Endoplasmic reticulum glucosidases and protein quality control factors cooperate to establish biotrophy in Ustilago maydis

Plant Cell

Volumn 25, Issue 11, 2013, Pages 4676-4690

  Fernández Álvarez, Alfonso ^a,b   Elías Villalobos, Alberto ^a   Jiménez Martín, Alberto ^a   Marín Menguiano, Miriam ^a   Ibeas, José I ^a  

^a CSIC   (Spain)

^b IMPERIAL CANCER RESEARCH FUND   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

CALNEXIN; FUNGAL PROTEIN; GLUCOSIDASE; GLYCOPROTEIN;

ARTICLE; ENDOPLASMIC RETICULUM; ENZYMOLOGY; GENETICS; GLYCOSYLATION; HOST PATHOGEN INTERACTION; MAIZE; METABOLISM; MICROBIOLOGY; MUTATION; PATHOGENICITY; PHYLOGENY; PHYSIOLOGY; PLANT DISEASE; USTILAGO;

CALNEXIN; ENDOPLASMIC RETICULUM; FUNGAL PROTEINS; GLUCOSIDASES; GLYCOPROTEINS; GLYCOSYLATION; HOST-PATHOGEN INTERACTIONS; MUTATION; PHYLOGENY; PLANT DISEASES; USTILAGO; ZEA MAYS;

EID: 84891533534     PISSN: 10404651     EISSN: 1532298X     Source Type: Journal    
DOI: 10.1105/tpc.113.115691     Document Type: Article

References (59)

1. Apweiler, R., Hermjakob, H., and Sharon, N. (1999). On the frequency of protein glycosylation, as deduced from analysis of the SWISS-PROT database. Biochim. Biophys. Acta 1473: 4-8.
2. Arendt, C.W., and Ostergaard, H.L. (2000). Two distinct domains of the beta-subunit of glucosidase II interact with the catalytic alphasubunit. Glycobiology 10: 487-492.
3. Banuett, F. (1995). Genetics of Ustilago maydis, a fungal pathogen that induces tumors in maize. Annu. Rev. Genet. 29: 179-208.
4. Banuett, F., and Herskowitz, I. (1996). Discrete developmental stages during teliospore formation in the corn smut fungus, Ustilago maydis. Development 122: 2965-2976.
5. Bölker, M., Böhnert, H.U., Braun, K.H., Görl, J., and Kahmann, R. (1995). Tagging pathogenicity genes in Ustilago maydis by restriction enzyme-mediated integration (REMI). Mol. Gen. Genet. 248: 547-552.
6. Braakman, I., Helenius, J., and Helenius, A. (1992). Manipulating disulfide bond formation and protein folding in the endoplasmic reticulum. EMBO J. 11: 1717-1722.
7. Brachmann, A., König, J., Julius, C., and Feldbrügge, M. (2004). A reverse genetic approach for generating gene replacement mutants in Ustilago maydis. Mol. Genet. Genomics 272: 216-226.
8. Brachmann, A., Schirawski, J., Müller, P., and Kahmann, R. (2003). An unusual MAP kinase is required for efficient penetration of the plant surface by Ustilago maydis. EMBO J. 22: 2199-2210.
9. Brefort, T., Doehlemann, G., Mendoza-Mendoza, A., Reissmann, S., Djamei, A., and Kahmann, R. (2009). Ustilago maydis as a pathogen. Annu. Rev. Phytopathol. 47: 423-445.
10. Djamei, A., et al. (2011). Metabolic priming by a secreted fungal effector. Nature 478: 395-398.
11. 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.
12. Doehlemann, G., Wahl, R., Horst, R.J., Voll, L.M., Usadel, B., Poree, F., Stitt, M., Pons-Kühnemann, J., Sonnewald, U., Kahmann, R., and Kämper, J. (2008). Reprogramming a maize plant: Transcriptional and metabolic changes induced by the fungal biotroph Ustilago maydis. Plant J. 56: 181-195.
13. Ecker, M., Mrsa, V., Hagen, I., Deutzmann, R., Strahl, S., and Tanner, W. (2003). O-mannosylation precedes and potentially controls the N-glycosylation of a yeast cell wall glycoprotein. EMBO Rep. 4: 628-632.
14. Ellgaard, L., and Helenius, A. (2003). Quality control in the endoplasmic reticulum. Nat. Rev. Mol. Cell Biol. 4: 181-191.
15. Fernández, F.S., Trombetta, S.E., Hellman, U., and Parodi, A.J. (1994). Purification to homogeneity of UDP-glucose:glycoprotein glucosyltransferase from Schizosaccharomyces pombe and apparent absence of the enzyme for Saccharomyces cerevisiae. J. Biol. Chem. 269: 30701-30706.
16. Fernández-Alvarez, A., Elías-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.
17. Fernández-Alvarez, A., Elías-Villalobos, A., and Ibeas, J.I. (2010). Protein glycosylation in the phytopathogen Ustilago maydis: From core oligosaccharide synthesis to the ER glycoprotein quality control system, a genomic analysis. Fungal Genet. Biol. 47: 727-735.
18. Fernández-Álvarez, A., Marín-Menguiano, M., Lanver, D., Jiménez-Martín, A., Elías-Villalobos, A., Pérez-Pulido, A.J., Kahmann, R., and Ibeas, J.I. (2012). Identification of O-mannosylated virulence factors in Ustilago maydis. PLoS Pathog. 8: e1002563.
19. Gillissen, B., Bergemann, J., Sandmann, C., Schroeer, B., Bölker, M., and Kahmann, R. (1992). A two-component regulatory system for self/non-self recognition in Ustilago maydis. Cell 68: 647-657.
20. Glazebrook, J. (2005). Contrasting mechanisms of defense against biotrophic and necrotrophic pathogens. Annu. Rev. Phytopathol. 43: 205-227.
21. Hammond, C., Braakman, I., and Helenius, A. (1994). Role of N-linked oligosaccharide recognition, glucose trimming, and calnexin in glycoprotein folding and quality control. Proc. Natl. Acad. Sci. USA 91: 913-917.
22. Helenius, A., and Aebi, M. (2004). Roles of N-linked glycans in the endoplasmic reticulum. Annu. Rev. Biochem. 73: 1019-1049.
23. 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.
24. Herscovics, A. (1999). Processing glycosidases of Saccharomyces cerevisiae. Biochim. Biophys. Acta 1426: 275-285.
25. Hitt, R., and Wolf, D.H. (2004). DER7, encoding alpha-glucosidase I is essential for degradation of malfolded glycoproteins of the endoplasmic reticulum. FEMS Yeast Res. 4: 815-820.
26. Hoffman, C.S., and Winston, F. (1987). A ten-minute DNA preparation from yeast efficiently releases autonomous plasmids for transformation of Escherichia coli. Gene 57: 267-272.
27. Hong, Y., Sundaram, S., Shin, D.J., and Stanley, P. (2004). The Lec23 Chinese hamster ovary mutant is a sensitive host for detecting mutations in alpha-glucosidase I that give rise to congenital disorder of glycosylation IIb (CDG IIb). J. Biol. Chem. 279: 49894-49901.
28. Kämper, J., et al. (2006). Insights from the genome of the biotrophic fungal plant pathogen Ustilago maydis. Nature 444: 97-101.
29. Kern, G., Kern, D., Jaenicke, R., and Seckler, R. (1993). Kinetics of folding and association of differently glycosylated variants of invertase from Saccharomyces cerevisiae. Protein Sci. 2: 1862-1868.
30. Kloppholz, S., Kuhn, H., and Requena, N. (2011). A secreted fungal effector of Glomus intraradices promotes symbiotic biotrophy. Curr. Biol. 21: 1204-1209.
31. Lai, Z.W., Nice, E.C., and Schilling, O. (2013). Glycocapture-based proteomics for secretome analysis. Proteomics 13: 512-525.
32. 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 alpha-mannosidases are required for N-glycan processing and root development in Arabidopsis thaliana. Plant Cell 21: 3850-3867.
33. Lipari, F., and Herscovics, A. (1996). Role of the cysteine residues in the alpha1,2-mannosidase involved in N-glycan biosynthesis in Saccharomyces cerevisiae. The conserved Cys340 and Cys385 residues form an essential disulfide bond. J. Biol. Chem. 271: 27615-27622.
34. Määttänen, P., Gehring, K., Bergeron, J.J., and Thomas, D.Y. (2010). Protein quality control in the ER: The recognition of misfolded proteins. Semin. Cell Dev. Biol. 21: 500-511.
35. Mendoza-Mendoza, A., Berndt, P., Djamei, A., Weise, C., Linne, U., Marahiel, M., Vranes, M., Kämper, J., and Kahmann, R. (2009). Physical-chemical plant-derived signals induce differentiation in Ustilago maydis. Mol. Microbiol. 71: 895-911.
36. 2detoxification is required for virulence. Plant Cell 19: 2293-2309.
37. Mora-Montes, H.M., Bates, S., Netea, M.G., Díaz-Jiménez, D.F., López-Romero, E., Zinker, S., Ponce-Noyola, P., Kullberg, B.J., Brown, A.J., Odds, F.C., Flores-Carreón, A., and Gow, N.A. (2007). Endoplasmic reticulum alpha-glycosidases of Candida albicans are required for N glycosylation, cell wall integrity, and normal hostfungus interaction. Eukaryot. Cell 6: 2184-2193.
38. Mueller, A.N., Ziemann, S., Treitschke, S., Aßmann, D., and Doehlemann, G. (2013). Compatibility in the Ustilago maydis-maize interaction requires inhibition of host cysteine proteases by the fungal effector Pit2. PLoS Pathog. 9: e1003177.
39. Mueller, O., Kahmann, R., Aguilar, G., Trejo-Aguilar, B., Wu, A., and de Vries, R.P. (2008). The secretome of the maize pathogen Ustilago maydis. Fungal Genet. Biol. 45 (Suppl 1): S63-S70.
40. Nguyen, Q.B., Kadotani, N., Kasahara, S., Tosa, Y., Mayama, S., and Nakayashiki, H. (2008). Systematic functional analysis of calcium-signalling proteins in the genome of the rice-blast fungus, Magnaporthe oryzae, using a high-throughput RNA-silencing system. Mol. Microbiol. 68: 1348-1365.
41. Nimchuk, Z., Eulgem, T., Holt, B.F., III., and Dangl, J.L. (2003). Recognition and response in the plant immune system. Annu. Rev. Genet. 37: 579-609.
42. Parodi, A.J. (2000). Protein glucosylation and its role in protein folding. Annu. Rev. Biochem. 69: 69-93.
43. Powers-Fletcher, M.V., Jambunathan, K., Brewer, J.L., Krishnan, K., Feng, X., Galande, A.K., and Askew, D.S. (2011). Impact of the lectin chaperone calnexin on the stress response, virulence and proteolytic secretome of the fungal pathogen Aspergillus fumigatus. PLoS ONE 6: e28865.
44. Romaniouk, A., and Vijay, I.K. (1997). Structure-function relationships in glucosidase I: Amino acids involved in binding the substrate to the enzyme. Glycobiology 7: 399-404.
45. Romero, P.A., Vallée, F., Howell, P.L., and Herscovics, A. (2000). Mutation of Arg(273) to Leu alters the specificity of the yeast N-glycan processing class I alpha1,2-mannosidase. J. Biol. Chem. 275: 11071-11074.
46. 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.
47. Schirawski, J., et al. (2010). Pathogenicity determinants in smut fungi revealed by genome comparison. Science 330: 1546-1548.
48. Schwarz, F., and Aebi, M. (2011). Mechanisms and principles of Nlinked protein glycosylation. Curr. Opin. Struct. Biol. 21: 576-582.
49. Skibbe, D.S., Doehlemann, G., Fernandes, J., and Walbot, V. (2010). Maize tumors caused by Ustilago maydis require organspecific genes in host and pathogen. Science 328: 89-92.
50. Takeda, Y., Totani, K., Matsuo, I., and Ito, Y. (2009). Chemical approaches toward understanding glycan-mediated protein quality control. Curr. Opin. Chem. Biol. 13: 582-591.
51. Tamura, K., Dudley, J., Nei, M., and Kumar, S. (2007). MEGA4: Molecular Evolutionary Genetics Analysis (MEGA) software version 4.0. Mol. Biol. Evol. 24: 1596-1599.
52. Trombetta, E.S., Simons, J.F., and Helenius, A. (1996). Endoplasmic reticulum glucosidase II is composed of a catalytic subunit, conserved from yeast to mammals, and a tightly bound noncatalytic HDEL-containing subunit. J. Biol. Chem. 271: 27509-27516.
53. van Esse, H.P., Van't Klooster, J.W., Bolton, M.D., Yadeta, K.A., van Baarlen, P., Boeren, S., Vervoort, J., de Wit, P.J., and Thomma, B.P. (2008). The Cladosporium fulvum virulence protein Avr2 inhibits host proteases required for basal defense. Plant Cell 20: 1948-1963.
54. Völker, C., De Praeter, C.M., Hardt, B., Breuer, W., Kalz-Füller, B., Van Coster, R.N., and Bause, E. (2002). Processing of N-linked carbohydrate chains in a patient with glucosidase I deficiency (CDG type IIb). Glycobiology 12: 473-483.
55. Wilkinson, B.M., Purswani, J., and Stirling, C.J. (2006). Yeast GTB1 encodes a subunit of glucosidase II required for glycoprotein processing in the endoplasmic reticulum. J. Biol. Chem. 281: 6325-6333.
56. Wojtaszek, P. (1997). Oxidative burst: An early plant response to pathogen infection. Biochem. J. 322: 681-692.
57. Yan, A., and Lennarz, W.J. (2005). Unraveling the mechanism of protein N-glycosylation. J. Biol. Chem. 280: 3121-3124.
58. Yan, Q., Prestwich, G.D., and Lennarz, W.J. (1999). The Ost1p subunit of yeast oligosaccharyl transferase recognizes the peptide glycosylation site sequence,-Asn-X-Ser/Thr-. J. Biol. Chem. 274: 5021-5025.
59. Zhang, L., Feng, D., Fang, W., Ouyang, H., Luo, Y., Du, T., and Jin, C. (2009). Comparative proteomic analysis of an Aspergillus fumigatus mutant deficient in glucosidase I (AfCwh41). Microbiology 155: 2157-2167.