Aberrant protein N-glycosylation impacts upon infection-related growth transitions of the haploid plant-pathogenic fungus Mycosphaerella graminicola

Molecular Microbiology

Volumn 81, Issue 2, 2011, Pages 415-433

  Motteram, Juliet ^a   Lovegrove, Alison ^a   Pirie, Elizabeth ^a   Marsh, Justin ^a   Devonshire, Jean ^a   van de Meene, Allison ^a   Hammond Kosack, Kim ^a   Rudd, Jason J ^a  

^a ROTHAMSTED RESEARCH   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

DNA; MANNOSYLTRANSFERASE; PROTEIN SCALG2; T DNA; UNCLASSIFIED DRUG;

ARTICLE; ASCOMYCETES; FUNGAL GENE; FUNGAL PLANT DISEASE; FUNGUS GROWTH; FUNGUS HYPHAE; GENE DELETION; GENE EXPRESSION; GENE FUNCTION; GENETIC COMPLEMENTATION; GLYCOSYLATION; HAPLOID SPORE; MGALG2 GENE; MUTAGENESIS; MUTANT; MYCOSPHAERELLA GRAMINICOLA; NONHUMAN; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN FOLDING; SACCHAROMYCES CEREVISIAE; SEPTORIA TRITICI BLOTCH DISEASE; TEMPERATURE SENSITIVITY; WHEAT;

AMINO ACID SEQUENCE; ASCOMYCOTA; GENE DELETION; GENE EXPRESSION PROFILING; GENETIC COMPLEMENTATION TEST; GLYCOSYLATION; HYPHAE; MANNOSYLTRANSFERASES; MOLECULAR SEQUENCE DATA; MUTAGENESIS, INSERTIONAL; PLANT DISEASES; PLANT LEAVES; PROTEOME; SACCHAROMYCES CEREVISIAE PROTEINS; SEQUENCE HOMOLOGY, AMINO ACID; TRITICUM; VIRULENCE; VIRULENCE FACTORS;

FUNGI; MYCOSPHAERELLA GRAMINICOLA; SACCHAROMYCES CEREVISIAE; TRITICUM AESTIVUM;

EID: 79960159264     PISSN: 0950382X     EISSN: 13652958     Source Type: Journal    
DOI: 10.1111/j.1365-2958.2011.07701.x     Document Type: Article

References (69)

1. An, G., Ebert, P.R., Mitra, A., and Ha, S.B. (1988) Binary vectors. In Plant Molecular Biology Manual A3. Gelvin, S.B., and Schilperroort, R.A. (eds). Dordrecht: Kluwer Academic Press, pp. 1-19.
2. Bai, C., Xu, X.L., Chan, F.Y., Lee, R.T.H., and Wang, Y. (2006) MNN5 encodes an iron-regulated alpha-1, 2-mannosyltransferase important for protein glycosylation, cell wall integrity, morphogenesis and virulence in Candida albicans. Eukaryot Cell 5: 238-247.
3. Bates, S., Hughes, H.B., Munro, C.A., Thomas, W.P.H., MacCallum, D.M., Bertram, G., etal. (2006) Outer chain N-glycans are required for cell wall integrity and virulence of Candida albicans. J Biol Chem 281: 90-98.
4. Borges-Walmsley, M.I., Chen, D.L., Shu, X.H., and Walmsley, A.R. (2002) The pathobiology of Paracoccidioides brasiliensis. Trends Microbiol 10: 80-87.
5. Bowler, J., Scott, E., Tailor, R., Scalliet, G., Ray, J., and Csukai, M. (2010) New capabilities for Mycosphaerella graminicola research. Mol Plant Pathol 11: 691-704.
6. Brodsky, J.L., and Wojcikiewicz, R.J.H. (2009) Substrate-specific mediators of ER associated degradation (ERAD). Curr Opin Cell Biol 21: 516-521.
7. Burda, P., and Aebi, M. (1999) The dolichol pathway of N-linked glycosylation. Biochim Biophys Acta-Gen Subj 1426: 239-257.
8. Chavan, M., Suzuki, T., Rekowicz, M., and Lennarz, W. (2003) Genetic, biochemical, and morphological evidence for the involvement of N-glycosylation in biosynthesis of the cell wall beta 1, 6-glucan of Saccharomyces cerevisiae. Proc Natl Acad Sci USA 100: 15381-15386.
9. Church, G.M., and Gilbert, W. (1984) Genomic sequencing. Proc Natl Acad Sci USA 81: 1991-1995.
10. Dell, A., Reason, A.J., Khoo, K.H., Panico, M., McDowell, R.A., and Morris, H.R. (1994) Mass-spectrometry of carbohydrate-containing bioplymers. Guide Tech Glycobiol 230: 108-132.
11. Deshpande, N., Wilkins, M.R., Packer, N., and Nevalainen, H. (2008) Protein glycosylation pathways in filamentous fungi. Glycobiology 18: 626-637.
12. Fernandez-Alvarez, A., Elias-Villalobos, A., and Ibeas, J.I. (2009) The O-mannosyltransferase PMT4 is essential for normal appressorium formation and penetration in Ustilago maydis. Plant Cell 21: 3397-3412.
13. Freeze, H.H., and Aebi, M. (2005) Altered glycan structures: the molecular basis of congenital disorders of glycosylation. Curr Opin Struct Biol 15: 490-498.
14. Giaever, G., Chu, A.M., Ni, L., Connelly, C., Riles, L., Veronneau, S., etal. (2002) Functional profiling of the Saccharomyces cerevisiae genome. Nature 418: 387-391.
15. Harty, C., Strahl, S., and Romisch, K. (2001) O-mannosylation protects mutant alpha-factor precursor from endoplasmic reticulum-associated degradation. Mol Biol Cell 12: 1093-1101.
16. Helenius, A., and Aebi, M. (2001) Intracellular functions of N-linked glycans. Science 291: 2364-2369.
17. Huffaker, T.C., and Robbins, P.W. (1982) Temperature sensitive yeast mutants deficient in asparagine-linked glycosylation. J Biol Chem 257: 3203-3210.
18. Huffaker, T.C., and Robbins, P.W. (1983) Yeast mutants deficient in protein glycosylation. Proc Natl Acad Sci USA 80: 7466-7470.
19. Jackson, B.J., Kukuruzinska, M.A., and Robbins, P. (1993) Biosynthesis of Asparagine linked oligosaccharides in Saccharomyces cerevisiae- The Alg2 mutation. Glycobiology 3: 357-364.
20. Jaeken, J., and Matthijs, G. (2007) Congenital disorders of glycosylation: a rapidly expanding disease family. Annu Rev Genomics Hum Genet 8: 261-278.
21. Jakob, C.A., Burda, P., Roth, J., and Aebi, M. (1998) Degradation of misfolded endoplasmic reticulum glycoproteins in Saccharomyces cerevisiae is determined by a specific oligosaccharide structure. J Cell Biol 142: 1223-1233.
22. Kamper, J., Kahmann, R., Bolker, M., Ma, L.J., Brefort, T., Saville, B.J., etal. (2006) Insights from the genome of the biotrophic fungal plant pathogen Ustilago maydis. Nature 444: 97-101.
23. Kampf, M., Absmanner, B., Schwarz, M., and Lehle, L. (2009) Biochemical characterization and membrane topology of Alg2 from Saccharomyces cerevisiae as a bifunctional alpha 1, 3-and 1, 6-mannosyltransferase involved in lipid-linked oligosaccharide biosynthesis. J Biol Chem 284: 11900-11912.
24. Kema, G.H.J., Yu, D.Z., Rijkenberg, F.H.J., Shaw, M.W., and Baayen, R.P. (1996) Histology of the pathogenesis of Mycosphaerella graminicola in wheat. Phytopathology 86: 777-786.
25. Keon, J., Rudd, J.J., Antoniw, J., Skinner, W., Hargreaves, J., and Hammond-Kosack, K.E. (2005) Metabolic and stress adaptation by Mycosphaerella graminicola during sporulation in its host revealed through microarray transcription profiling. Mol Plant Pathol 6: 527-540.
26. Keon, J., Antoniw, J., Carzaniga, R., Deller, S., Ward, J.L., Baker, J.M., etal. (2007) Transcriptional adaptation of Mycosphaerella graminicola to programmed cell death of its susceptible wheat host. Mol Plant Microbe Interact 20: 178-193.
27. Klein, B.S., and Tebbets, B. (2007) Dimorphism and virulence in fungi. Curr Opin Microbiol 10: 314-319.
28. Klosterman, S.J., Perlin, M.H., Garcia-Pedrajas, M., Covert, S.F., and Gold, S.E. (2007) Genetics of morphogenesis and pathogenic development of Ustilago maydis. Adv Genet 57: 1-47.
29. Kukuruzinska, M.A., and Lennon, K. (1994) Growth-related coordination of the early N-glycosylation genes in yeast. Glycobiology 4: 437-443.
30. Lee, S.B., and Taylor, J.W. (1990) Isolation of DNA from fungal mycelia and single spores. In PCR Protocols. A Guide to Methods and Applications. Innis, M.A., Gelfand, D.H., Sninsky, J.J., and White, T.J. (eds). San Diego, CA: Academic Press, pp. 282-287.
31. 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 45: 6802-6818.
32. Lengeler, K.B., Davidson, R.C., D'Souza, C., Harashima, T., Shen, W.C., Wang, P., etal. (2000) Signal transduction cascades regulating fungal development and virulence. Microbiol Mol Biol Rev 64: 746-785.
33. Lennon, K., Bird, A., and Kukuruzinska, M.A. (1997) Deregulation of the first N-glycosylation gene, ALG7, perturbs the expression of G1 cyclins and cell cycle arrest in Saccharomyces cerevisiae. Biochem Biophys Res Commun 237: 562-565.
34. Liu, Y.G., Mitsukawa, N., Oosumi, T., and Whittier, R.F. (1995) Efficient isolation and mapping of Arabidopsis thaliana T-DNA insert junctions by thermal asymmetric interlaced PCR. Plant J 8: 457-463.
35. Lommel, M., and Strahl, S. (2009) Protein O-mannosylation: Conserved from bacteria to humans. Glycobiology 19: 816-828.
36. Mehrabi, R., Zwiers, L.H., de Waard, M.A., and Kema, G.H.J. (2006) MgHog1 regulates dimorphism and pathogenicity in the fungal wheat pathogen Mycosphaerella graminicola. Mol Plant Microbe Interact 19: 1262-1269.
37. Mori, K. (2009) Signalling pathways in the unfolded protein response: development from Yeast to mammals. J Biochem 146: 743-750.
38. Motteram, J., Kufner, I., Deller, S., Brunner, F., Hammond-Kosack, K.E., Nurnberger, T., and Rudd, J.J. (2009) Molecular characterization and functional analysis of MgNLP, the sole NPP1 domain-containing protein, from the fungal wheat leaf pathogen Mycosphaerella graminicola. Mol Plant Microbe Interact 22: 790-799.
39. Mouyna, I., Kniemeyer, O., Jank, T., Loussert, C., Mellado, E., Aimanianda, V., etal. (2010) Members of protein O-mannosyltransferase family in Aspergillus fumigatus differentially affect growth, morphogenesis and viability. Mol Microbiol 76: 1205-1221.
40. Murakami, K., Aikawa, J.I., Wada, M., Horinouchi, S., and Beppu, T. (1994) A Mucor pusillus mutant defective in asparagine-linked glycosylation. J Bacteriol 176: 2635-2639.
41. Nadal, M., Garcia-Pedrajas, M.D., and Gold, S.E. (2008) Dimorphism in fungal plant pathogens. FEMS Microbiol Lett 284: 127-134.
42. Nakatsukasa, K., Okada, S., Umebayashi, K., Fukuda, R., Nishikawa, S., and Endo, T. (2004) Roles of O-mannosylation of aberrant proteins in reduction of the load for endoplasmic reticulum chaperones in yeast. J Biol Chem 279: 49762-49772.
43. Nemecek, J.C., Wuthrich, M., and Klein, B.S. (2006) Global control of dimorphism and virulence in fungi. Science 312: 583-588.
44. Olson, G.M., Fox, D.S., Wang, P., Alspaugh, J.A., and Buchanan, K.L. (2007) Role of protein O-mannosyltransferase Pmt4 in the morphogenesis and virulence of Cryptococcus neoformans. Eukaryot Cell 6: 222-234.
45. Prill, S.K.H., Klinkert, B., Timpel, C., Gale, C.A., Schroppel, K., and Ernst, J.F. (2005) PMT family of Candida albicans: five protein mannosyltransferase isoforms affect growth, morphogenesis and antifungal resistance. Mol Microbiol 55: 546-560.
46. Rappleye, C.A., and Goldman, W.E. (2006) Defining virulence genes in the dimorphic fungi. Annu Rev Microbiol 60: 281-303.
47. Reiss, G., Heesen, S.T., Zimmerman, J., Robbins, P.W., and Aebi, M. (1996) Isolation of the ALG6 locus of Saccharomyces cerevisiae required for glucosylation in the N-linked glycosylation pathway. Glycobiology 6: 493-498.
48. Resheat-Eini, Z., Zelter, A., Gorovits, R., Read, N.D., and Yarden, O. (2008) The Neurospora crassa colonial temperature sensitive 2, 4 and 5 (cot-2, cot-4 and cot-5) genes encode regulatory and structural proteins required for hyphal elongation and branching. Fungal Genet Rep 55: 32-36.
49. Richie, D.L., Hartl, L., Aimanianda, V., Winters, M.S., Fuller, K.K., Miley, M.D., etal. (2009) A role for the unfolded protein response (UPR) in virulence and antifungal susceptibility in Aspergillus fumigatus. PloS Pathog 5: e1000258.
50. Rudd, J.J., Keon, J., and Hammond-Kosack, K.E. (2008) The wheat mitogen-activated protein kinases TaMPK3 and TaMPK6 are differentially regulated at multiple levels during compatible disease interactions with Mycosphaerella graminicola. Plant Physiol 147: 802-815.
51. Rudd, J.J., Antoniw, J., Marshall, R., Motteram, J., Fraaije, B., and Hammond-Kosack, K. (2010) Identification and characterisation of Mycosphaerella graminicola secreted or surface-associated proteins with variable intragenic coding repeats. Fungal Genet Biol 47: 19-32.
52. Ruddock, L.W., and Molinari, M. (2006) N-glycan processing in ER quality control. J Cell Sci 119: 4373-4380.
53. Ruizherrera, J., Leon, C.G., Guevaraolvera, L., and Carabeztrejo, A. (1995) Yeast-mycelial dimorphism of haploid and diploid strains of Ustilago maydis. Microbiology-UK 141: 695-703.
54. Sanchez-Martinez, C., and Perez-Martin, J. (2001) Dimorphism in fungal pathogens: Candida albicans and Ustilago maydis - similar inputs, different outputs. Curr Opin Microbiol 4: 214-221.
55. Schirawski, J., Bohnert, 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.
56. Schroder, M., Chang, J.S., and Kaufman, R.J. (2000) The unfolded protein response represses nitrogen-starvation induced developmental differentiation in yeast. Genes Dev 14: 2962-2975.
57. Stolz, A., and Wolf, D.H. (2010) Endoplasmic reticulum associated protein degradation: a chaperone assisted journey to hell. Biochim Biophys Acta-Mol Cell Res 1803: 694-705.
58. Strahl-Bolsinger, S., Gentzsch, M., and Tanner, W. (1999) Protein O-mannosylation. Biochim Biophys Acta-Gen Subj 1426: 297-307.
59. Takeuchi, K., Yamazaki, H., Shiraishi, N., Ohnishi, Y., Nishikawa, Y., and Horinouchi, S. (1999) Characterization of an alg2 mutant of the zygomycete fungus Rhizomucor pusillus. Glycobiology 9: 1287-1293.
60. Thiel, C., Schwarz, M., Peng, J.H., Grzmil, M., Hasilik, M., Braulke, T., etal. (2003) A new type of congenital disorders of glycosylation (CDG-Ii) provides new insights into the early steps of dolichol-linked oligosaccharide biosynthesis. J Biol Chem 278: 22498-22505.
61. Timpel, C., Strahl-Bolsinger, S., Ziegelbauer, K., and Ernst, J.F. (1998) Multiple functions of Pmt1p-mediated protein O-mannosylation in the fungal pathogen Candida albicans. J Biol Chem 273: 20837-20846.
62. Timpel, C., Zink, S., Strahl-Bolsinger, S., Schroppel, K., and Ernst, J. (2000) Morphogenesis, adhesive properties, and antifungal resistance depend on the Pmt6 protein mannosyltransferase in the fungal pathogen Candida albicans. J Bacteriol 182: 3063-3071.
63. Travers, K.J., Patil, C.K., Wodicka, L., Lockhart, D.J., Weissman, J.S., and Walter, P. (2000) Functional and genomic analyses reveal an essential coordination between the unfolded protein response and ER-associated degradation. Cell 101: 249-258.
64. Verostek, M.F., Atkinson, P.H., and Trimble, R.B. (1991) Structure of Saccharomyces cerevisiae Alg3, Sec18 mutant oligosaccharides. J Biol Chem 266: 5547-5551.
65. Verostek, M.F., Atkinson, P.H., and Trimble, R.B. (1993) Glycoprotein-biosynthesis in the Alg3 Saccharomyces cerevisiae mutant. 1. Role of glucose in the initial glycosylation of invertase in the endoplasmic reticulum. J Biol Chem 268: 12095-12103.
66. Whiteway, M., and Bachewich, C. (2007) Morphogenesis in Candida albicans. Annu Rev Microbiol 61: 529-553.
67. Woods, J.P. (2002) Histoplasma capsulatum molecular genetics, pathogenesis, and responsiveness to its environment. Fungal Genet Biol 35: 81-97.
68. Yamazaki, H., Shiraishi, N., Takeuchi, K., Ohnishi, Y., and Horinouchi, S. (1998) Characterization of alg2 encoding a mannosyltransferase in the zygomycete fungus Rhizomucor pusillus. Gene 221: 179-184.
69. Zwiers, L.H., and de Waard, M.A. (2001) Efficient Agrobacterium tumefaciens-mediated gene disruption in the phytopathogen Mycosphaerella graminicola. Curr Genet 39: 388-393.