Nonmycorrhizal (Myc-) mutants of Hebeloma cylindrosporum obtained through insertional mutagenesis

Molecular Plant-Microbe Interactions

Volumn 17, Issue 9, 2004, Pages 1029-1038

  Combier, Jean Philippe ^a   Melayah, Delphine ^a   Raffier, Colette ^a   Pépin, Régis ^a   Marmeisse, Roland ^a   Gay, Gilles ^a  

^a University of Lyon   (France)

Author keywords

[No Author keywords available]

Indexed keywords

FUNGI; HEBELOMA; HEBELOMA CYLINDROSPORUM; INSERTION SEQUENCES; PINUS PINASTER; PROKARYOTA; TRANSPOSONS;

EID: 4143060267     PISSN: 08940282     EISSN: None     Source Type: Journal    
DOI: 10.1094/MPMI.2004.17.9.1029     Document Type: Article

References (60)

1. Ané, J. M., Kiss, G. B., Riely, B. K., Penmetsa, R. V., Oldroyd, G. E. D., Ayax, C., Lévy, J., Debellé, F., Baek, J. M., Kalo, P., Rosenberg, C., Roe, B. A., Long, S. R., Dénarié, J., and Cook, D. R. 2004. Medicago truncatula DMII required for bacterial and fungal symbioses in legumes. Science 303:1364-1367.
2. Balhadère, P. V., Foster, A. J., and Talbot, N. 1999. Identification of pathogenicity mutants of the rice blast fungus Magnaporthe grisea by insertional mutagenesis. Mol. Plant-Microbe Interact. 12:129-142.
3. Basse, C. W., Stumpferl, S., and Kahmann, R. 2000. Characterization of a Ustilago maydis gene specifically induced during the biotrophic phase: Evidence for negative as well as posititve regulation. Mol. Cell. Biol. 20:329-339.
4. Bölker, M., Böhnert, H. U., Braun, K. H., Gröl, J., and Kahmann, R. 1995. Tagging pathogenicity genes in Ustilago maydis by restriction enzyme mediated integration (REMI). Mol. Gen. Genet. 248:547-552.
5. Bonfante, P., Genre, A., Faccio, A., Martini, I., Schauser, L., Stougaard, J., Webb, J., and Parniske, M. 2000. The Lotus japonicus LjSym4 gene is required for the successful symbiotic infection of root epidermal cells. Mol. Plant-Microbe Interact. 13:1109-1120.
6. Chung, K. R., Ehrenshaft, M., Wetzel, D. K., and Daub, M. E. 2003. Cercosporin-deficient mutants by plasmid tagging in the asexual fungus Cercospora nicotianae. Mol. Genet. Genomics 270:103-113.
7. Clergeot, P. H., Gourgues, M., Cots, J., Laurans, F., Latorse, M. P., Pépin, R., Tharreau, D., Notteghem, J. L., and Lebrun, M. H. 2001. PLS1, a gene encoding a tetraspanin-like protein, is required for penetration of rice leaf by the fungal pathogen Magnaporthe grisea. Proc. Natl. Acad. Sci. U.S.A. 98:6963-6968.
8. Combier, J.-P., Melayah, D., Raffier, C., Gay, G., and Marmeisse, R. 2003. Agrobacterium tumefaciens-mediated transformation as a tool for insertional mutagenesis in the symbiotic ectomycorrhizal fungus Hebeloma cylindrosporum. FEMS (Fed. Eur. Microbiol. Soc.) Lett. 220:141-148.
9. Cummings, W. J., Celerin, M., Crodian, J., Brunick, L. K., and Zolan, M. E. 1999. Insertional mutagenesis in Coprinus cinereus: Use of a dominant selectable marker to generate tagged, sporulation defective mutants. Curr. Genet. 36:371-382.
10. David-Schwartz, R., Badani, H., Smadar, W., Levy, A. A., Galili, G., and Kapulnik, Y. 2001. Identification of a novel genetically controlled step in mycorrhiza colonization: Plant resistance to infection by fungal spores but not extra-radical hyphae. Plant J. 27:561-569.
11. David-Schwartz, R., Gadkar, V., Wininger, S., Bendov, R., Galili, G., Levy, A. A., and Kapulnik, Y. 2003. Isolation of a premycorrhizal infection (pmi2) mutant of tomato resistant to arbuscular mycorrhizal fungal colonization. Mol. Plant-Microbe Interact. 16:382-388.
12. Debaud J. C., and Gay, G. 1987. In vitro fruiting under controlled conditions of the ectomycorrhizal fungus Hebeloma cylindrosporum associated with Pinus pinaster. New Phytol. 105:429-435.
13. Debaud, J. C., Gay, G., Prevost, A., Lei, J., and Dexheimer, J. 1988. Ectomycorrhizal ability of genetically different homokaryotic and dikaryotic strains of Hebeloma cylindrosporum. New Phytol. 108:323-328.
14. de Groot, M. J. A., Bundock, P., Hooykaas, P. J. J., and Beijersbergen, A. G. M. 1998. Agrobacterium tumefaciens-mediated transformation of filamentous fungi. Nature Biotechnol. 16:839-842.
15. -) obtained in pea (Pisiun sativum L.) and fava bean (Vicia faba L.). Plant Sci. 60:215-222.
16. Dufresne, M., Bailey, J. A., Dron, M., and Langin, T. 1998. Clk1, a serine/threonine kinase-encoding gene, is involved in pathogenicity of Collelotrichum lindemuthianum on common bean. Mol. Plant-Microbe Interact. 11:99-108.
17. Durand, N., Debaud, J. C., Casselton, L. A., and Gay, G. 1992. Isolation and preliminary characterization of 5-fluoroindole-resistant and IAA-overproducer mutants of the ectomycorrhizal fungus Hebeloma cylindrosporum Romagnesi. New Phytol. 121:545-553.
18. Gay, G. 1990. Effect of the ectomycorrhizal fungus Hebeloma hiemale on adventitious root formation in derooted Pinus halepensis shoot hypocotyls. Can. J. Bot. 68:1265-1270.
19. 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 Romagnesi. New Phytol. 128:659-670.
20. Granado, J. D., Kertesz-Chaloupkovà, K., Aebi, M., and Kües, U. 1997. Restriction enzyme-mediated DNA integration in Coprinus cinereus. Mol. Gen. Genet. 256:28-36.
21. Guidot, A., Lumini, E., Debaud, J. C., and Marmeisse R. 1999. The nuclear ribosomal DNA intergenic spacer as a target sequence to study intraspecific diversity of the ectomycorrhizal basidiomycete Hebeloma cylindrosporum directly on Pinus root systems. Appl. Environ. Microbiol. 65:903-909.
22. Hébraud, M., and Fèvre, M. 1987. Protoplast production and regeneration from mycorrhizal fungi and their use for isolation of mutants. Can. J. Microbiol. 34:157-161.
23. Heller, R. 1953. Recherches sur la nutrition des tissus végétaux cultivés in vitro. Ann. Sci. Nat. Bot. Biol. Vég. 14:1-21.
24. Hibbet, D. S., Gilbert, L. B., and Donoghue, M. J. 2000. Evolutionary instability of ectomycorrhizal symbioses in Basidiomycetes. Nature. 407:506-508.
25. Hilbert, J. L., Costa, G., and Martin, F. 1991. Ectomycorrhizin synthesis and polypeptide changes during the early stage of eucalyptus mycorrhiza development. Plant Physiol. 97:977-984.
26. Idnurm, A., and Howlett, B. J. 2003. Analysis of loss of pathogenicity mutants reveals that repeat-induced point mutations can occur in the Dothideomycete Leptosphaeria maculans. Fungal Genet. Biol. 39:31-37.
27. Johansson, T., Le Quéré, A., Ahren, D., Söderström, B., Erlandsson, R., Lundeberg, J., Uhlén, M., and Tunlid A. 2004. Transcriptional responses of Paxilus involutus and Betula pendula during formation of ectomycorrhizal root tissues. Mol. Plant-Microbe Interact. 17:202-215.
28. Kahmann, R., and Basse, C. 1999. REMI (restriction enzyme mediated integration) and its impact on the isolation of pathogenicity genes in fungi attacking plants. Eur. J. Plant Pathol. 105:221-229.
29. Kim, S. J., Bernreuther, D., Thumm, M., and Podila, G. K. 1999. LB-AUT7, a novel symbiosis-regulated gene from an ectomycorrhizal fungus, Laccaria bicolor is functionally related to vesicular transport and autophagocytosis. J. Bacteriol. 181:1963-1967.
30. Kuspa, A., and Loomis, W. F. 1992. Tagging developmental genes in Dictyostelium by restriction enzyme-mediated integration of plasmid DNA. Proc. Natl. Acad. Sci. U.S.A. 89:8803-8807.
31. 2+ and calmodulin-dependent protein kinase required for bacterial and fungal symbioses. Science 303:1361-1363.
32. Lu, S. W., Lyngholm, L., Yang, G., Bronson, C., Yoder, O. C., and Turgeon, B. G. 1994. Tagged mutations at the Tox1 locus of Cochliobolus heterostrophus by restriction enzyme-mediated integration. Proc. Natl. Acad. Sci. U.S.A. 91:12649-12653.
33. Lu, S. W., Kroken, S., Lee, B. N., Robbertse, B., Churchill, A. C. L., Yoder, O. C., and Turgeon, B. G. 2003. A novel class of gene controlling virulence in plant pathogenic ascomycete fungi. Proc. Natl. Acad. Sci. U.S.A. 100:5980-5985.
34. Maier, F. J., and Schäfer, W. 1999. Mutagenesis via insertional - or restriction enzyme-mediated - integration (REMI) as a tool to tag pathogenicity related genes in plant pathogenic fungi. Biol. Chem. 380:885-864.
35. Marsch, J. F., and Schultze, M. 2001. Analysis of arbuscular mycorrhizas using symbiosis-defective plant mutants. New Phytol. 150:525-532.
36. 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.
37. Martin, F. 2001. Frontiers in molecular mycorrhizal research - genes, loci, dots and spins. New Phytol. 150:499-505.
38. Martin, F., and Tagu, D. 1999. Developmental biology of plant-fungus symbiosis: The ectomycorrhiza. Pages 51-73 in: Mycorrhiza: Structure, Molecular Biology and Function. A. Varma and B. Hock, eds. Springer Verlag, Heidelberg, Germany.
39. Mullins, E. D., and Kang, S. 2001. Transformation: A tool for studying fungal pathogens of plants. Cell. Mol. Life Sci. 58:2043-2052.
40. Norkrans, B. 1949. Some mycorrhiza-forming Tricholoma species. Svensk. Bot. Tidskr. 43:485-490.
41. Rao, P. S., and Niederpruem, D. J. 1969. Carbohydrate metabolism during morphogenesis of Coprinus lagopus (sensu Buller) J. Bacteriol. 100:1222-1228.
42. Riggle, P. J., and Kumamoto, C. A. 1998. Genetic analysis in fungi using restriction-enzyme-mediated integration. Curr. Opin. Microbiol. 1:395-399.
43. Sambrook, J., Fritsch, E. F., and Maniatis, T. 1989. Molecular cloning: A Laboratory Manual. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY, U.S.A.
44. Sanchez, O., Navarro, R. E., and Aguirre, J. 1998. Increased transformation frequency and tagging of developmental genes in Aspergillus nidulans by restriction enzyme-mediated integration (REMI). Mol. Gen. Genet. 258:89-94.
45. Schiestl, R. H., and Petes, T. D. 1991. Integration of DNA fragments by illegitimate recombination in Saccharomyces cerevisiae. Proc. Natl. Acad. Sci. U.S.A. 88:7585-7589.
46. Schuren, F. H. J., and Wessels, J. G. H. 1998. Expression of heterologous genes in Schizophyllum commune is often hampered by the formation of truncated transcripts. Curr. Genet. 33:151-156.
47. Shi, Z., and Leung, H. 1995. Genetic analysis of sporulation in Magnaporthe grisea by chemical and insertional mutagenesis. Mol. Plant-Microbe Interact. 8:949-959.
48. Shi, Z., Christian, D., and Leung, H. 1995. Enhanced transformation in Magnaponhe grisea by restriction enzyme mediated integration of plasmid DNA. Phytopathol. 85:329-333.
49. Smith, S. E., and Read, D. J. 1997. Mycorrhizal symbiosis. 2nd ed. Academic Press, San Diego, CA, U.S.A..
50. Sundaram, S., Kim, S. J., Suzuki, H., Mcquattie, C. J., Hiremath, S. T., and Podila, G. K. 2001. Isolation and characterization of a symbiosis-regulated ras from the ectomycorrhizal fungus Laccaria bicolor. Mol. Plant-Microbe Interact. 14:618-628.
51. Sweigard, J. A., Carroll, A. M., Farrall, L., Chumley, F. G., and Valent, B. 1998. Magnaporthe grisea pathogenicity genes obtained through insertional mutagenesis. Mol. Plant-Microbe Interact. 11:404-412.
52. Tagu, D., Phyton, M., Crétin, C., and Martin, F. 1993. Cloning symbiosis-related cDNAs from eucalypt ectomycorrhiza by PCR-assisted differential screening. New Phytol. 152:339-343.
53. Thon, M. R., Nuckles, E. M., and Vaillancourt, L. J. 2000. Restriction enzyme-mediated integration used to produce pathogenicity mutants of Colletotrichum graminicola. Mol. Plant-Microbe Interact. 13:1356-1365.
54. Urban, M., Bhargava, T., and Hamer, J. E. 1999. An ATP-driven efflux pump is a novel pathogenicity factor in rice blast disease. EMBO (Eur. Mol. Biol. Organ.) J. 18:512-521.
55. Van Kan, J. A. L., Van Den Ackerveken, F. J. M., and De Wit, P. J. G. M. 1991. Cloning and characterization of the cDNA of avirulence avr9 of the fungal pathogen Cladosporium fulvum, the causal agent of tomato leaf mold. Mol. Plant-Microbe Interact. 4:52-59.
56. Voiblet, C., Duplessis, S., Encelot, N., and Martin, F. 2001. Identification of symbiosis-regulated genes in Eucalyptus globulus-Pisolithus tinctorius ectomycorrhiza by differential hybridization of arrayed cDNAs. Plant J. 25:181-191.
57. Wilkinson, D. M. 2001. Mycorrhizal evolution. Trends Ecol. Evol. 16:64-65.
58. Yakoby, N., Zhou, R., Kobiler, A., Dinoor, A., and Prusky, D. 2001. Development of Colletotrichum gloeosporoides restriction enzyme-mediated integration mutants as biocontrol agents against anthracnose disease in avocado fruits. Phytopathol. 91:143-148.
59. Yang, G., Rose, M. S., Turgeon, B. G., and Yoder, O. C. 1996. A polyketide synthase is required for fungal virulence and production of the polyketide T-toxin. Plant Physiol. 8:2139-2150.
60. Yaver, D. S., Lamsa, M., Munds, R., Brown, S. H., Otani, S., Franssen, L., Johnstone, J. A., and Brody, H. 2000. Using DNA-tagged mutagenesis to improve heterologous protein production in Aspergillus oryzae. Fungal Genet. Biol. 29:28-37.