Hydrophobins and repellents: Proteins with fundamental roles in fungal morphogenesis

Fungal Genetics and Biology

Volumn 23, Issue 1, 1998, Pages 18-33

  Kershaw, Michael J ^a   Talbot, Nicholas J ^a  

^a UNIVERSITY OF EXETER   (United Kingdom)

Author keywords

Aerial morphogenesis; Bimodular proteins; Clock control genes; Conidiation; Cysteine rich proteins; Filament formation; Fungal development; Mating type genes; Mushroom development

Indexed keywords

FUNGAL PROTEIN; SECRETORY PROTEIN;

CELL WALL; FUNGAL GENETICS; FUNGUS; FUNGUS HYPHAE; HYDROPHOBICITY; MORPHOGENESIS; NONHUMAN; PRIORITY JOURNAL; PROTEIN ASSEMBLY; REVIEW;

EID: 0031711659     PISSN: 10871845     EISSN: None     Source Type: Journal    
DOI: 10.1006/fgbi.1997.1022     Document Type: Review

References (83)

1. Arntz, C., and Tudzynski, P. 1997. Identification of genes induced in alkaloid-producing cultures of Claviceps sp. Curr. Genet. 31: 357-360.
2. Asgeìrsdòttir, S. A., Halsall, J. R., and Casselton, L. A. 1997. Expression of two closely linked hydrophobin genes of Coprinus cinereus is monokaryon-specific and down-regulated by the oid-1 mutation. Fungal Genet. Biol. (in press).
3. Banuett, F. 1995. The genetics of Ustilago maydis, a fungal pathogen that induces tumors in maize. Annu. Rev. Genet. 29: 179-208.
4. Baud, F., Pebay-Peyroula, E., Cohen-Adda, C., Odani, S., and Lehmann, M. S. 1993. Crystal structure of a hydrophobic protein from soybean: a member of a new cysteine-rich family. J. Mol. Biol. 231: 877-887.
5. Beckerman, J. L., and Ebbole, D. J. 1996. MPG1, a gene encoding a fungal hydrophobin of Magnaporthe grisea, is involved in surface recognition. Mol. Plant-Microb. Interact. 9: 450-456.
6. Beever, R. E., and Dempsey G. P. 1978. Function of rodlets on the surface of fungal spores. Nature 272: 608-610.
7. Bell-Pederson, D., Dunlap, J. C., and Loros, J. J. 1992. The Neurospora circadian clock-controlled gene, ccg-2, is allelic to eas and encodes a fungal hydrophobin required for formation of the conidial rodlet layer. Genes Dev. 6: 2382-2394.
8. Bell-Pederson, D., Dunlap, J. C., and Loros, J. J. 1996. Distinct cis-acting elements mediate clock, light, and developmental regulation of the Neurospora crassa EAS (ccg-2) gene. Mol. Cell Biol. 16: 513-521.
9. Bidochka, M. J., St. Leger, R. J., Joshi, L., and Roberts, D. W. 1995. The rodlet layer from aerial and submerged conidia of the entomopathogenic fungus Beauvaria bassiana contains hydrophobin. Mycol. Res. 99: 403-406.
10. Bohlmann, R. 1996. Isolierung und characterisierung van filamentwspezifisch exprimierten gene vo Ustilago maydis. Ph.D. thesis, University of München.
11. Bostian, K. A., Elliott, Q., Bussey, H., Burn, V., Smith, A., and Tipper, D. J. 1984. Sequence of the preprotoxin dsRNA gene of type I killer yeast: Multiple processing events produce a two-component toxin. Cell 36: 741-751.
12. Bowden, C. G., Hintz, W. E., Jeng, R., Hubber, M., and Horgen, P. 1993. Isolation and characterization of the cerato-ulmin toxin gene of the Dutch elm disease pathogen Ophiostoma ulmi. Curr. Genet. 25: 223-229.
13. Bowden, C. G., Smalley E., Guries, R. P., Hubbes, M., and Horgen, P. A. 1996. Lack of association between cerato-ulmin production and virulence in Ophiostoma novo-ulmi. Mol. Plant-Microb. Interact. 9: 556-564.
14. Brasier, C. M., Kirk, S. A., and Tegli, S. 1995. Naturally occurring non cerato-ulmin producing mutants of Ophiostoma novo-ulmi are pathogenic but lack aerial mycelium. Mycol. Res. 99: 436-440.
15. Carpenter, C. E., Mueller, R. J., Kazmierczak, P., Zhang, L., Villalon, D. K., and Van Alfen, N. K. 1992. Effect of a virus on the accumulation of a tissue-specific cell-surface protein of the fungus Cryphonectria parasitica. Mol. Plant-Microb. Interact. 4: 55-61.
16. Castonguay, Y., Laberge, S., Nadeau, P., and Vézina, L.-P. 1994. A cold-induced gene from Medicago sativa encodes a bimodular protein similar to developmentally regulated proteins. Plant Mol. Biol. 24: 799-804.
17. Chang, Y. C., and Timberlake, W. E. 1993. Identification of Aspergillus brlA response elements (BREs) by genetic selection in yeast. Genetics 13: 29-38.
18. de Vries, O. M. H., Fekkes, M. P., Wosten, H. A. B., and Wessels, J. G. H. 1993. Insoluble hydrophobin complexes in the walls of Schizophyllum commune and other filamentous fungi. Arch. Microbiol. 159: 330-335.
19. de Groot, P. W. J., Schaap, P. J., Sonnenberg, A. S. M., Visser, J., and Van Griensven, L. J. L. D. 1996. The Agaricus bisporus HypA gene encodes a hydrophobin and specifically accumulates in peel tissue of mushroom caps during fruit body development. J. Mol. Biol. 257: 1008-1018.
20. Dempsey, G. P., and Beever, R. E. 1979. Electron microscopy of the rodlet layer of Neurospora crassa conidia. J. Bacteriol. 139: 757-761.
21. Désormeaux, A., Blochet, J.-E., Pézolet, M., and Marion, D. 1992. Amino acid sequence of a non-specific wheat phospholipid transfer protein and its conformation as revealed by infrared and Raman spectroscopy. Role of disulfide bridges in the stabilization of the α-helix structure. Biochim. Biophys. Acta 1121: 137-152.
22. Fuller, R. S., Sterne, R. E., and Thorner, J. 1988. Enzymes required for yeast prohormone processing. Annu. Rev. Physiol. 50: 345-362.
23. Hess, W. M., Sassen, M. M. A., and Remson, C. C. 1968. Surface characteristics of Penicillium conidia. Mycologia 60: 290-303.
24. Honegger, R. (1993). Developmental biology of lichens. New Phytol. 125: 659-677.
25. José-Estanyol, M., Ruiz-Avila, L., and Puigdomenech, P. 1992. A maize embryo-specific gene encodes a proline-rich and hydrophobic protein. Plant Cell 4: 413-423.
26. Kaldenhoff, R., and Russo, V. E. A. 1993. Promoter analysis of the bli-7/eas gene. Curr. Genet. 24: 394-399.
27. Kazmierczak, P., Pfeiffer, P., Zhang, L., and Van Alfen, N. K. 1996. Transcriptional repression of specific host genes by the mycovirus Cryphonectria-hypovirus-1. J. Virol. 70: 1137-1142.
28. Lau, G., and Hamer, J. E. 1996. Regulatory genes controlling MPG1 expression and pathogenicity in the rice blast fungus Magnaporthe grisea. The Plant Cell 8: 771-781.
29. Lauter, F. R., Russo, V. E. A., and Yanofsky C. 1992. Developmental and light regulation of Eas, the structural gene for the rodlet protein of Neurospora crassa. Genes Dev. 6: 2373-2381.
30. Lora, J. M., Pinto-Toro, J. A., Bentítez, T., and Romero, L. C. 1995. Qid3 protein links plant bimodular proteins with fungal hydrophobins. Mol. Microbiol. 18: 380-382.
31. Lugones, L. G., Bosscher, J. S., Scholtmeyer, K., de Vries, O. M. H., and Wessels, J. G. H. 1996. An abundant hydrophobin (ABH1) forms hydrophobic rodlet layers in Agaricus bisporus fruiting bodies. Microbiology 142: 1321-1329.
32. Mendgen, K., and Deising, H. 1993. Infection structures of fungal plant pathogens - A cytological and physiological evaluation. New Phytol. 124: 193-213.
33. Mulder, G. H., and Wessels, J. G. H. (1986) Molecular cloning of mRNAs differentially expressed in monokaryons and dikaryons of Schizophyllum commune. Exp. Mycol. 10: 214-227.
34. Nakari-Setälä, T., Aro, N., Kalkkinen, N., Alatalo, E., and Penttila, M. 1996. Genetic and biochemical characterization of the Trichoderma reesei hydrophobin HFB1. Eur. J. Biochem. 235: 248-255.
35. Okamoto, H., Otani, H., and Takai, S. 1986. Effect of cerato-ulmin (CU) on electrogenic pumps of elm cell membrane and ion loss from cells. Phytopathol. 76: 116 (Abstr.).
36. Parta, M., Chang, Y., Rulong, S., Pinto da Silva, P., and KwonChung, K. J. 1994. Hyp1, a hydrophobin gene from Aspergillus fumigatus complements the rodletless phenotype in Aspergillus nidulans. Infect. Immun. 62: 4389-4395.
37. Richards, W. C. 1993. Cerato-ulmin: A unique wilt toxin of instrumental significance in the development of Dutch elm disease. In Dutch Elm Disease Research, Cellular and Molecular Approaches (M. B. Sticklen and J. L. Sherald, Eds.), pp. 89-151. Springer-Verlag, New York.
38. Richards, W. C., and Takai, S. 1993. Amino acid sequence and spectroscopic studies of Dutch elm disease toxin, cerato-ulmin. In Dutch Elm Disease Research, Cellular and Molecular Approaches (M. B. Sticklen and J. L. Sherald, Eds.), pp. 152-170. Springer-Verlag, New York.
39. Rohe, M., Gierlich, A., Hermann, H., Hahn, M., Schmidt, B., Rosahl, S., and Knogge, W. 1995. The race-specific elicitor, NIP 1, from the barley pathogen, Rhynchosporium secalis, determines avirulence on host plants of the Rrsl resistance genotype. EMBO J. 14: 4168-4177.
40. Russo, P. S., Blum, F. D., Ipsen, J. D., Abul-Hajj, Y. J., and Miller, W. G. 1982. The surface activity of the phytotoxin cerato-ulmin. Can. J. Bot. 60: 1414-1422.
41. Schuren, F. H. J., and Wessels, J. G. H. 1990. Two genes specifically expressed in fruiting dikaryons of Schizophyllum commune: homologies with a gene not regulated by mating type genes. Gene 90: 199-205.
42. Selitrennikof, C. P. 1976. Easily wettable, a new mutant. Neurospora Newslett. 23: 23.
43. Spanu, P. 1997. HCf-1, a hydrophobin from the tomato pathogen Cladosporium fulvum. Gene 193: 89-96.
44. St. Leger, R. J., Staples, R. C., and Roberts, D. W. 1992. Cloning and regulatory analysis of starvation-stress gene, ssgA, encoding a hydrophobin-like protein from the entomopathogenic fungus Metarhizium anisopliae. Gene 120: 119-124.
45. Sterk, P., Booij, H., Schellekens, G. A., Van Kammen, A., and de Vries, S. C. 1991. Cell-specific expression of the carrot lipid transfer protein gene. Plant Cell 3: 907-921.
46. Sticklen, M. B., and Bolyard, M. 1994. Refinement of physiological roles for cerato-ulmin by analogy with other hydrophobins. Trends Microbiol. 2: 213-215.
47. Stringer, M. A., and Timberlake, W. E. 1993. Cerato-ulmin, a toxin involved in Dutch Elm disease, is a fungal hydrophobin. Plant Cell. 5: 145-146.
48. Stringer, M. A., and Timberlake, W. E. 1995. dewA encodes a fungal hydrophobin component of the Aspergillus spore wall. Mol. Microbiol. 16: 33-44.
49. Stringer, M. A., Dean, R. A., Sewell, T. C., and Timberlake, W. E. 1991. Rodletless, a new Aspergillus developmental mutant induced by directed gene inactivation. Genes Dev. 5: 1161-1171.
50. Tagu, D., Nasse, B., and Martin, F. 1996. Cloning and characterization of hydrophobin-encoding cDNAs from the ectomycorrhizal basidiomycete Pisolithus tinctorius. Gene 168: 93-97.
51. Takai, S. 1974. Pathogenicity and cerato-ulmin production in Ceratocystis ulmi. Nature 252: 124-126.
52. Takai, S. 1980. Relationship of the production of toxin, cerato-ulmin, to synnemata formation, pathogenicity, mycelial habit, and growth of Ceratocystis ulmi isolates. Can. J. Bot. 58: 658-662.
53. Takai, S., and Hiratsuka, Y. 1980. Accumulation of the material containing the toxin cerato-ulmin on the hyphal surface of Ceratocystis ulmi. Can. J. Bot. 58: 658-662.
54. Takai, S., and Hiratsuka, Y. 1984. Scanning electron microscope observations of internal symptoms of white elm following Ceratocystis ulmi infection and cerato-ulmin treatment. Can. J. Bot. 62: 1365-1371.
55. Takai, S., and Richards, W. C. 1978. Cerato-ulmin, a wilting toxin of Ceratocystis ulmi: Isolation and some properties of cerato-ulmin from the culture of C. ulmi. J. Phytopathol. 91: 129-146.
56. Talbot, N. J. 1995. Having a blast: Exploring the pathogenicity of Magnaporthe grisea. Trends Microbiol. 3: 9-16.
57. Talbot, N. J. 1997. Fungal biology: Growing into the air. Curr. Biol. 7: R78-82.
58. Talbot, N. J., Ebbole, D. J., and Hamer, J. E. 1993. Identification and characterization of MPG1, a gene involved in pathogenicity from the rice blast fungus Magnaporthe grisea. Plant Cell 5: 1575-1590.
59. Talbot, N. J., Kershaw, M. J., Wakley, G. E., de Vries, O. M. H., Wessels, J. G. H., and Hamer, J. E. 1996. MPG1 encodes a fungal hydrophobin involved in surface interactions during infection-related development by Magnaporthe grisea. Plant Cell 8: 985-989.
60. Teeter, M. M., and Whitlow, M. D. 1986. Hydrogen boding in the high resolution structure of the protein crambin. Trans. Am. Cryst. Assoc. 22: 75-89.
61. Temple, B., Hintz, W. E., Bernier, L., and Horgen, P. A. 1997. The biological role of the hydrophobin cerato-ulmin in the life history of Ophiostoma ulmi and O. novo-ulmi. Fungal Genet. Newslett. 44: (in press). [Abstract 19th Fungal Genetics Conference]
62. Templeton, M. D., Greenwood, D. R., and Beever, R. E. 1995. Solubilization of Neurospora crassa rodlet proteins and identification of the predominant protein as the proteolytically processed eas (ccg-2) gene product. Exp. Mycol. 19: 166-169.
63. Templeton, M. D., Rikkerink, E. H. A., and Beever, R. E. 1994. Small, cysteine-rich proteins and recognition in fungal-plant interactions. Mol. Plant-Microb. Interact. 7: 320-325.
64. Thau, N., Monod, M., Crestani, B., Rolland, C., Tronchin, G., Latge, J. P., and Paris, S. 1994. Rodletless mutants of Aspergillus fumigatus. Infect. Immun. 62: 4380-4388.
65. Van den Ackervecken, G. F. J. M., Van Kan, J. A. L., and De Wit, P. J. G. M. 1992. Molecular analysis of the avirulence gene avr9 of the fungal tomato pathogen Cladosporium fulvum fully supports the gene-for-gene hypothesis. Plant J. 2: 359-366.
66. Van der Vegt, W., Van der Mei, H. C., Wösten, H. A. B., Wessels, J. G. H., and Busscher, H. J. 1996. A comparison of the surface activity of the fungal hydrophobin Sc3p with those of other proteins. Biophys. Chem. 51: 253-260.
67. Van Wetter, M.-A., Schuren, F. H. J., Schuurs, T. A., and Wessels, J. G. H. 1996. Targeted mutation of the Sc3 hydrophobin gene of Schizophyllum commune affects formation of aerial hyphae. FEMS Microbiol. Lett. 140: 265-269.
68. Wessels, J. G. H. 1992. Gene expression during fruiting in Schizophyllum commune. Mycol. Res. 96: 609-620.
69. Wessels, J. G. H. 1994. Developmental regulation of fungal cell wall formation. Annu. Rev. Phytopathol. 32: 413-437.
70. Wessels, J. G. H. 1996. Fungal hydrophobins: Proteins that function at an interface. Trends Plant Sci. 1: 9-15.
71. Wessels, J. G. H. 1997. Hydrophobins: Proteins that change the nature of the fungal surface. Adv. Microbial Physiol. 38: 1-45.
72. Wessels, J. G. H., de Vries, O. M. H., Ásgeirsdóttir, S. A., and Schuren, F. H. J. 1991a. Hydrophobin genes involved in formation of aerial hyphae and fruit bodies in Schizophyllum. Plant Cell 3: 793-799.
73. Wessels, J. G. H., de Vries, O. M. H., Ásgeirsdóttir, S. A., and Springer, J. 1991b. The thn mutation of Schizophyllum commune, which suppresses formation of aerial hyphae, affects expression of the Sc3 hydrophobin gene. J. Gen. Microbiol. 137: 2439-2445.
74. Willey, J., Santamaria, R., Guijarro, J., Geistlich, M., and Losick, R. 1991. Extracellular complementation of a developmental mutation implicates a small sporulation protein in aerial mycelium formation by S. coelicolor. Cell 65: 641-650.
75. Willey, J., Schwedock, J., and Losick, R. 1993. Multiple extracellular signals govern production of a morphogenetic protein involved in aerial mycelium formation by Streptomyces coelicolor. Genes Dev. 7: 895-903.
76. Williams, S. J., Bradshaw, R. M., Costerton, J. W., and Forge, A. 1972. Fine structure of the spore sheath of some Streptomyces species. J. Gen. Microbiol. 72: 249-258.
77. Wösten, H. A. B., de Vries, O. M. H., and Wessels, J. G. H. 1993. Interfacial self-assembly of a fungal hydrophobin into a hydrophobic rodlet layer. Plant Cell 5: 1567-1574.
78. Wösten, H. A. B., Ásgeirsdóttir, S. A., Krook, J. H., Drenth, J. H. H., and Wessels, J. G. H. 1994a. The fungal hydrophobin Sc3p self-assembles at the surface of aerial hyphae as a protein membrane constituting the hydrophobic rodlet layer. Eur. J. Cell Biol. 63: 122-129.
79. Wösten, H. A. B., Schuren, F. H. J., and Wessels, J. G. H. 1994b. Interfacial self-assembly of a hydrophobin into an amphipathic membrane mediates fungal attachment to hydrophobic surfaces. EMBO J. 13: 5848-5854.
80. Wösten, H. A. B., Ruardy T. G., Van der Mei, H. C., Busscher, H. J., and Wessels, J. G. H. 1995. Interfacial self-assembly of a Schizophyllum commune hydrophobin into an insoluble amphipathic membrane depends on surface hydrophobicity. Colloids Surfaces B. 5, 189-195.
81. Wösten, H. A. B., Bohlmann, R., Eckerskom, C., Lottspeich, F., Bolker, M., and Kahmann, R. 1996. A novel class of small amphipathic peptides affect aerial growth and surface hydrophobicity in Ustilago maydis. EMBO J. 16: 4274-4281.
82. Yaguchi, M., Pusztai-Carey M., Roy, C., Surewicz, W. K., Carey P. R., Stevenson, K. J., Richards, W. C., and Takai, S. 1993. Amino acid sequence and spectroscopic studies of Dutch elm disease toxin, cerato-ulmin. In Dutch Elm Disease Research, Cellular and Molecular Approaches (M. B. Sticklen and J. L. Sherald, Eds.), pp. 152-170. Springer-Verlag, New York.
83. Zhang, L., Villalon, D., Sin, Y., Kazmierczak, P., and Van Alfen, N. K. 1994. Virus-associated down-regulation of the gene encoding cryparin, an abundant cell surface protein of the chestnut blight fungus Cryphonectria parasitica. Gene 139: 59-64.