULATION; GENETICS; HOMEOSTASIS; MAGNAPORTHE; METABOLISM; MICROBIOLOGY; PATHOGENICITY; PLANT GENE; RICE; XANTHOMONAS;

BETA-FRUCTOFURANOSIDASE; CARBOHYDRATE METABOLISM; CELL WALL; GENE EXPRESSION REGULATION, PLANT; GENES, PLANT; HOMEOSTASIS; MAGNAPORTHE; ORYZA SATIVA; REACTIVE OXYGEN SPECIES; XANTHOMONAS;

EID: 84891739107     PISSN: 14646722     EISSN: 13643703     Source Type: Journal    
DOI: 10.1111/mpp.12078     Document Type: Article

References (63)

1. Asselbergh, B., Curvers, K., Francxa, S.C., Audenaert, K., Vuylsteke, M., Van Breusegem, F. and Höfte, M. (2007) Resistance to Botrytis cinerea in sitiens, an abscisic acid-deficient tomato mutant, involves timely production of hydrogen peroxide and cell wall modifications in the epidermis. Plant Physiol. 144, 1863-1877.
2. Berger, S., Sinha, A.K. and Roitsch, T. (2007) Plant physiology meets phytopathology: plant primary metabolism and plant pathogen interactions. J. Exp. Bot. 58, 4019-4026.
3. Boller, T. and He, S.Y. (2009) Innate immunity in plants: an arms race between pattern recognition receptors in plants and effectors in microbial pathogens. Science, 324, 742-744.
4. Bolouri-Moghaddam, M.R. and Van den Ende, W. (2012) Sugars and plant innate immunity. J. Exp. Bot. 63, 3989-3998.
5. Bolouri-Moghaddam, M.R. and Van den Ende, W. (2013a) Sugars, the clock and transition to flowering. Front. Plant Sci. 4, 22.
6. Bolouri-Moghaddam, M.R. and Van den Ende, W. (2013b) Sweet immunity in the plant circadian regulatory network. J. Exp. Bot. 64, 1439-1449.
7. Bolouri-Moghaddam, M.R., Le Roy, K., Xiang, L., Rolland, F. and Van den Ende, W. (2010) Sugar signalling and antioxidant network connections in plant cells. FEBS J. 277, 2022-2037.
8. Bonfig, K.B., Gabler, A., Simon, U.K., Luschin-Ebengreuth, N., Hatz, M., Berger, S., Muhammad, N., Zeier, J., Sinha, A.K. and Roitsch, T. (2010) Post-translational derepression of invertase activity in source leaves via down-regulation of invertase inhibitor expression is part of the plant defense response. Mol. Plant, 3, 1037-1048.
9. Chen, F., Gao, M.J., Miao, Y.S., Yuan, Y.X., Wang, M.Y., Li, Q., Mao, B.Z., Jiang, L.W. and He, Z.H. (2010) Plasma membrane localization and potential endocytosis of constitutively expressed XA21 proteins in transgenic rice. Mol. Plant, 3, 917-926.
10. 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., Sommerville, S.C., Mudgett, M.B. and Frommer, W.B. (2010) Sugar transporters for intercellular exchange and nutrition of pathogens. Nature, 468, 527-532.
11. Chen, L.Q., Qu, X.Q., Hou, B.H., Sosso, D., Osorio, S., Fernie, A.R. and Frommer, W.B. (2012) Sucrose efflux mediated by SWEET proteins as a key step for phloem transport. Science, 335, 207-211.
12. Chisholm, S.T., Coaker, G., Day, B. and Staskawicz, B.J. (2006) Host-microbe interactions: shaping the evolution of the plant immune response. Cell, 124, 803-814.
13. Cho, J.I., Lee, S.K., Ko, S., Kim, H.K., Jun, S.H., Lee, Y.H., Bhoo, S.H., Lee, K.W., An, G., Hahn, T.R. and Jeon, J.S. (2005) Molecular cloning and expression analysis of the cell-wall invertase gene family in rice (Oryza sativa L.). Plant Cell Rep. 24, 225-236.
14. Chou, H.M., Bundock, N., Rolfe, S.A. and Scholes, J.D. (2000) Infection of Arabidopsis thaliana leaves with Albugo candida (white blister rust) causes a reprogramming of host metabolism. Mol. Plant Pathol. 1, 99-113.
15. Chu, Z., Yuan, M., Yao, J., Ge, X., Yuan, B., Xu, C., Li, X., Fu, B., Li, Z., Bennetzen, J.L., Zhang, Q. and Wang, S.P. (2006) Promoter mutations of an essential gene for pollen development result in disease resistance in rice. Genes Dev. 20, 1250-1255.
16. Couée, I., Sulmon, C., Gouesbet, G. and El Amrani, A. (2006) Involvement of soluble sugars in reactive oxygen species balance and responses to oxidative stress. J. Exp. Bot. 57, 449-459.
17. Delgado-Cerezo, M., Sánchez-Rodrígueza, C., Escuderoa, V., Miedesa, E., Fernándezc, P.V., Jordáa, L., Hernández-Blancoa, C., Sánchez-Valleta, A., Bednareke, P., Schulze-Leferte, P., Somervilleg, S., Estevezc, J.M., Perssonb, S. and Molinaa, A. (2012) Arabidopsis heterotrimeric G-protein regulates cell wall defense and resistance to necrotrophic fungi. Mol. Plant, 5, 98-114.
18. Djonović, S., Urbach, J.M., Drenkard, E., Bush, J., Feinbaum, R., Ausubel, J.L., Traficante, D., Risech, M., Kocks, C., Fischbach, M.A., Priebe, G.P. and Ausubel, F.M. (2013) Trehalose biosynthesis promotes Pseudomonas aeruginosa pathogenicity in plants. PLoS Pathog. 9, e1003217.
19. Dodds, P.N. and Rathjen, J.P. (2010) Plant immunity: towards an integrated view of plant-pathogen interactions. Nat. Rev. Genet. 11, 539-548.
20. Ellis, C. and Turner, J.G. (2001) The Arabidopsis mutant cev1 has constitutively active jasmonate and ethylene signal pathways and enhanced resistance to pathogens. Plant Cell, 13, 1025-1033.
21. Essmann, J., Schmitz-Thom, I., Schön, H., Sonnewald, S., Weis, E. and Scharte, J. (2008) RNA interference-mediated repression of cell wall invertase impairs defense in source leaves of tobacco. Plant Physiol. 147, 1288-1299.
22. Fotopoulos, V., Gilbert, M.J., Pittman, J.K., Marvier, A.C., Buchanon, A.J., Sauer, N., Hall, J.L. and Williams, L.E. (2003) The monosaccharide transporter gene, AtSTP4, and the cell wall invertase, AtBfruct1, are induced in Arabidopsis during infection with the fungal biotroph Erysiphe cichoracearum. Plant Physiol. 132, 821-829.
23. Gómez-Ariza, J., Campo, S., Rufat, M., Estopà, M., Messeguer, J., San Segundo, B. and Coca, M. (2007) Sucrose-mediated priming of plant defense responses and broad-spectrum disease resistance by overexpression of the maize pathogenesis-related PRms protein in rice plants. Mol. Plant-Microbe Interact. 20, 832-842.
24. Hao, P.Y., Liu, C.X., Wang, Y.Y., Chen, R.Z., Tang, M., Du, B., Zhu, L.L. and Hong, G.C. (2008) Herbivore-induced callose deposition on the sieve plates of rice: an important mechanism for host resistance. Plant Physiol. 146, 1810-1820.
25. Hématy, K., Cherk, C. and Somerville, S. (2009) Host-pathogen warfare at the plant cell wall. Curr. Opin. Plant Biol. 12, 406-413.
26. Herbers, K., Meuwly, P., Frommer, W.B., Metraux, J.P. and Sonnewald, U. (1996) Systemic acquired resistance mediated by the ectopic expression of invertase: possible hexose sensing in the secretory pathway. Plant Cell, 8, 793-803.
27. Hernández-Blanco, C., Feng, D.X., Hu, J., Sánchez-Vallet, A., Deslandes, L., Llorente, F., Berrocal-Lobo, M., Keller, H., Barlet, X., Sánchez-Rodríguez, C., Anderson, L.K., Somerville, S., Marco, Y. and Molina, A. (2007) Impairment of cellulose synthases required for Arabidopsis secondary cell wall formation enhances disease resistance. Plant Cell, 19, 890-903.
28. Hückelhoven, R. (2007) Cell wall-associated mechanisms of disease resistance and susceptibility. Annu. Rev. Phytopathol. 45, 101-127.
29. Jones, J.D. and Dangl, J.L. (2006) The plant immune system. Nature, 444, 323-329.
30. 2 in transgenic rice leads to cell death and enhanced resistance to both bacterial and fungal pathogens. Transgenic Res. 12, 577-586.
31. Kano, A., Gomi, K., Yamasaki-Kokudo, Y., Satoh, M., Fukumoto, T., Ohtani, K., Tajima, S., Izumori, K., Tanaka, K., Ishi, Y., Tada, Y., Nishizawa, Y. and Akimitsu, K. (2010) A rare sugar, d-allose, confers resistance to rice bacterial blight with upregulation of defense-related genes in Oryza sativa. Phytopathology, 100, 85-90.
32. Kocal, N., Sonnewald, U. and Sonnewald, S. (2008) Cell wall-bound invertase limits sucrose export and is involved in symptom development and inhibition of photosynthesis during compatible interaction between tomato and Xanthomonas campestris pv. vesicatoria. Plant Physiol. 148, 1523-1536.
33. Le Roy, K., Lammens, W., Verhaest, M., De Coninck, B., Rabijns, A., Van Laere, A. and Van den Ende, W. (2007) Unraveling the difference between invertases and fructan exohydrolases: a single amino acid (Asp-239) substitution transforms Arabidopsis cell wall invertase1 into a fructan 1-exohydrolase. Plant Physiol. 145, 616-625.
34. Le Roy, K., Vergauwen, R., Struyf, T., Yuan, S., Lammens, W., Mátrai, J., De Maeyer, M. and Van den Ende, W. (2013) Understanding the role of defective invertases in plants: tobacco Nin88 fails to degrade sucrose. Plant Physiol. 161, 1670-1881.
35. Li, W., Zhong, S.H., Li, G.J., Li, Q., Mao, B.Z., Deng, Y.W., Zhang, H.J., Zeng, L.J., Song, F.M. and He, Z.H. (2011) Rice RING protein OsBBI1 with E3 ligase activity confers broad-spectrum resistance against Magnaporthe oryzae by modifying the cell wall defence. Cell Res. 21, 835-848.
36. Lin, L., Zhong, S.H., Cui, X.F., Li, J.M. and He, Z.H. (2012) Characterization of temperature-sensitive mutants reveals a role for receptor-like kinase SCRAMBLED/STRUBBELIG in coordinating cell proliferation and differentiation during Arabidopsis leaf development. Plant J. 72, 707-720.
37. Lionetti, V., Raiola, A., Camardella, L., Giovane, A., Obel, N., Pauly, M., Favaron, F., Cervone, F. and Bellincampi, D. (2007) Overexpression of pectin methylesterase inhibitors in Arabidopsis restricts fungal infection by Botrytis cinerea. Plant Physiol. 143, 1871-1880.
38. Nakao, M., Nakamura, R., Kita, K., Inukai, R. and Ishikawa, A. (2011) Non-host resistance to penetration and hyphal growth of Magnaporthe oryzae in Arabidopsis. Sci. Rep. 1, 171.
39. Narayanasamy, P. (2006) Post Harvest Pathogens and Disease Management. Hoboken, NJ: John Wiley and Sons, Inc.
40. Ning, J., Li, X.H., Hicks, L.M. and Xiong, L.Z. (2010) A Raf-like MAPKKK gene DSM1 mediates drought resistance through reactive oxygen species scavenging in rice. Plant Physiol. 152, 876-890.
41. Ramírez, V., Agorio, A., Coego, A., García-Andrade, J., Hernández, M.J., Balaguer, B., Ouwerkerk, P.B., Zarra, I. and Vera, P. (2011) MYB46 modulates disease susceptibility to Botrytis cinerea in Arabidopsis. Plant Physiol. 155, 1920-1935.
42. Roitsch, T. and González, M.C. (2004) Function and regulation of plant invertases: sweet sensations. Trends Plant Sci. 9, 606-613.
43. Rolland, F., Baena-Gonzalez, E. and Sheen, J. (2006) Sugar sensing and signaling in plants: conserved and novel mechanisms. Annu. Rev. Plant Biol. 57, 675-709.
44. von Schaewen, A., Stitt, M., Schmidt, R., Sonnewald, U. and Willmitzer, L. (1990) Expression of a yeast-derived invertase in the cell wall of tobacco and Arabidopsis plants leads to accumulation of carbohydrate and inhibition of photosynthesis and strongly influences growth and phenotype of transgenic tobacco plants. EMBO J. 9, 3033-3044.
45. Sánchez-Rodríguez, C., Estévez, J.M., Llorente, F., Hernández-Blanco, C., Jordá, L., Pagán, I., Berrocal, M., Marco, Y, Somerville, S. and Molina, A. (2009) The ERECTA receptor-like kinase regulates cell wall-mediated resistance to pathogens in Arabidopsis thaliana. Mol. Plant-Microbe Interact. 22, 953-963.
46. Scharte, J., Schön, H. and Weis, E. (2005) Photosynthesis and carbohydrate metabolism in tobacco leaves during an incompatible interaction with Phytophthora nicotianae. Plant Cell Environ. 28, 1421-1435.
47. Schulze-Lefert, P. (2004) Knocking on the heaven's wall: pathogenesis of and resistance to biotrophic fungi at the cell wall. Curr. Opin. Plant Biol. 7, 377-383.
48. Seo, Y.S., Cho, J.I., Lee, S.K., Ryu, H.S., Han, M., Hahn, T.R., Sonnewald, U. and Jeon, J.S. (2007) Current insights into the primary carbon flux that occurs in plants undergoing a defense response. Plant Stress, 1, 42-49.
49. Smeekens, S. (2000) Sugar-induced signal transduction in plants. Annu. Rev. Plant Physiol. Plant Mol. Biol. 51, 49-81.
50. Sonnewald, S., Priller, J.P., Schuster, J., Glickmann, E., Hajirezaei, M.R., Siebig, S., Mudgett, M.B. and Sonnewald, U. (2012) Regulation of cell wall-bound invertase in pepper leaves by Xanthomonas campestris pv. Vesicatoria type three effectors. PLoS ONE, 7, e51763.
51. Sutton, P.N., Gilbert, M.J., Williams, L.E. and Hall, J.L. (2007) Powdery mildew infection of wheat leaves changes host solute transport and invertase activity. Plant Physiol. 129, 787-795.
52. Van den Ende, W., Lammens, W., Van Laere, A., Schroeven, L. and Le Roy, K. (2009) Donor and acceptor substrate selectivity among plant glycoside hydrolase family 32 enzymes. FEBS J. 276, 5788-5798.
53. Vogel, J.P., Raab, T.K., Schiff, C. and Somerville, S.C. (2002) PMR6, a pectate lyase-like gene required for powdery mildew susceptibility in Arabidopsis. Plant Cell, 14, 2095-2106.
54. Vogel, J.P., Raab, T.K., Somerville, C.R. and Somerville, S.C. (2004) Mutations in PMR5 result in powdery mildew resistance and altered cell wall composition. Plant J. 40, 968-978.
55. Vorwerk, S., Somerville, S. and Somerville, C. (2004) The role of plant cell wall polysaccharide composition in disease resistance. Trends Plant Sci. 9, 203-209.
56. Wang, E.T., Wang, J.J., Zhu, X.D., Hao, W., Wang, L.Y., Li, Q., Zhang, L.X., He, W., Lu, B.R., Ling, H.X., Ma, H., Zhang, G.Q. and He, Z.H. (2008) Control of rice grain-filling and yield by a gene with potential signature of domestication. Nat. Genet. 40, 1270-1274.
57. Wang, E.T., Xu, X., Zhang, L., Zhang, H., Lin, L., Wang, Q., Li, Q., Ge, S., Lu, B.R., Wang, W. and He, Z.H. (2010) Duplication and independent selection of cell-wall invertase genes GIF1 and OsCIN1 during rice evolution and domestication. BMC Evol. Biol. 10, 108-121.
58. Wang, Y.L., Gao, M.J., Li, Q., Wang, L.Y., Wang, J.J., Jeon, J.S., Qu, N., Zhang, Y.L. and He, Z.H. (2008) OsRAR1 and OsSGT1 physically interact and function in rice basal disease resistance. Mol. Plant-Microbe Interact. 21, 294-303.
59. Wright, D.P., Baldwin, B.C., Shephard, M.C. and Scholes, J.D. (1995) Source-sink relationships in wheat leaves infected with powdery mildew. I: alterations in carbohydrate metabolism. Physiol. Mol. Plant Pathol. 47, 237-253.
60. Xiang, L., Le Roy, K., Bolouri-Moghaddam, M.R., Vanhaecke, M., Lammens, W., Rolland, F. and Van den Ende, W. (2011) Exploring the neutral invertase-oxidative stress defence connection in Arabidopsis thaliana. J. Exp. Bot. 62, 3849-3862.
61. 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.
62. Yang, D.L., Li, Q., Deng, Y.W., Lou, Y.G., Wang, M.Y., Zhou, G.X., Zhang, Y.Y. and He, Z.H. (2008) Altered disease development in the eui mutants and Eui overexpressors indicates that gibberellins negatively regulate rice basal disease resistance. Mol. Plant 1, 528-537.
63. Zhang, S.J., Song, X.Q., Yu, B.S., Zhang, B.C., Sun, C.Q., Knox, J.P. and Zhou, Y.H. (2011) Identification of quantitative trait loci affecting hemicellulose characteristics based on cell wall composition in a wild and cultivated rice species. Mol. Plant 5, 162-175.