Endoplasmic reticulum glucosidase II is required for pathogenicity of Ustilago maydis

Plant Cell

Volumn 17, Issue 12, 2005, Pages 3532-3543

  Schirawski, Jan ^a   Böhnert, Heidi U ^b,d   Steinberg, Gero ^a   Snetselaar, Karen ^c   Adamikowa, Lubica ^a,e   Kahmann, Regine ^a,b  

^a MAX PLANCK INSTITUTE FOR TERRESTRIAL MICROBIOLOGY   (Germany)

^b Institut fur Genetik und Mikrobiologie   (Germany)

^c SAINT JOSEPH S UNIVERSITY   (United States)

^d CNRS   (France)

^e NONE   (Slovakia)

Author keywords

[No Author keywords available]

Indexed keywords

MUTAGENESIS; PLANT CELL CULTURE;

ENDOPLASMIC RETICULUM GLUCOSIDASE II; EPIDERMAL CELL LAYER; PATHOGENICITY; USTILAGO MAYDIS;

ENZYMES;

CELLS; ENZYMES; GENES; PLANTS;

FUNGI; SACCHAROMYCES CEREVISIAE; USTILAGO MAYDIS;

4 NITROPHENYL ALPHA GLUCOSIDASE; 4-NITROPHENYL-ALPHA-GLUCOSIDASE; ALPHA GLUCOSIDASE; PRIMER DNA;

AMINO ACID SEQUENCE; ARTICLE; CHEMISTRY; ENDOPLASMIC RETICULUM; ENZYMOLOGY; METABOLISM; MOLECULAR GENETICS; MUTAGENESIS; NUCLEOTIDE SEQUENCE; PATHOGENICITY; PLASMID; SEQUENCE HOMOLOGY; USTILAGO;

ALPHA-GLUCOSIDASES; AMINO ACID SEQUENCE; BASE SEQUENCE; DNA PRIMERS; ENDOPLASMIC RETICULUM; MOLECULAR SEQUENCE DATA; MUTAGENESIS; PLASMIDS; SEQUENCE HOMOLOGY, AMINO ACID; USTILAGO;

EID: 33644816684     PISSN: 10404651     EISSN: None     Source Type: Journal    
DOI: 10.1105/tpc.105.036285     Document Type: Article

References (57)

1. Altschul, S.F., Madden, T.L., Schaffer, A.A., Zhang, J., Zhang, Z., Miller, W., and Lipman, D.J. (1997). Gapped BLAST and PSI-BLAST: A new generation of protein database search programs. Nucleic Acids Res. 25, 3389-3402.
2. Banuett, F., and Herskowitz, I. (1989). Different a alleles are necessary for maintenance of filamentous growth but not for meiosis. Proc. Natl. Acad. Sci. USA 86, 5878-5882.
3. Banuett, F., and Herskowitz, I. (1996). Discrete developmental stages during teliospore formation in the corn smut fungus, Ustilago maydis. Development 122, 2965-2976.
4. Bateman, A., Birney, E., Cerruti, L., Durbin, R., Etwiller, L., Eddy, S.R., Griffiths-Jones, S., Howe, K.L., Marshall, M., and Sonnhammer, E.L. (2002). The Pfam protein families database. Nucleic Acids Res. 30, 276-280.
5. Bauer, R., Oberwinkler, F., and Vanky, K. (1997). Ultrastructural markers and systematics in smut fungi and allied taxa. Can. J. Bot. 75, 1273-1314.
6. Bechinger, C., Giebel, K.P., Schnell, M., Leiderer, P., Deising, H.B., and Bastmeyer, M. (1999). Optical measurements of invasive forces exerted by appressoria of a plant pathogenic fungus. Science 285, 1896-1899.
7. Becker, D.M., and Lundblad, V. (1994). Introduction of DNA into yeast cells. In Current Protocols in Molecular Biology, P.M. Ausubel, R. Brent, R.E. Kingston, D.D. Moore, J.G. Seidman, J.A. Smith, and K. Struhl, eds (New York: John Wiley & Sons), pp. 13.7.1-13.7.10.
8. Bickle, M., Delley, P.A., Schmidt, A., and Hall, M.N. (1998). Cell wall integrity modulates RHO1 activity via the exchange factor ROM2. EMBO J. 17, 2235-2245.
9. Böhnert, H.U. (2001). Charakterisierung Apathogener REMI-Mutanten in Ustilago maydis. PhD dissertation (Munich, Germany: Ludwigs-Maximilians- Universität).
10. Bölker, M. (2001). Ustilago mayoYs - A valuable model system for the study of fungal dimorphism and virulence. Microbiology 147, 1395-1401.
11. Bölker, M., Bohnert, H.U., Braun, K.H., Görl, J., and Kahmann, R. (1995b). Tagging pathogenicity genes in Ustilago maydis by restriction enzyme-mediated integration (REMI). Mol. Gen. Genet. 248, 547-552.
12. Bölker, M., Genin, S., Lehmler, C., and Kahmann, R. (1995a). Genetic regulation of mating, and dimorphism in Ustilago maydis. Can. J. Bot. 73, 320-325.
13. Bölker, M., Urban, M., and Kahmann, R. (1992). The a mating type locus of Ustilago maydis specifies cell signaling components. Cell 68, 441-450.
14. 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.
15. Brachmann, A., Weinzierl, G., Kämper, J., and Kahmann, R. (2001). Identification of genes in the bW/bE regulatory cascade in Ustilago maydis. Mol. Microbiol. 42, 1047-1063.
16. Cormack, B.P., Valdivia, R.H., and Falkow, S. (1996). FACS-optimized mutants of the green fluorescent protein (GFP). Gene 173, 33-38.
17. D'Alessio, C., Fernandez, F., Trombetta, E.S., and Parodi, A.J. (1999). Genetic evidence for the heterodimeric structure of glucosidase II. The effect of disrupting the subunit-encoding genes on glycoprotein folding. J. Biol. Chem. 274, 25899-25905.
18. Day, P.R., and Anagnostakis, S.L. (1971). Corn smut dikaryon in culture. Nat. New Biol. 231, 19-20.
19. Deising, H., Heiler, S., Rauscher, M., Xu, H., and Mendgen, K. (1996). Cellular Aspects of Rust Infection Structure Differentiation: Spore Adhesion and Fungal Morphogenesis. (Dordrecht, The Netherlands: Kluwer Academic Publishers).
20. Fanchiotti, S., Fernandez, F., D'Alessio, C., and Parodi, A.J. (1998). The UDP-Glc:glycoprotein glucosyltransferase is essential for Schizosaccharomyces pombe viability under conditions of extreme endoplasmic reticulum stress. J. Cell Biol. 143, 625-635.
21. Freeze, H.H., Lammertz, M., lranfar, N., Fuller, D., Panneerselvam, K., and Loomis, W.F. (1997). Consequences of disrupting the gene that encodes alpha-glucosidase II in the N-linked oligosaccharide biosynthesis pathway of Dictyostelium discoideum. Dev. Genet. 21, 177-186.
22. Gillissen, B., Bergemann, J., Sandmann, C., Schröer, B., Bölker, M., and Kahmann, R. (1992). A two-component regulatory system for self/non-self recognition in Ustilago maydis. Cell 68, 647-657.
23. Helenius, A., and Aebi, M. (2001). Intracellular functions of N-linked glycans. Science 291, 2364-2369.
24. Henrissat, B. (1991). A classification of glycosyl hydrolases based on amino acid sequence similarities. Biochem. J. 280, 309-316.
25. Holliday, R. (1974). Ustilago maydis. In Handbook of Genetics, R.C. King, ed (New York: Plenum Press), pp. 575-595.
26. 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.
27. Kämper, J., Reichmann, M., Romeis, T., Bölker, M., and Kahmann, R. (1995). Multiallelic recognition: Nonself-dependent dimerization of the bE and bW homeodomain proteins in Ustilago maydis. Cell 81, 73-83.
28. Kukuruzinska, M.A., and Lennon, K. (1995). Diminished activity of the first N-glycosylation enzyme, dolichol-P-dependent N-acetylglucosamine-1-P transferase (GPT), gives rise to mutant phenotypes in yeast. Biochim. Biophys. Acta 1247, 51-59.
29. Lehle, L., and Tanner, W, (1976). The specific site of tunicamycin inhibition in the formation of dolichol-bound N-acetylglucosamine derivatives. FEBS Lett. 72, 167-170.
30. Lorenz, M.C. (2002). Genomic approaches to fungal pathogenicity. Curr. Opin. Microbiol. 5, 372-378.
31. Loubradou, G., Brachmann, A., Feldbrügge, M., and Kahmann, R. (2001). A homolog of the transcriptional repressor Ssn6p antagonizes cAMP signalling in Ustilago maydis. Mol. Microbiol. 40, 719-730.
32. Mendgen, K., and Hahn, M. (2002). Plant infection and the establishment of fungal biotrophy. Trends Plant Sci. 7, 352-356.
33. Mumberg, D., Müller, R., and Funk, M. (1994). Regulatable promoters of Saccharomyces cerevisiae: Comparison of transcriptional activity and their use for heterologous expression. Nucleic Acids Res. 22, 5767-5768.
34. Nakai, K., and Horton, P. (1999). PSORT: A program for detecting sorting signals in proteins and predicting their subcellular localization. Trends Biochem. Sci. 24, 34-36.
35. O'Connell, R.J. (1991). Cytochemical analysis of infection structures of Colletotrichum lindemuthianum using fIuorochrome-labelled lectins. Physiol. Mol. Plant Pathol. 39, 189-200.
36. Parodi, A.J. (2000). Protein glucosylation and its role in protein folding. Annu. Rev. Biochem. 69, 69-93.
37. Rademacher, T.W., Parekh, R.B., and Dwek, R.A. (1988). Glycobiology. Annu. Rev. Biochem. 57, 785-838.
38. Sambrook, J., Frisch, E.F., and Maniatis, T. (1989). Molecular Cloning: A Laboratory Manual. (Cold Spring Harbor, NY: Cold Spring Harbor Laboratory Press).
39. Schulz, B., Banuett, F., Dahl, M., Schlesinger, R., Schäfer, W., Martin, T., Herskowitz, I., and Kahmann, R. (1990). The b alleles of U. maydis, whose combinations program pathogenic development, code for polypeptides containing a homeodomain-related motif. Cell 60, 295-306.
40. Simons, J.F., Ebersold, M., and Helenius, A. (1998). Cell wall 1,6-beta-glucan synthesis in Saccharomyces cerevisiae depends on ER glucosidases I and II, and the molecular chaperone BiP/Kar2p. EMBO J. 17, 396-405.
41. Snetselaar, K., and Mims, C. (1994). Light and electron microscopy of Ustilago maydis hyphae in maize. Mycol. Res. 98, 347-355.
42. Snetselaar, K.M., Carfioli, M.A., and Cordisco, K.M. (2001). Pollination can protect maize ovaries from infection by Ustilago maydis, the corn smut fungus. Can. J. Bot. 79, 1390-1399.
43. Snetselaar, K.M., and Mims, C.W. (1992). Sporidial fusion and infection of maize seedlings by the smut fungus Ustilago maydis. Mycologia 84, 193-203.
44. Snetselaar, K.M., and Mims, C.W. (1993). Infection of maize stigmas by Ustilago maydis: Light and electron microscopy. Phytopathology 83, 843-850.
45. Spellig, T., Bottin, A., and Kahmann, R. (1996). Green fluorescent protein (GFP) as a new vital marker in the phytopathogenic fungus Ustilago maydis. Mol. Gen. Genet. 252, 503-509.
46. Staples, R.C. (1985). The development of infection structures by the rusts and other fungi. Microbiol. Sci. 2, 193-194, 197-198.
47. Talbot, N.J. (2003). On the trail of a cereal killer: Exploring the biology of Magnaporthe grisea. Annu. Rev. Microbiol. 57, 177-202.
48. Tkacz, J.S., and Lampen, O. (1975). Tunicamycin inhibition of polyisoprenyl N-acetylglucosaminyl pyrophosphate formation in calf-liver microsomes. Biochem. Biophys. Res. Commun. 65, 248-257.
49. Treco, D.A., and Lundblad, V. (1993). Preparation of yeast media. In Current Protocols in Molecular Biology, P.M. Ausubel, R. Brent, R.E. Kingston, D.D. Moore, J.G. Seidman, J.A. Smith, and K. Struhl, eds (New York: John Wiley & Sons), pp. 13.1.1-13.1.7.
50. Trombetta, E.S., and Helenius, A. (1998). Lectins as chaperones in glycoprotein folding. Curr. Opin. Struct. Biol. 8, 587-592.
51. 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.
52. Tsukuda, T., Carleton, S., Fotheringham, S., and Holloman, W.K. (1988). Isolation and characterization of an autonomously replicating sequence from Ustilago maydis. Mol. Cell. Biol. 8, 3703-3709.
53. Urban, M., Kahmann, R., and Bölker, M. (1996). The biallelic a mating type locus of Ustilago maydis: Remnants of an additional pheromone gene indicate evolution from a multiallelic ancestor. Mol. Gen. Genet. 250, 414-420.
54. Varki, A. (1993). Biological roles of oligosaccharides: All of the theories are correct. Glycobiology 3, 97-130.
55. Wedlich-Söldner, R., Bölker, M., Kahmann, R., and Steinberg, G. (2000). A putative endosomal t-SNARE links exo- and endocytosis in the phytopathogenic fungus Ustilago maydis. EMBO J. 19, 1974-1986.
56. Wedlich-Söldner, R., Schulz, I., Straube, A., and Steinberg, G. (2002). Dynein supports motility of endoplasmic reticulum in the fungus Ustilago maydis. Mol. Biol. Cell 13, 965-977.
57. Yanisch-Perron, C., Vieira, J., and Messing, J. (1985). Improved M13 phage cloning vectors and host strains: Nucleotide sequences of the M13mp18 and pUC19 vectors. Gene 33, 103-119.