Cell wall proteins of the ectomycorrhizal basidiomycete Pisolithus tinctorius: Identification, function, and expression in symbiosis

Fungal Genetics and Biology

Volumn 27, Issue 2-3, 1999, Pages 161-174

  Martin, Francis ^a   Laurent, Pascal ^a   De Carvalho, Dulcinéia ^a   Voiblet, Catherine ^a   Balestrini, Raffaella ^b   Bonfante, Paola ^b   Tagu, Denis ^a  

^a CEMAGREF   (France)

^b UNIVERSITY OF TURIN   (Italy)

Author keywords

Cell wall proteins; Ectomycorrhiza; Eucalyptus; Fungal development; Mannoproteins; Pisolithus; Plant microbe interactions; Symbiosis regulated proteins

Indexed keywords

ADHESIN; CELL MEMBRANE PROTEIN;

BASIDIOMYCETES; CYTOSKELETON; GENE FUNCTION; NONHUMAN; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN EXPRESSION; REVIEW; SYMBIOSIS;

BASIDIOMYCOTA; EUCALYPTUS; FUNGI; MYCORRHIZAE; PISOLITHUS; PISOLITHUS TINCTORIUS;

EID: 0032830487     PISSN: 10871845     EISSN: None     Source Type: Journal    
DOI: 10.1006/fgbi.1999.1138     Document Type: Review

References (86)

1. Adams, T. H., Wieser, J. K., and Yu, J. H. 1998. Asexual sporulation in Aspergillus nidulans. Microbiol. Mol. Biol. Rev. 62: 35-54.
2. Albrecht, C., Geurts, R., Lapeyrie, F., and Bisseling, T. 1998. Endomycorrhizae and rhizobial Nod factors both require SYM8 to induce the expression of the early nodulin genes PsENOD5 and PsENOD12A. Plant J. 15: 605-614.
3. Balestrini, R., Hahn, M. G., and Bonfante, P. 1996. Location of cell-wall components in ectomycorrhizae of Corylus avellana and Tuber magnatum. Protoplasma 191: 55-69.
4. Barker, S. J., Tagu, D., and Delp, G. 1998. Regulation of root and fungal morphogenesis in mycorrhizal symbioses. Plant Physiol. 116: 1201-1207.
5. Barrett, V., Dixon, R. K., and Lemke, P. A. 1990. Genetic transformation of a mycorrhizal fungus. Appl. Microbiol. Biotechnol. 33: 313-316.
6. Béguiristain, T., and Lapeyrie, F. 1997. Host plant stimulates hypaphorine accumulation in Pisolithus tinctorius hyphae during ectomycorrhizal infection while excreted fungal hypaphorine controls root hair development. New Phytol. 136: 525-532.
7. Bills, S. N., Richter, D. L., and Podila, G. K. 1995. Genetic transformation of the ectomycorrhizal fungus Paxillus involutus by particle bombardment. Mycol. Res. 99: 557-561.
8. Bonfante, P., Balestrini, R., Martino, E., Perotto, S., Plassard, C., and Mousain, D. 1998. Morphological analysis of early contacts between pine roots and two ectomycorrhizal Suillus strains. Mycorrhiza 8: 1-10.
9. Burgess, T. 1995. Changes in Protein Biosynthesis Associated with the Development of Pisolithus-Eucalyptus grandis ectomycorrhizas. Ph.D. thesis, Murdoch University, Western Australia.
10. Burgess, T., Laurent, P., Dell, B., Malajczuk, N., and Martin, F. 1995. Effect of the fungal isolate aggressivity on the biosynthesis of symbiosis-related polypeptides in differentiating eucalypt ectomycorrhiza. Planta 195: 408-417.
11. Celerin, M., Ray, J. M., Schisler, N. J., Day, A. W., Stetler-Stevenson, W. G., and Laudenbach, D. E. 1996. Fungal fimbriae are composed of collagen. EMBO J. 15: 4445-4453.
12. Chaffin, W. L., Lopez-Ribot, J. L., Casanova, M., Gozalbo, D., and Martinez, J. P. 1998. Cell wall and secreted proteins of Candida albicans: Identification, function, and expression. Microbiol. Mol. Biol. Rev. 62: 130-180.
13. Chalot, M., and Botton, B. 1999. Nitrogen assimilation: Enzymology in ectomycorrhizas. In Mycorrhiza: Structure, Molecular Biology and Function (A. K. Varma, B. Hock, Eds.), 2nd ed. pp. 333-372, Springer-Verlag, Berlin/Heidelberg/New York.
14. Cleves, A. E. D., Cooper, D. N. W., Barondes, S. H., and Kelly, R. B. 1996. A new pathway for protein export in Saccharomyces cerevisiae. J. Cell Biol. 133: 1017-1026.
15. Cid, V. J., Duran, A., Del Rey, F., Snyder, M. P., Nombela, C., and Sanchez, M. 1995. Molecular basis of cell integrity and morphogenesis in Saccharomyces cerevisiae. Microbiol. Rev. 59: 345-386.
16. Dean, R. A. 1997. Signal pathways and appressorium morphogenesis. Annu. Rev. Phytopathol. 35: 211-234.
17. De Carvalho, D. 1994. Contribution à l'étude des protéines régulées par la symbiose ectomycorhizienne. Ph.D. thesis, Ecole Nationale du Génie Rurale et Forestier, Nancy, France.
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. Dexheimer, J., and Pargney, J. C. 1991. Comparative anatomy of the host-fungus interface in mycorrhizas. Experientia 47: 312-320.
20. Dexheimer, J., Gérard, J., and Genet, P. 1994. Study of transformations of the root system of Eucalyptus globulus associated with Pisolithus tinctorius. I. Aptitude to mycorrhization of different kinds of roots. Phytomorphology 44: 235-245.
21. Faik, A., Labouré, A. M., Gulino, D., Mandaron, P., and Falconet, D. 1998. A plant surface protein sharing structural properties with animal integrins. Eur. J. Biochem. 253: 552-559.
22. Fries, N., Serck-Hanssen, K., Häll Dimberg, L., and Theander, O. 1987. Abietic acid, an activator of basidiospore germination in ectomycorrhizal species of the genus Suillus (Boletaceae). Exp. Mycol. 11: 360-363.
23. Gea, L., Normand, L., Vian, B., and Gay, G. 1994. Structural aspects of ectomycorrhiza of Pinus pinaster (Ait.) Sol. formed by an IAA-overproducer mutant of Hebeloma cylindrosporum Romagnési. New Phytol. 128: 659-670.
24. Gianinazzi-Pearson, V. 1996. Plant cell responses to arbuscular mycorrhizal fungi: Getting to the roots of the symbiosis. Plant Cell 8: 1871-1883.
25. Giollant, M., Guillot, J., Damez, M., Dusser, M., Didier, P., and Didier, E. 1993. Characterization of a lectin from Lactarius deterrimus. Research on the possible involvement of the fungal lectin in recognition between mushroom and spruce during the early stages of mycorrhizae formation. Plant Physiol. 101: 513-522.
26. Hampp, R., and Schaeffer, C. 1999. Mycorrhiza - carbohydrates and energy metabolism. In Mycorrhiza: Structure, Molecular Biology and Function (A. K. Varma, B. Hock, Eds.), pp. 273-304, Springer-Verlag, Berlin/Heidelberg/New York.
27. Hardham, A. R., and Mitchell, H. J. 1998. Use of molecular cytology to study the structure and biology of phytopathogenic and mycorrhizal fungi. Fungal. Genet. Biol. 24: 252-284.
28. Harrison, M. J. 1998. Development of the arbuscular mycorrhizal symbiosis. Curr. Opin. Plant Biol. 1: 360-365.
29. Hilbert, J. L., Costa, G., and Martin, F. 1991. Ectomycorrhizin synthesis and polypeptide changes during the early stage of eucalypt mycorrhiza development. Plant Physiol. 97: 977-984.
30. Horan, D. P., and Chilvers, G. A. 1990. Chemotropism: The key to ectomycorrhizal formation? New Phytol. 116: 297-301.
31. Jacobs, P. F., Peterson, R. L., and Massicotte, H. B. 1989. Altered fungal morphogenesis during early stages of ectomycorrhiza formation in Eucalyptus pilularis. Scanning Microsc. 3: 249-255.
32. Jones, E. B. G. 1994. Fungal adhesion. Mycol. Res. 98: 961-981.
33. Kershaw, M. J., and Talbot, N. J. 1998. Hydrophobins and repellents: Proteins with fundamental roles in fungal morphogenesis. Fungal Genet. Biol. 23: 18-33.
34. Kim, S. J., Hiremath, S. T., and Podila, G. K. 1998a. Cloning and identification of symbiosis-regulated genes from the ectomycorrhizal Laccaria bicolor. Mycol. Res. 103: 168-172.
35. Kim, S. J., Zheng, J., Hiremath, S. T., and Podila, G. K. 1998b. Cloning and characterization of a symbiosis-related gene from an ectomycorrhizal fungus Laccaria bicolor. Gene 222: 203-212.
36. Kondoh, O., Muto, A., Kajiwara, S., Takagi, J., Saito, Y., and Shishido, K. 1995. Fruiting body-specific cDNA, mftAc, from the mushroom Lentinus edodes encodes a high-molecular-weight cell-adhesion protein containing an Arg-Gly-Asp motif. Gene 154: 31-37.
37. Kottke, I. 1997. Fungal adhesion pad formation and penetration of root cuticle in early stage mycorrhizas of Picea abies and Laccaria amethystea. Protoplasma 196: 55-64.
38. Lapeyrie, F., and Mendgen, K. 1993. Quantitative estimation of surface carbohydrates of ectomycorrhizal fungi in pure culture and during Eucalyptus root infection. Mycol. Res. 97: 603-609.
39. Lapeyrie, F., Lei, J., Malajczuk, N., and Dexheimer, J. 1989. Ultrastructural and biochemical changes at the pre-infection stage of mycorrhizal formation by two isolates of Pisolithus tinctorius. Ann. Sci. For. 46s: 754s-757s.
40. Laurent, P. 1995. Contribution à l'étude des protéines régulées par la symbiose chez l'ectomycorhize d'Eucalyptus - Pisolithus. Caractérisation de mannoprotéines pariétales chez le basidiomycète Pisolithus tinctorius. Ph.D. thesis, University Henri Poincaré-Nancy 1, France.
41. Laurent, P., Tagu, D., De Carvalho, D., Nehls, U., De Bellis, R., Balestrini, R., Bauw, G., Bonfante, P., and Martin, F. 1999. Cell wall acidic polypeptides in Pisolithus tinctorius are up-regulated during the development of Eucalyptus globulus ectomycorrhiza. Mol. Plant-Microb. Interact., in press.
42. Leahy, D. J., Aukhil, I., and Erikson, H. P. 1996. A crystal structure of a four-domain segment of human fibronectin encompassing the RGD loop and synergy region. Cell 84: 155-164.
43. Lei, J., Lapeyrie, F., Malajczuk, N., and Dexheimer, J. 1990. Infectivity of pine and eucalypt isolates of Pisolithus tinctorius on roots of Eucalyptus urophylla in vitro. II. Ultrastructural and biochemical changes at the early stage of mycorrhiza formation. New Phytol. 116: 115-122.
44. Lei, J., Wong, K. K., and Piché, Y. 1991. Extracellular concanavalin A-binding sites during early interactions between Pinus banksiana and two closely related genotypes of the ectomycorrhizal basidiomycete Laccaria bicolor. Mycol. Res. 95: 357-363.
45. Marmeisse, R., Gay, G., Debaud, J. C., and Casselton, L. A. 1992. Genetic transformation of the symbiotic basidiomycete fungus Hebeloma cylindrosporum. Curr. Genet. 22: 41-45.
46. Martin, F., and Hilbert, J. L. 1991. Morphological, biochemical and molecular changes during ectomycorrhiza development. Experientia 47: 321-331.
47. Martin, F., and Botton, B. 1993. Nitrogen metabolism of ectomycorrhizal fungi and ectomycorrhiza. Adv. Plant Pathol. 9: 83-102.
48. Martin, F., and Tagu, D. 1999. Developmental biology of a plant - fungus symbiosis: The ectomycorrhiza. In Mycorrhiza: Structure, Function, Molecular Biology and Biotechnology (A. K. Varma, B. Hock, Eds.), pp. 51-73, Springer-Verlag, Berlin/Heidelberg.
49. Martin, F., Laurent, P., De Carvalho, D., Burgess, T., Murphy, P., Nehls, U., and Tagu, D. 1995. Fungal gene expression during ectomycorrhiza formation. Can. J. Bot. 73: S541-S547.
50. Martin, F., Lapeyrie, F., and Tagu, D. 1997. Altered gene expression during ectomycorrhiza development. In The Mycota. Vol. VI. Plant Relationships (P. Lemke and G. Caroll, Eds.), pp. 223-242, Springer-Verlag, Berlin.
51. Massicotte, H. B., Peterson, R. L., Ackerley, C. A., and Melville, L. H. 1990. Structure and ontogeny of Betula alleghaniensis - Pisolithus tinctorius ectomycorrhizae. Can. J. Bot. 68: 579-593.
52. Massicotte, H. B., Peterson, R. L., and Ashford, A. E. 1987. Ontogeny of Eucalyptus pilularis - Pisolithus tinctorius ectomycorrhizae. II. Transmission electron microscopy. Can. J. Bot. 65: 1940-1947.
53. Mendgen, K., and Deising, H. 1993. Infection structures of fungal plant pathogens: A cytological and physiological evaluation. New Phytol. 124: 193-213.
54. Moore, D. 1998. Fungal Morphogenesis. British Mycological Society, London.
55. Nehls, U., Béguiristain, T., Ditengou, F., Lapeyrie, F., and Martin, F. 1998. The expression of a symbiosis-regulated gene in eucalypt roots is regulated by auxins and hypaphorine, the tryptophan betaine of the ectomycorrhizal basidiomycete Pisolithus tinctorius. Planta 207: 296-302.
56. Paris, F., Dexheimer, J., and Lapeyrie, F. 1993. Cytochemical evidence of a fungal cell wall alteration during infection of Eucalyptus roots by the ectomycorrhizal fungus Cenococcum geophilum. Arch. Microbiol. 159: 526-529.
57. Peterson, R. L., and Bonfante, P. 1994. Comparative structure of vesicular-arbuscular mycorrhizas and ectomycorrhizas. Plant Soil 159: 79-88.
58. Peterson, R. L., and Farquhar, M. L. 1994. Mycorrhizas integrated development between roots and fungi. Mycologia 86: 311-326.
59. Pierschbacher, M. D., and Ruoslahti, E. 1984. Cell attachment activity of fibronectin can be duplicated by small synthetic fragments of the molecule. Nature 309: 30-33.
60. Rosado, S. C. S., Kropp, B. R., and Piché, Y. 1994a. Genetics of ectomycorrhizal symbiosis. I. Host plant variability and heritability of ectomycorhizal and root traits. New Phytol. 126: 105-110.
61. Rosado, S. C. S., Kropp, B. R., and Piché, Y. 1994b. Genetics of ectomycorrhizal symbiosis. II. Fungal variability and heritability of ectomycorrhizal traits. New Phytol. 126: 111-117.
62. Ruoslahti, E. 1996. RGD and other recognition sequences for integrins. Annu. Rev. Cell Dev. Biol. 12: 697-715.
63. 2 synthesis of Picea abies cells. Planta 203: 470-479.
64. Salzer, P., Hebe, G., Reith, A., Zitterell-Haid, B., Stransky, H., Gaschler, K., and Hager, A. 1995. Rapid reactions of spruce cells to elicitors released from the ectomycorrhizal fungus Hebeloma crustuliniforme, and inactivation of these elicitors by extracellular spruce cell enzymes. Planta 198: 118-126.
65. Salzer, P., Hübner, B., Sirrenberg, A., and Hager, A. 1997b. Differential effect of purified spruce chitinases and β-1,3-glucanases on the activity of elicitors from ectomycorrhizal fungi. Plant Physiol. 114: 957-968.
66. Smith, S. E., and Smith, F. A. 1990. Structure and function of the interfaces in biotrophic symbioses as they relate to nutrient transport. New Phytol. 114: 1-38.
67. Smith, S. E., and Read, D. J. 1997. Mycorrhizal Symbiosis. 2nd ed., Academic Press, London.
68. Stringer, M. A., Dean, R. A., Sewall, T. C., and Timberlake, W. E. 1991. Rodletless, a new Aspergillus developmental mutant induced by directed gene activation. Genes Dev. 5: 1161-1171.
69. Tagu, D., and Martin, F. 1995. Expressed sequence tags of randomly selected cDNA clones from Eucalyptus globulus - Pisolithus tinctorius ectomycorrhiza. Mol. Plant-Microb. Interact. 8: 781-783.
70. Tagu, D., Nasse, B., and Martin, F. 1996. Cloning and characterization of hydrophobins-encoding cDNAs from the ectomycorrhizal Basidiomycete Pisolithus tinctorius. Gene 168: 93-97.
71. Tagu, D., Kottke, I., and Martin, F. 1998. Hydrophobins in ectomycorhizal symbiosis: Hypothesis. Symbiosis 25: 5-18.
72. Tagu, D., De Bellis, R., Balestrini, R., Piccoli, G., Stocchi, V., Bonfante, P., and Martin, F. 1999. Localization of the HYDPt-1 hydrophobin from the ectomycorrhizal basidiomycete Pisolithus tinctorius during colonization of Eucalyptus globulus roots. Submitted for publication.
73. Talbot, N. J. 1995. Having a blast: Exploring the pathogenicity of Magnaporthe grisea. Trends Microbiol. 3: 9-16.
74. 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.
75. 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 of Magnaporthe grisea. Plant Cell 8: 985-999.
76. Unestam, T., and Sun, Y. P. 1995. Extramatrical structures of hydrophobic and hydrophilic ectomycorrhizal fungi. Mycorrhiza 5: 301-311.
77. Wessels, J. G. H., de Vries, O. M. H., Asgeirsdottirs, A., and Schuren, F. H. J. 1991. Hydrophobin genes involved in formation of aerial hyphae and fruit bodies in Schizophyllum. Plant Cell 3: 793-799.
78. Wessels, J. G. H. 1993. Wall growth, protein excretion and morphogenesis in fungi. New Phytol. 123: 397-413.
79. Wessels, J. G. H. 1994. Developmental regulation of fungal cell wall formation. Annu. Rev. Phytopathol. 32: 413-437.
80. Wessels, J. G. H. 1996. Fungal hydrophobins: Proteins that function at an interface. Trends Plant Sci. 1: 9-15.
81. Wessels, J. G. H. 1997. Hydrophobins: Proteins that change the nature of the fungal surface. Adv. Microbial Physiol. 38: 1-45.
82. 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.
83. Wösten, H. A. B., Schuren, F. H. J., and Wessels, J. G. H. 1994. Interfacial self-assembly of a hydrophobin into an amphipathic protein membrane mediates fungal attachment to hydrophobic surfaces. EMBO J. 13: 5848-5854.
84. Yasuda, T., and Shishido, K. 1997. Aggregation of yeast cells induced by the Arg-Gly-Asp motif-containing fragment of high-molecular-mass cell-adhesion protein MFBA, derived from the basidio-mycetous mushroom Lentinus edodes. FEMS Microbiol. Lett. 154: 195-200.
85. Yasuda, T., Ishihara, H., Amano, H., and Shishido, K. 1997. Generation of basidiomycetous hyphal cell-aggregates by addition of the Arg-Gly-Asp motif-containing fragment of high-molecular-weight cell-adhesion protein MFBA derived from the basidiomycete Lentinus edodes. Biosci. Biotech. Biochem. 61: 1587-1589.
86. Zlotnik, H., Fernandez, M. P., Bowers, B., and Cabib, E. 1994. Saccharomyces cerevisiae mannoproteins form an external cell wall layer that determines wall porosity. J. Bacteriol. 159: 1018-1026.