Rapid adhesion of Stagonospora nodorum spores to a hydrophobic surface requires pre-formed cell surface glycoproteins

Mycological Research

Volumn 111, Issue 11, 2007, Pages 1255-1267

  Newey, Lisa J ^a   Caten, Chris E ^a   Green, Jonathan R ^a  

^a UNIVERSITY OF BIRMINGHAM   (United Kingdom)

Author keywords

Conidia; Fungal pathogen; Phaeosphaeria nodorum; Plant pathology; Spore

Indexed keywords

MEMBRANE PROTEIN; POLYSTYRENE DERIVATIVE;

ADHESION; DETERGENT; ELECTROKINESIS; ENZYME ACTIVITY; FUNGUS; HYDROPHOBICITY; PATHOLOGY; PROTEIN; SECRETION; SPORE;

ARTICLE; ASCOMYCETES; CELL ADHESION; FUNGUS SPORE; GENE EXPRESSION REGULATION; HYDROPHOBICITY; METABOLISM; PHYSIOLOGY; POLYACRYLAMIDE GEL ELECTROPHORESIS; SURFACE PROPERTY; TIME;

ASCOMYCOTA; CELL ADHESION; ELECTROPHORESIS, POLYACRYLAMIDE GEL; GENE EXPRESSION REGULATION, FUNGAL; HYDROPHOBICITY; MEMBRANE GLYCOPROTEINS; POLYSTYRENES; SPORES, FUNGAL; SURFACE PROPERTIES; TIME FACTORS;

BACTERIA (MICROORGANISMS); PHAEOSPHAERIA NODORUM; TRITICUM AESTIVUM;

EID: 36549038145     PISSN: 09537562     EISSN: 14698102     Source Type: Journal    
DOI: 10.1016/j.mycres.2007.09.007     Document Type: Article

References (62)

1. Ahn N., Kim S., Choi W., Im K.-H., and Lee Y.-H. Extracellular matrix protein gene, EMP1, is required for appressorium formation and pathogenicity of the rice blast fungus Magnaporthe grisea. Molecular Cell 17 (2004) 166-173
2. Ahn I.P., Uhm K.H., Kim S., and Lee Y.-H. Signaling pathways involved in preinfection development of Colletotrichum gloeosporioides, C. coccodes, and C. dematium pathogenic on red pepper. Physiological and Molecular Plant Pathology 63 (2003) 281-289
3. Apoga D., Barnard J., Craighead H.G., and Hoch H.C. Quantification of substratum contact required for initiation of Colletotrichum graminicola appressoria. Fungal Genetics and Biology 41 (2004) 1-12
4. Apoga D., Jansson H.B., and Tunlid A. Adhesion of conidia and germlings of the plant pathogenic fungus Bipolaris sorokiniana to solid surfaces. Mycological Research 105 (2001) 1251-1260
5. Beckett A., Tatnell J.A., and Taylor N. Adhesion and pre-invasion behaviour of uridiniospores of Uromyces viciae-fabae during germination on host and synthetic surfaces. Mycological Research 94 (1990) 865-875
6. Bird P.M., and Ride J.P. The resistance of wheat to Septoria nodorum: fungal development in relation to host lignification. Physiological Plant Pathology 19 (1981) 289-299
7. Bollag D.M., and Edelstein S.J. Protein extraction. Protein Methods (1991), Wiley-Liss, NY
8. Braun E.J., and Howard R.J. Adhesion of Cochliobolus heterosrophus conidia and germlings to leaves and artificial surfaces. Experimental Mycology 18 (1994) 211-220
9. Cappellaro C., Mrsa V., and Tanner W. New potential cell wall glucanases of Saccharomyces cerevisiae and their involvement in mating. Journal of Bacteriology 180 (1998) 5030-5037
10. Carlson S.R. Glycobiology: a practical approach (1993), Oxford University Press, Oxford
11. Carzaniga R., Bowyer P., and O'Connell R.J. Production of extracellular matrices during development of infection structures by the downy mildew Peronospora parasitica. New Phytologist 149 (2001) 83-93
12. Casanova M., and Chaffin W.L. Cell wall glycoproteins of Candida albicans as released by different methods. Journal of General Microbiology 137 (1991) 1045-1051
13. Casanova M., Lopez-Ribot J.L., Martinez J.P., and Sentandreu R. Characterisation of cell wall proteins of yeast and mycelial cells of Candida albicans by labelling with biotin: comparison with other techniques. Infection and Immunity 60 (1992) 4898-4906
14. Chaffin W.L., Lopez-Ribot J.L., Casanova M., Gozalbo D., and Martinez J.P. Cell wall and secreted proteins of Candida albicans: identification, function and expression. Microbiology and Molecular Biology Reviews 62 (1998) 130-180
15. Chaky J., Anderson K., Moss M., and Vaillancourt L. Surface hydrophobicity and surface rigidity induce spore germination in Colletotrichum graminicola. Phytopathology 91 (2001) 558-564
16. Clement J.A., Martin S.G., Butt T.M., and Beckett A. Germination and the role of extracellular matrix in adhesion of urediniospores of Uromyces vicia-fabae to synthetic surfaces. Mycological Research 97 (1993) 585-593
17. Clement J.A., Porter R., Butt T.M., and Beckett A. Characterisics of adhesion pad formation during imbibition and germination of urediniospores of Uromyces vicia-fabae on host and synthetic surfaces. Mycological Research 101 (1997) 1445-1458
18. de Groot P.W.J., Ram A.F., and Klis F.M. Features and functions of covalently linked proteins in fungal cell walls. Fungal Genetics and Biology 42 (2005) 657-675
19. de Vries O.M.H., Fekkes M.P., Wosten H.A.B., and Wessels J.G.H. Insoluble hydrophobin complexes in the walls of Schizophyllum commune and other filamentous fungi. Archives of Microbiology 159 (1993) 330-335
20. Doss R.P., Potter S.W., Chastagnen G.A., and Christian J.K. Adhesion of non-germinated Botrytis cinerea conidia to several substrata. Applied and Environmental Microbiology 59 (1993) 1786-1791
21. Douaiher M.N., Halama P., and Janex-Favre M.-C. The ontogeny of Stagonospora nodorum pycnidia in culture. Sydowia 56 (2004) 39-50
22. Doughty J., Hedderson F., McCubbin A., and Dickinson H. Interaction between a coating-borne peptide of the brassica pollen grain and stigmatic S-locus-specifc glycoproteins. Proceedings of the National Academy of Sciences, USA 90 (1993) 467-471
23. Eyal Z. The Septoria tritici and Stagonospora nodorum blotch diseases of wheat. European Journal of Plant Pathology 105 (1999) 629-641
24. Faulkner M.J., and Colhoun J. Aerial dispersal of pycnidiospores of Leptosphaeria nodorum. Phytopathologische Zeitschrift 86 (1976) 357-360
25. Fontaine T., Simenel C., Dubreucq G., Adam O., Delepierre M., Lemoine J., Vorgias C.E., Diaquin M., and Latge J.-P. Molecular organisation of the alkali insoluble fraction of Aspergillus fumigatus cell wall. Journal of Biological Chemistry 275 (2000) 27594-27607
26. Hamer J.E., Howard R.J., Chumley F.G., and Valent B. A mechanism for surface attachment of spores of a plant pathogenic fungus. Science 239 (1988) 288-290
27. Hughes H.B., Carzaniga R., Rawlings S.L., Green J.R., and O'Connell R.J. Spore surface glycoproteins of Colletotrichum lindemuthianum are recognised by a monoclonal antibody which inhibits adhesion to polystyrene. Microbiology 145 (1999) 1927-1936
28. Hutchison K.A., Green J.R., Wharton P.S., and O'Connell R.J. Identification and localisation of glycoproteins in the extracellular matrices around germ-tubes and appressoria of Colletotrichum species. Mycological Research 106 (2002) 729-736
29. Kapteyn J.C., Hoyer L.L., Hecht J.E., Muller W.H., Andel A., and Verkleij A.J. The cell wall architecture of Candida albicans wild-type cells and cell wall defective mutants. Molecular Microbiology 35 (2000) 601-611
30. Karjalainen R., and Lounatmaa K. Ultrastructure of pycnidiospore walls and hyphae of Septoria nodorum. Transactions of the British Mycological Society 83 (1984) 239-244
31. Karjalainen R., and Lounatmaa K. Ultrastructure of penetration and colonisation of wheat leaves by Septoria nodorum. Physiological and Molecular Plant Pathology 29 (1986) 263-270
32. Kim Y., Liu Z., Daoxin L., and Kollatukudy P. Two novel genes induced by hard-surface contact of Colletotrichum gloeosporioides conidia. Journal of Bacteriology 182 (2000) 4688-4695
33. Klis F.M., Mol P., Hellingwerf K., and Brul S. Dynamics of cell wall structure in Saccharomyces cerevisiae. FEMS Microbiology Reviews 26 (2002) 239-256
34. Kuo K., and Hoch H.C. Germination of Phyllosticta ampelicida pycnidiospores: prerequisite of adhesion to the substratum and the relationship of substratum wettability. Fungal Genetics and Biology 20 (1996) 18-29
35. Kwon Y.H., and Epstein L. A 90 kDa glycoprotein associated with adhesion of Nectria haematococca macronidia to substrata. Molecular Plant-Microbe Interactions 6 (1993) 481-487
36. Laemmli U.K. Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227 (1970) 680-685
37. Marcilla A., Elorza M.V., Mormeneo S., Rico H., and Sentandreu R. Candida albicans mycelial wall structure: supramolecular complexes released by zymolase, chitinase and beta-mercaptoethanol. Archives of Microbiology 155 (1991) 312-319
38. Mercure E.W., Kunoh H., and Nicholson R.L. Adhesion of Colletotrichum graminicola conidia to corn leaves. A requirement for disease development. Physiological and Molecular Plant Pathology 45 (1994) 407-420
39. Mercure E.W., Kunoh H., and Nicholson R.L. Visualisation of materials released fron adhered, ungerminated conidia of Colletotrichum graminicola. Physiological and Molecular Plant Pathology 46 (1995) 121-135
40. Mercure E.W., Leite B., and Nicholson R.L. Adhesion of ungerminated conidia of Colletotrichum graminicola to artificial hydrophobic surfaces. Physiological and Molecular Plant Pathology 45 (1994) 421-440
41. Momany M., Lindsey R., Hill T.W., Richardson E.A., Momany C., and Pedreira M. The Aspergillus fumigatus cell wall is organised in domains that are remodelled during polarity establishment. Microbiology 150 (2004) 3261-3268
42. Mrsa V., Seidl T., Gentzsch M., and Tanner W. Specific labelling of cell wall proteins by biotinylation. Identification of four covalently linked O-mannosylated proteins of Saccharomyces cerevisiae. Yeast 13 (1997) 1145-1154
43. Newton A.C., and Caten C.E. Auxotrophic mutants of Septoria nodorum isolated by direct screening and by selection for resistance to chlorate. Transactions of the British Mycological Society 90 (1988) 199-207
44. Nicholson R.L. Adhesion of fungal propagules - significance to the success of the fungal infection process. In: Nicole M., and Gianinazzi-Pearson (Eds). Histology, Ultrastructure and Molecular Cytology of Plant-Microbe Interactions (1996), Kluwer Academic Publishers, Dordrecht 117-134
45. O'Connell R.J. Cytochemical analysis of infection structures of Colletotrichum lindemuthianum using fluorochrome-labelled lectins. Physiological and Molecular Plant Pathology 39 (1991) 189-200
46. Pain N.A., Green J.R., Jones G.L., and O'Connell R.J. Composition and organisation of extracellular matrices around germ tubes and appressoria of Colletotrichum lindemuthianum. Protoplasma 190 (1996) 119-130
47. Pain N.A., O'Connell R.J., Bailey J.A., and Green J.R. Monoclonal antibodies which show restricted binding to four Colletotrichum species: C. lindemuthianum, C. malvarum, C. orbiculare and C. trifolii. Physiological and Molecular Plant Pathology 40 (1992) 111-126
48. Robold A.V., and Hardham A.R. During attachment Phytophthora spores secrete proteins containing thrombospondin type 1 repeats. Current Genetics 47 (2005) 307-315
49. Schoffelmeer E.A., Vossen J.H., Van Doorn A.A., Cornelissen B.J., and Haring M.A. FEM1, a Fusarium oxysporum glycoprotein that is covalently linked to the cell wall matrix and is conserved in filamentous fungi. Molecular Genetics and Genomics 265 (2001) 143-152
50. Sela-Buurlage M.B., Epstein L., and Rodriguez R.J. Adhesion of ungerminated Colletotrichum musae conidia. Physiological and Molecular Plant Pathology 39 (1991) 345-352
51. Shaw B.D., and Hoch H.C. The pycnidiospore of Phyllosticta ampelicida: surface properties involved in substratum attachment and germination. Mycological Research 103 (1999) 915-924
52. Shaw B.D., Carroll G.C., and Hoch H.C. Generality of the prerequisite of conidium attachment to a hydrophobic substratum as a signal for germination among Phyllosticta species. Mycologia 98 (2006) 186-194
53. Solomon P.S., Lowe R.G.T., Tan K.-C., Water D.C., and Oliver R.P. Stagonospora nodorum: cause of Stagonospora nodorum blotch of wheat. Molecular Plant Pathology 7 (2006) 147-156
54. Solomon P.S., Wilson T.J.G., Rybak K., Parker K., Lowe R.G.T., and Oliver R.P. Structural characterisation of the interaction between Triticum aestivum and doththideomycete pathogen Stagonospora nodorum. European Journal of Plant Pathology 114 (2006) 275-282
55. Talbot N.J., Kershaw M.J., Wakley G.E., de Vries O.M.H., Wessesl J.G.H., and Hamer J.E. MPG1 encodes a fungal hydrophobin involved insurface interactions during infection-related development of Magnaporthe grisea. The Plant Cell 8 (1996) 985-999
56. Terhune B.T., and Hoch H.C. Substrate hydrophobicity and adhesion of Uromyces urediospores and germlings. Experimental Mycology 17 (1993) 241-252
57. Valentin E., Herrero W., Pastor J.F.I., and Sentandreu R. Solubilisation and analysis of mannoprotein molecules from the cell wall of Saccharomyces cerevisiae. Journal of General Microbiology 130 (1984) 1419-1428
58. Viret O., Toti L., Chapela I.H., and Petrini O. The role of the extracellular sheath in recognition and attachment of conidia of Discula umbrinella (Berk. & Br.) Morelet to the host surface. New Phytologist 127 (1994) 123-131
59. Xiao J.Z., Watanabe T., Kamakura T., Ohshima A., and Yamaguchi I. Studies on cellular differentiation of Magnaporthe grisea. Physicochemical aspects of substratum surfaces in relation to appressorium formation. Physiological and Molecular Plant Pathology 44 (1994) 227-236
60. Young D.H., and Kauss H. Adhesion of Colletotrichum lindemuthianum spores to Phaseolus vulgaris hypocotyls and to polystyrene. Applied and Environmental Microbiology 47 (1984) 616-619
61. Zelinger Z., Hawes C.R., Gurr S.J., and Dewey F.M. An immunocytochemical and ultra-structural study of the extracellular matrix produced by germinating spores of Stagonospora nodorum on natural and artificial surfaces. Physiological and Molecular Plant Pathology 65 (2004) 123-135
62. Zelinger Z., Hawes C.R., Gurr S.J., and Dewey F.M. Attachment and adhesion of conidia of Stagonospora nodorum to natural and artificial surfaces. Physiological and Molecular Plant Pathology 68 (2006) 209-215