N-Glycosylation of effector proteins by an α-1,3-Mannosyltransferase is required for the rice blast fungus to evade host innate immunity

Plant Cell

Volumn 26, Issue 3, 2014, Pages 1360-1376

  Chen, Xiao Lin ^a   Shi, Tao ^a,d   Yang, Jun ^a   Shi, Wei ^a   Gao, Xusheng ^a   Chen, Deng ^a   Xu, Xiaowen ^a   Xu, Jin Rong ^b   Talbot, Nicholas J ^c   Peng, You Liang ^a  

^a CHINA AGRICULTURAL UNIVERSITY   (China)

^b PURDUE UNIVERSITY   (United States)

^c UNIVERSITY OF EXETER   (United Kingdom)

^d INSTITUTE OF TROPICAL BIOSCIENCE AND BIOTECHNOLOGY   (China)

Author keywords

[No Author keywords available]

Indexed keywords

MANNOSYLTRANSFERASE; REACTIVE OXYGEN METABOLITE; VEGETABLE PROTEIN;

CELL WALL; ENDOPLASMIC RETICULUM; ENZYMOLOGY; GENETICS; GLYCOSYLATION; GROWTH, DEVELOPMENT AND AGING; HORDEUM; IMMUNE EVASION; IMMUNOLOGY; INNATE IMMUNITY; MAGNAPORTHE; METABOLISM; MICROBIOLOGY; MOLECULAR GENETICS; PATHOGENICITY;

CELL WALL; ENDOPLASMIC RETICULUM; GLYCOSYLATION; HORDEUM; IMMUNE EVASION; IMMUNITY, INNATE; MAGNAPORTHE; MANNOSYLTRANSFERASES; MOLECULAR SEQUENCE DATA; PLANT PROTEINS; REACTIVE OXYGEN SPECIES;

EID: 84899145740     PISSN: 10404651     EISSN: 1532298X     Source Type: Journal    
DOI: 10.1105/tpc.114.123588     Document Type: Article

References (86)

1. Adam, T., Bouhidel, K., Der, C., Robert, F., Najid, A., Simon-Plas, F., and Leborgne-Castel, N. (2012). Constitutive expression of clathrin hub hinders elicitor-induced clathrin-mediated endocytosis and defense gene expression in plant cells. FEBS Lett. 586: 3293-3298.
2. Aebi, M., Gassenhuber, J., Domdey, H., and te Heesen, S. (1996). Cloning and characterization of the ALG3 gene of Saccharomyces cerevisiae. Glycobiology 6: 439-444.
3. Anelli, T., and Sitia, R. (2008). Protein quality control in the early secretory pathway. EMBO J. 27: 315-327.
4. Bourett, T.M., Sweigard, J.A., Czymmek, K.J., Carroll, A., and Howard, R.J. (2002). Reef coral fluorescent proteins for visualizing fungal pathogens. Fungal Genet. Biol. 37: 211-220.
5. Bowman, S.M., and Free, S.J. (2006). The structure and synthesis of the fungal cell wall. Bioessays 28: 799-808.
6. Burda, P., and Aebi, M. (1999). The dolichol pathway of N-linked glycosylation. Biochim. Biophys. Acta 1426: 239-257.
7. Chi, M.-H., Park, S.-Y., Kim, S., and Lee, Y.H. (2009). A novel pathogenicity gene is required in the rice blast fungus to suppress the basal defenses of the host. PLoS Pathog. 5: e1000401.
8. 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.
9. Cross, A.R., and Jones, O.T.G. (1986). The effect of the inhibitor diphenylene iodonium on the superoxide-generating system of neutrophils: Specific labelling of a component polypeptide of the oxidase. Biochem. J. 237: 111-116.
10. Dean, N. (1999). Asparagine-linked glycosylation in the yeast Golgi. Biochim. Biophys. Acta 1426: 309-322.
11. Dean, R., Van Kan, J.A., Pretorius, Z.A., Hammond-Kosack, K.E., Di Pietro, A., Spanu, P.D., Rudd, J.J., Dickman, M., Kahmann, R., Ellis, J., and Foster, G.D. (2012). The top 10 fungal pathogens in molecular plant pathology. Mol. Plant Pathol. 13: 414-430.
12. de Jong, J.C., McCormack, B.J., Smirnoff, N., and Talbot, N.J. (1997). Glycerol generates turgor in rice blast. Nature 389: 244-245.
13. de Jonge, R., van Esse, H.P., Kombrink, A., Shinya, T., Desaki, Y., Bours, R., van der Krol, S., Shibuya, N., Joosten, M.H., and Thomma, B.P. (2010). Conserved fungal LysM effector Ecp6 prevents chitin-triggered immunity in plants. Science 329: 953-955.
14. Deshpande, N., Wilkins, M.R., Packer, N., and Nevalainen, H. (2008). Protein glycosylation pathways in filamentous fungi. Glycobiology 18: 626-637.
15. Ding, S.L., Liu, W., Iliuk, A., Ribot, C., Vallet, J., Tao, A., Wang, Y., Lebrun, M.H., and Xu, J.R. (2010). The tig1 histone deacetylase complex regulates infectious growth in the rice blast fungus Magnaporthe oryzae. Plant Cell 22: 2495-2508.
16. Doehlemann, G., Reissmann, S., Assmann, D., Fleckenstein, M., and Kahmann, R. (2011). Two linked genes encoding a secreted effector and a membrane protein are essential for Ustilago maydisinduced tumour formation. Mol. Microbiol. 81: 751-766.
17. Doehlemann, G., van der Linde, K., Assmann, D., Schwammbach, D., Hof, A., Mohanty, A., Jackson, D., and Kahmann, R. (2009). Pep1, a secreted effector protein of Ustilago maydis, is required for successful invasion of plant cells. PLoS Pathog. 5: e1000290.
18. Elorza, M.V., Rico, H., and Sentandreu, R. (1983). Calcofluor white alters the assembly of chitin fibrils in Saccharomyces cerevisiae and Candida albicans cells. J. Gen. Microbiol. 129: 1577-1582.
19. Farman, M.L., Eto, Y., Nakao, T., Tosa, Y., Nakayashiki, H., Mayama, S., and Leong, S.A. (2002). Analysis of the structure of the AVR1-CO39 avirulence locus in virulent rice-infecting isolates of Magnaporthe grisea. Mol. Plant Microbe Interact. 15: 6-16.
20. Fernández-Álvarez, A., Elías-Villalobos, A., Jiménez-Martín, A., Marín-Menguiano, M., and Ibeas, J.I. (2013). Endoplasmic reticulum glucosidases and protein quality control factors cooperate to establish biotrophy in Ustilago maydis. Plant Cell 25: 4676-4690.
21. Fujikawa, T., Sakaguchi, A., Nishizawa, Y., Kouzai, Y., Minami, E., Yano, S., Koga, H., Meshi, T., and Nishimura, M. (2012). Surface α-1,3-glucan facilitates fungal stealth infection by interfering with innate immunity in plants. PLoS Pathog. 8: e1002882.
22. Giniger, E., Varnum, S.M., and Ptashne, M. (1985). Specific DNA binding of GAL4, a positive regulatory protein of yeast. Cell 40: 767-774.
23. Giraldo, M.C., Dagdas, Y.F., Gupta, Y.K., Mentlak, T.A., Yi, M., Martinez-Rocha, A.L., Saitoh, H., Terauchi, R., Talbot, N.J., and Valent, B. (2013). Two distinct secretion systems facilitate tissue invasion by the rice blast fungus Magnaporthe oryzae. Nat. Commun. 4: 1996.
24. Guo, M., Chen, Y., Du, Y., Dong, Y., Guo, W., Zhai, S., Zhang, H., Dong, S., Zhang, Z., Wang, Y., Wang, P., and Zheng, X. (2011). The bZIP transcription factor MoAP1 mediates the oxidative stress response and is critical for pathogenicity of the rice blast fungus Magnaporthe oryzae. PLoS Pathog. 7: e1001302.
25. Guo, M., et al. (2010). The basic leucine zipper transcription factor Moatf1 mediates oxidative stress responses and is necessary for full virulence of the rice blast fungus Magnaporthe oryzae. Mol. Plant Microbe Interact. 23: 1053-1068.
26. Hamer, J.E., Howard, R.J., Chumley, F.G., and Valent, B. (1988). A mechanism for surface attachment in spores of a plant pathogenic fungus. Science 239: 288-290.
27. Häweker, H., Rips, S., Koiwa, H., Salomon, S., Saijo, Y., Chinchilla, D., Robatzek, S., and von Schaewen, A. (2010). Pattern recognition receptors require N-glycosylation to mediate plant immunity. J. Biol. Chem. 285: 4629-4636.
28. Helenius, A., and Aebi, M. (2001). Intracellular functions of N-linked glycans. Science 291: 2364-2369.
29. Helenius, A., and Aebi, M. (2004). Roles of N-linked glycans in the endoplasmic reticulum. Annu. Rev. Biochem. 73: 1019-1049.
30. Helenius, J., and Aebi, M. (2002). Transmembrane movement of dolichol linked carbohydrates during N-glycoprotein biosynthesis in the endoplasmic reticulum. Semin. Cell Dev. Biol. 13: 171-178.
31. Hemetsberger, C., Herrberger, C., Zechmann, B., Hillmer, M., and Doehlemann, G. (2012). The Ustilago maydis effector Pep1 suppresses plant immunity by inhibition of host peroxidase activity. PLoS Pathog. 8: e1002684.
32. Hiller, E., Zavrel, M., Hauser, N., Sohn, K., Burger-Kentischer, A., Lemuth, K., and Rupp, S. (2011). Adaptation, adhesion and invasion during interaction of Candida albicans with the host-Focus on the function of cell wall proteins. Int. J. Med. Microbiol. 301: 384-389.
33. Horton, R.M. (1995). PCR-mediated recombination and mutagenesis: SOEing together tailor-made genes. Mol. Biotechnol. 3: 93-99.
34. Howard, R.J., Ferrari, M.A., Roach, D.H., and Money, N.P. (1991). Penetration of hard substrates by a fungus employing enormous turgor pressures. Proc. Natl. Acad. Sci. USA 88: 11281-11284.
35. Huang, K., Czymmek, K.J., Caplan, J.L., Sweigard, J.A., and Donofrio, N.M. (2011). HYR1-mediated detoxification of reactive oxygen species is required for full virulence in the rice blast fungus. PLoS Pathog. 7: e1001335.
36. Hubbard, S.C., and Ivatt, R.J. (1981). Synthesis and processing of asparagine-linked oligosaccharides. Annu. Rev. Biochem. 50: 555-583.
37. Huffaker, T.C., and Robbins, P.W. (1983). Yeast mutants deficient in protein glycosylation. Proc. Natl. Acad. Sci. USA 80: 7466-7470.
38. Jia, Y., McAdams, S.A., Bryan, G.T., Hershey, H.P., and Valent, B. (2000). Direct interaction of resistance gene and avirulence gene products confers rice blast resistance. EMBO J. 19: 4004-4014.
39. Jones, J.D., and Dangl, J.L. (2006). The plant immune system. Nature 444: 323-329.
40. Kaku, H., Nishizawa, Y., Ishii-Minami, N., Akimoto-Tomiyama, C., Dohmae, N., Takio, K., Minami, E., and Shibuya, N. (2006). Plant cells recognize chitin fragments for defense signaling through a plasma membrane receptor. Proc. Natl. Acad. Sci. USA 103: 11086-11091.
41. Kang, J.S., et al. (2008). Salt tolerance of Arabidopsis thaliana requires maturation of N-glycosylated proteins in the Golgi apparatus. Proc. Natl. Acad. Sci. USA 105: 5933-5938.
42. Kankanala, P., Czymmek, K., and Valent, B. (2007). Roles for rice membrane dynamics and plasmodesmata during biotrophic invasion by the blast fungus. Plant Cell 19: 706-724.
43. Kelleher, D.J., and Gilmore, R. (2006). An evolving view of the eukaryotic oligosaccharyltransferase. Glycobiology 16: 47R-62R.
44. Kong, L.A., Yang, J., Li, G.T., Qi, L.L., Zhang, Y.J., Wang, C.F., Zhao, W.S., Xu, J.R., and Peng, Y.L. (2012). Different chitin synthase genes are required for various developmental and plant infection processes in the rice blast fungus Magnaporthe oryzae. PLoS Pathog. 8: e1002526.
45. Kostova, Z., and Wolf, D.H. (2005). Importance of carbohydrate positioning in the recognition of mutated CPY for ER-associated degradation. J. Cell Sci. 118: 1485-1492.
46. Lehle, L., Strahl, S., and Tanner, W. (2006). Protein glycosylation, conserved from yeast to man: A model organism helps elucidate congenital human diseases. Angew. Chem. Int. Ed. Engl. 45: 6802-6818.
47. Lerouge, P., Cabanes-Macheteau, M., Rayon, C., Fischette-Lainé, A.C., Gomord, V., and Faye, L. (1998). N-Glycoprotein biosynthesis in plants: Recent developments and future trends. Plant Mol. Biol. 38: 31-48.
48. Li, W., et al. (2009). The Magnaporthe oryzae avirulence gene AvrPiz-t encodes a predicted secreted protein that triggers the immunity in rice mediated by the blast resistance gene Piz-t. Mol. PlantMicrobe Interact. 22: 411-420.
49. Liebminger, E., Hüttner, S., Vavra, U., Fischl, R., Schoberer, J., Grass, J., Blaukopf, C., Seifert, G.J., Altmann, F., Mach, L., and Strasser, R. (2009). Class I α-mannosidases are required for Nglycan processing and root development in Arabidopsis thaliana. Plant Cell 21: 3850-3867.
50. Liu, G., Greenshields, D.L., Sammynaiken, R., Hirji, R.N., Selvaraj, G., and Wei, Y. (2007). Targeted alterations in iron homeostasis underlie plant defense responses. J. Cell Sci. 120: 596-605.
51. Liu, J.X., and Howell, S.H. (2010). Endoplasmic reticulum protein quality control and its relationship to environmental stress responses in plants. Plant Cell 22: 2930-2942.
52. Liu, T., Liu, Z., Song, C., Hu, Y., Han, Z., She, J., Fan, F., Wang, J., Jin, C., Chang, J., Zhou, J.M., and Chai, J. (2012). Chitin-induced dimerization activates a plant immune receptor. Science 336: 1160-1164.
53. Mentlak, T.A., Kombrink, A., Shinya, T., Ryder, L.S., Otomo, I., Saitoh, H., Terauchi, R., Nishizawa, Y., Shibuya, N., Thomma, B. P., and Talbot, N.J. (2012). Effector-mediated suppression of chitin-triggered immunity by Magnaporthe oryzae is necessary for rice blast disease. Plant Cell 24: 322-335.
54. Miki, S., et al. (2009). Molecular cloning and characterization of the AVR-Pia locus from a Japanese field isolate of Magnaporthe oryzae. Mol. Plant Pathol. 10: 361-374.
55. Mitchell, T.K., and Dean, R.A. (1995). The cAMP-dependent protein kinase catalytic subunit is required for appressorium formation and pathogenesis by the rice blast pathogen Magnaporthe grisea. Plant Cell 7: 1869-1878.
56. Mora-Montes, H.M., Bates, S., Netea, M.G., Castillo, L., Brand, A., Buurman, E.T., Díaz-Jiménez, D.F., Jan Kullberg, B., Brown, A.J., Odds, F.C., and Gow, N.A. (2010). A multifunctional mannosyltransferase family in Candida albicans determines cell wall mannan structure and host-fungus interactions. J. Biol. Chem. 285: 12087-12095.
57. Mosquera, G., Giraldo, M.C., Khang, C.H., Coughlan, S., and Valent, B. (2009). Interaction transcriptome analysis identifies Magnaporthe oryzae BAS1-4 as biotrophy-associated secreted proteins in rice blast disease. Plant Cell 21: 1273-1290.
58. Motteram, J., Lovegrove, A., Pirie, E., Marsh, J., Devonshire, J., van de Meene, A., Hammond-Kosack, K., and Rudd, J.J. (2011). Aberrant protein N-glycosylation impacts upon infection-related growth transitions of the haploid plant-pathogenic fungus Mycosphaerella graminicola. Mol. Microbiol. 81: 415-433.
59. Ohtsubo, K., and Marth, J.D. (2006). Glycosylation in cellular mechanisms of health and disease. Cell 126: 855-867.
60. Pelham, H.R., Hardwick, K.G., and Lewis, M.J. (1988). Sorting of soluble ER proteins in yeast. EMBO J. 7: 1757-1762.
61. Peng, Y.L., and Shishiyama, J. (1988). Temporal sequence of cytological events in rice leaves infected with Pyricularia oryzae. Can. J. Bot. 66: 730-735.
62. Poulain, D., and Jouault, T. (2004). Candida albicans cell wall glycans, host receptors and responses: Elements for a decisive crosstalk. Curr. Opin. Microbiol. 7: 342-349.
63. Qin, C., Qian, W., Wang, W., Wu, Y., Yu, C., Jiang, X., Wang, D., and Wu, P. (2008). GDP-mannose pyrophosphorylase is a genetic determinant of ammonium sensitivity in Arabidopsis thaliana. Proc. Natl. Acad. Sci. USA 105: 18308-18313.
64. Roncero, C., and Durán, A. (1985). Effect of Calcofluor white and Congo red on fungal cell wall morphogenesis: In vivo activation of chitin polymerization. J. Bacteriol. 163: 1180-1185.
65. Roth, J. (2002). Protein N-glycosylation along the secretory pathway: Relationship to organelle topography and function, protein quality control, and cell interactions. Chem. Rev. 102: 285-303.
66. Ruiz-May, E., Kim, S.J., Brandizzi, F., and Rose, J.K. (2012). The secreted plant N-glycoproteome and associated secretory pathways. Front. Plant Sci. 3: 117.
67. Saijo, Y., Tintor, N., Lu, X., Rauf, P., Pajerowska-Mukhtar, K., Häweker, H., Dong, X., Robatzek, S., and Schulze-Lefert, P. (2009). Receptor quality control in the endoplasmic reticulum for plant innate immunity. EMBO J. 28: 3439-3449.
68. Sambrook, J., and Russell, D.W. (2001). Molecular Cloning: A Laboratory Manual. (Cold Spring Harbor, NY: Cold Spring Harbor Laboratory Press).
69. Sánchez-Vallet, A., Saleem-Batcha, R., Kombrink, A., Hansen, G., Valkenburg, D.J., Thomma, B.P., and Mesters, J.R. (2013). Fungal effector Ecp6 outcompetes host immune receptor for chitin binding through intrachain LysM dimerization. Elife 2: e00790.
70. Schirawski, J., Böhnert, H.U., Steinberg, G., Snetselaar, K., Adamikowa, L., and Kahmann, R. (2005). Endoplasmic reticulum glucosidase II is required for pathogenicity of Ustilago maydis. Plant Cell 17: 3532-3543.
71. Shimizu, T., Nakano, T., Takamizawa, D., Desaki, Y., Ishii-Minami, N., Nishizawa, Y., Minami, E., Okada, K., Yamane, H., Kaku, H., and Shibuya, N. (2010). Two LysM receptor molecules, CEBiP and OsCERK1, cooperatively regulate chitin elicitor signaling in rice. Plant J. 64: 204-214.
72. Shin, J., Dunbrack, R.L., Jr., Lee, S., and Strominger, J.L. (1991). Signals for retention of transmembrane proteins in the endoplasmic reticulum studied with CD4 truncation mutants. Proc. Natl. Acad. Sci. USA 88: 1918-1922.
73. Snider, M.D., Sultzman, L.A., and Robbins, P.W. (1980). Transmembrane location of oligosaccharide-lipid synthesis in microsomal vesicles. Cell 21: 385-392.
74. Sweigard, J.A., Carroll, A.M., Farrall, L., Chumley, F.G., and Valent, B. (1998). Magnaporthe grisea pathogenicity genes obtained through insertional mutagenesis. Mol. Plant Microbe Interact. 11: 404-412.
75. Sweigard, J.A., Carroll, A.M., Kang, S., Farrall, L., Chumley, F.G., and Valent, B. (1995). Identification, cloning, and characterization of PWL2, a gene for host species specificity in the rice blast fungus. Plant Cell 7: 1221-1233.
76. Thines, E., Weber, R.W., and Talbot, N.J. (2000). MAP kinase and protein kinase A-dependent mobilization of triacylglycerol and glycogen during appressorium turgor generation by Magnaporthe grisea. Plant Cell 12: 1703-1718.
77. Verostek, M.F., Atkinson, P.H., and Trimble, R.B. (1993). Glycoprotein biosynthesis in the alg3 Saccharomyces cerevisiae mutant. II. Structure of novel Man6-10GlcNAc2 processing intermediates on secreted invertase. J. Biol. Chem. 268: 12104-12115.
78. Wood, P.J., and Fulcher, R.G. (1983). Dye interactions: A basis for specific detection and histochemistry of polysaccharides. J. Histochem. Cytochem. 31: 823-826.
79. Xu, J.R., and Hamer, J.E. (1996). MAP kinase and cAMP signaling regulate infection structure formation and pathogenic growth in the rice blast fungus Magnaporthe grisea. Genes Dev. 10: 2696-2706.
80. Xu, J.R., Staiger, C.J., and Hamer, J.E. (1998). Inactivation of the mitogen-activated protein kinase Mps1 from the rice blast fungus prevents penetration of host cells but allows activation of plant defense responses. Proc. Natl. Acad. Sci. USA 95: 12713-12718.
81. Xue, M., et al. (2012). Comparative analysis of the genomes of two field isolates of the rice blast fungus Magnaporthe oryzae. PLoS Genet. 8: e1002869.
82. Yang, J., Kong, L., Chen, X., Wang, D., Qi, L., Zhao, W., Zhang, Y., Liu, X., and Peng, Y.L. (2012). A carnitine-acylcarnitine carrier protein, MoCrc1, is essential for pathogenicity in Magnaporthe oryzae. Curr. Genet. 58: 139-148.
83. Yang, J., Zhao, X., Sun, J., Kang, Z., Ding, S., Xu, J.R., and Peng, Y. L. (2010). A novel protein Com1 is required for normal conidium morphology and full virulence in Magnaporthe oryzae. Mol. Plant Microbe Interact. 23: 112-123.
84. Yoshida, K., Saitoh, H., Fujisawa, S., Kanzaki, H., Matsumura, H., Yoshida, K., Tosa, Y., Chuma, I., Takano, Y., Win, J., Kamoun, S., and Terauchi, R. (2009). Association genetics reveals three novel avirulence genes from the rice blast fungal pathogen Magnaporthe oryzae. Plant Cell 21: 1573-1591.
85. Zerangue, N., Schwappach, B., Jan, Y.N., and Jan, L.Y. (1999). A new ER trafficking signal regulates the subunit stoichiometry of plasma membrane K(ATP) channels. Neuron 22: 537-548.
86. Zufferey, R., Knauer, R., Burda, P., Stagljar, I., te Heesen, S., Lehle, L., and Aebi, M. (1995). STT3, a highly conserved protein required for yeast oligosaccharyl transferase activity in vivo. EMBO J. 14: 4949-4960.