Repeat-Induced Point Mutation (RIP) as an alternative mechanism of evolution toward virulence in leptosphaeria maculans

Molecular Plant-Microbe Interactions

Volumn 22, Issue 8, 2009, Pages 932-941

  Fudal, Isabelle ^a   Ross, Simon ^a   Brun, Hortense ^b   Besnard, Anne Laure ^b   Ermel, Magali ^b   Kuhn, Marie Line ^a   Balesdent, Marie Hélène ^a   Rouxel, Thierry ^a  

^a INRA Institut National de la Recherche Agronomique   (France)

^b CEMAGREF   (France)

Author keywords

[No Author keywords available]

Indexed keywords

FUNGAL PROTEIN;

ALLELE; AMINO ACID SEQUENCE; ARTICLE; ASCOMYCETES; CHEMISTRY; DNA SEQUENCE; GENETIC POLYMORPHISM; GENETICS; ISOLATION AND PURIFICATION; MOLECULAR EVOLUTION; MOLECULAR GENETICS; NUCLEOTIDE SEQUENCE; PATHOGENICITY; POINT MUTATION; SEQUENCE ALIGNMENT; VIRULENCE;

ALLELES; AMINO ACID SEQUENCE; ASCOMYCOTA; EVOLUTION, MOLECULAR; FUNGAL PROTEINS; MOLECULAR SEQUENCE DATA; POINT MUTATION; POLYMORPHISM, GENETIC; SEQUENCE ALIGNMENT; SEQUENCE ANALYSIS, DNA; VIRULENCE;

LEPTOSPHAERIA MACULANS;

EID: 67650473552     PISSN: 08940282     EISSN: None     Source Type: Journal    
DOI: 10.1094/MPMI-22-8-0932     Document Type: Article

References (52)

1. Ansan-Melayah, D., Balesdent, M. H., Buée, M., and Rouxel, T. 1995. Genetic characterization of AvrLm1, the first avirulence gene of Leptosphaeria maculans. Phytopathology 85:1525-1529.
2. Ansan-Melayah, D., Rouxel, T., Bertrandy, J., Letarnec, B., Mendes- Pereira, E., and Balesdent, M. H. 1997. Field efficiency of Brassica napus specific resistance correlates with Leptosphaeria maculans population structure. Eur. J. Plant Pathol. 103:835-841.
3. Attard, A., Gout, L., Gourgues, M., Kühn, M. L., Schmit, J., Laroche, S., Ansan-Melayah, D., Billault, A., Cattolico, L., Balesdent, M. H., and
4. Rouxel, T. 2002. Analysis of molecular markers genetically linked to the Leptosphaeria maculans avirulence gene AvrLm1 in field populations indicates a highly conserved event leading to virulence on Rlm1 genotypes. Mol. Plant-Microbe Interact. 15:672-682.
5. Attard, A., Gout, L., Ross, S., Parlange, F., Cattolico, L., Balesdent, M. H., and Rouxel, T. 2005. Truncated and RIP-degenerated copies of the LTR retrotransposon Pholy are clustered in a pericentromeric region of the Leptosphaeria maculans genome. Fungal Genet. Biol. 42:30-41.
6. Balesdent, M. H., Attard, A., Ansan-Melayah, D., Delourme, R., Renard, M., and Rouxel, T. 2001. Genetic control and host range of avirulence towards Brassica napus cultivars Quinta and Jet Neuf in Leptosphaeria maculans. Phytopathology 91:70-76.
7. Balesdent, M. H., Attard, A., Kuhn, M. L., and Rouxel, T. 2002. New avirulence genes in the phytopathogenic fungus Leptosphaeria maculans. Phytopathology 92:1122-1133.
8. Balesdent, M. H., Barbetti, M. J., Li, H., Sivasithamparam, K., Gout, L., and Rouxel, T. 2005. Analysis of Leptosphaeria maculans race structure in a worldwide collection of isolates. Phytopathology 95:1061- 1071.
9. Balesdent, M. H., Louvard, K., Pinochet, X., and Rouxel, T. 2006. A large scale survey of races of Leptosphaeria maculans occurring on oilseed rape in France. Eur. J. Plant Pathol. 114:53-65.
10. Brun, H., Levivier, S., Somda, I., Ruer, D., Renard, M., and Chèvre, A. M. 2000. A field method for evaluating the potential durability of new resistance sources: Application to the Leptosphaeria maculans-Brassica napus pathosystem. Phytopathology 90:961-964.
11. Cambareri, E. B., Jensen, B. C., Schabtach, E., and Selker, E. U. 1989. Repeat- induced G-C to A-T mutations in Neurospora. Science 244:1571- 1575.
12. Catanzariti, A. M., Dodds, P. N., Lawrence, G. J., Ayliffe, M. A., and Ellis, J. G. 2006. Haustorially expressed secreted proteins from flax rust are highly enriched for avirulence elicitors. Plant Cell 18:243-256.
13. Chisholm, S. T., Coaker, G., Day, B., and Staskawicz, B. J. 2006. Host- microbe interactions: Shaping the evolution of the plant immune response. Cell 124:803-814.
14. Delourme, R., Pilet-Nayel, M. L., Archipiano, M., Horvais, R., Tanguy, X., Rouxel, T., Brun, H., Renard, M., and Balesdent, M. H. 2004. A cluster of major specific resistance genes to Leptosphaeria maculans in Brassica napus. Phytopathology 94:578-583.
15. Ellis, J. G., Dodds, P. N., and Lawrence, G. J. 2007. Flax rust resistance gene specificity is based on direct resistance-avirulence protein interactions. Annu. Rev. Phytopathol. 45:289-306.
16. Farman, M. L., Eto, Y., Nakao, T., Tosa, Y., Nakayashiki, H., Mayama, S., and Leong, S. A. 2002. Analysis of the structure of the AVR1-CO39 avirulence locus in virulent rice-infecting isolates of Magnaporthe grisea. Mol. Plant-Microbe Interact. 15:6-16.
17. Fitt, B. D. L., Brun, H., Barbetti, M. J., and Rimmer, S. R. 2006. Worldwide importance of Phoma stem canker (Leptosphaeria maculans and L. biglobosa) on oilseed rape (Brassica napus). Eur. J. Plant Pathol. 114:3-15.
18. Flor, H. H. 1942. Inheritance of pathogenicity in Melampsora lini. Phytopathology 32:653-669.
19. Fudal, I., Bohnert, H. U., Tharreau, D., and Lebrun, M. H. 2005. Transposition of MINE, a composite retrotransposon, in the avirulence gene ACE1 of the rice blast fungus Magnaporthe grisea. Fungal Genet. Biol. 42:761-772.
20. Fudal, I., Ross, S., Gout, L., Blaise, F., Kuhn, M. L., Eckert, M. R., Cattolico, L., Bernard-Samain, S., Balesdent, M. H., and Rouxel, T. 2007. Heterochromatin-like regions as ecological niches for avirulence genes in the Leptosphaeria maculans genome: Map-based cloning of AvrLm6. Mol. Plant-Microbe Interact. 20:459-470.
21. Galagan, J. E., and Selker, E. U. 2004. RIP: The evolutionary cost of genome defense. Trends Genet. 20:417-423.
22. Galagan, J. E., Calvo, S. E., Borkovich, K. A., Selker, E. U., Read, N. D., Jaffe, D., FitzHugh, W., Ma, L. J., Smirnov, S., Purcell, S., Rehman, B., Elkins, T., Engels, R., Wang, S., Nielsen, C. B., Butler, J., Endrizzi, M., Qui, D., Ianakiev, P., Bell-Pedersen, D., Nelson, M. A., Werner- Washburne, M., Selitrennikoff, C. P., Kinsey, J. A., Braun, E. L., Zelter, A., Schulte, U., Kothe, G. O., Jedd, G., Mewes, W., Staben, C., Marcotte, E., Greenberg, D., Roy, A., Foley, K., Naylor, J., Stange-Thomann, N., Barrett, R., Gnerre, S., Kamal, M., Kamvysselis, M., Mauceli, E., Bielke, C., Rudd, S., Frishman, D., Krystofova, S., Rasmussen, C., Metzenberg, R. L., Perkins, D. D., Kroken, S., Cogoni, C., Macino, G., Catcheside, D., Li, W., Pratt, R. J., Osmani, S. A., DeSouza, C. P., Glass, L., Orbach, M. J., Berglund, J. A., Voelker, R., Yarden, O., Plamann, M., Seiler, S., Dunlap, J., Radford, A., Aramayo, R., Natvig, D. O., Alex, L. A., Mannhaupt, G., Ebbole, D. J., Freitag, M., Paulsen, I., Sachs, M. S., Lander, E. S., Nusbaum, C., and Birren, B. (2003). The genome sequence of the filamentous fungus Neurospora crassa. Nature 422:859-868. Gout, L., Fudal, I., Kuhn, M. L., Blaise, F., Eckert, M., Cattolico, L., Balesdent, M. H., and Rouxel, T. 2006. Lost in the middle of nowhere: The AvrLm1 avirulence gene of the Dothideomycete Leptosphaeria maculans. Mol. Microbiol. 60:67-80.
23. Gout, L., Kuhn, M. L., Vincenot, L., Bernard-Samain, S., Cattolico, L., Barbetti, M., Moreno-Rico, O., Balesdent, M. H., and Rouxel, T. 2007. Genome structure impacts molecular evolution at the AvrLm1 avirulence locus of the plant pathogen Leptosphaeria maculans. Environ. Microbiol. 9:2978-2992.
24. Graia, F., Lespinet, O., Rimbault, B., Dequard-Chablat, M., Coppin, E., and Picard, M. 2001. Genome quality control: RIP (repeat-induced point mutation) comes to Podospora. Mol. Microbiol. 40:586-595.
25. Hammond-Kosack, K. E., and Parker, J. E. 2003. Deciphering plant-pathogen communication: Fresh perspectives for molecular resistance breeding. Curr. Opin. Biotechnol. 14:177-193.
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. Ikeda, K., Nakayashiki, H., Kataoka, T., Tamba, H., Hashimoto, Y., Tosa, Y., and Mayama, S. 2002. Repeat-induced point mutation (RIP) in Magnaporthe grisea: Implications for its sexual cycle in the natural field context. Mol. Microbiol. 45:1355-1364.
28. Irelan, J. T., Hagemann, A. T., and Selker, E. U. 1994. High frequency repeat- induced point mutation (RIP) is not associated with efficient recombination in Neurospora. Genetics 138:1093-1103.
29. Jones, J. D., and Dangl, J. L. 2006. The plant immune system. Nature 444:323-329.
30. Joosten, M. H., Vogelsang, R., Cozijnsen, T. J., Verberne, M. C., and De Wit, P. J. 1997. The biotrophic fungus Cladosporium fulvum circumvents Cf-4-mediated resistance by producing unstable AVR4 elicitors. Plant Cell 9:367-379.
31. Kang, S., Lebrun, M. H., Farrall, L., and Valent, B. 2001. Gain of virulence caused by insertion of a Pot3 transposon in a Magnaporthe grisea avirulence gene. Mol. Plant-Microbe Interact. 14:671-674.
32. Li, C. X., and Cowling, W. A. 2003. Identification of a single dominant allele for resistance to blackleg in Brassica napus "Surpass 400". Plant Breed. 122:485-488.
33. Luderer, R., Takken, F. L., de Wit, P. J., and Joosten, M. H. 2002. Cladosporium fulvum overcomes Cf-2-mediated resistance by producing truncated AVR2 elicitor proteins. Mol. Microbiol. 45:875-884.
34. Mendes-Pereira, E., Balesdent, M. H., Brun, H., and Rouxel, T. 2003. Molecular phylogeny of the Leptosphaeria maculans-L. biglobosa species complex. Mycol. Res. 107:1287-1304.
35. Montiel, M. D., Lee, H. A., and Archer, D. B. 2006. Evidence of RIP (repeat- induced point mutation) in transposase sequences of Aspergillus oryzae. Fungal Genet. Biol. 43:439-445.
36. Orbach, M. J., Farrall, L., Sweigard, J. A., Chumley, F. G., and Valent, B. 2000. A telomeric avirulence gene determines efficacy for the rice blast resistance gene Pi-ta. Plant Cell 12:2019-2032.
37. Parlange, F., Daverdin ,G., Fudal, I., Kuhn, M. L., Balesdent, M. H., Blaise, F., Grezes-Besset, B., and Rouxel, T. 2009. Leptosphaeria maculans avirulence gene AvrLm4-7 confers a dual recognition specificity by Rlm4 and Rlm7 resistance genes of oilseed rape, and circumvents Rlm4-mediated recognition through a single amino acid change. Mol. Microbiol. 71:851-863
38. Plummer, K. M. and Howlett, B. J. 1993. Major chromosomal length polymorphisms are evident after meiosis in the blackleg fungus, Leptosphaeria maculans. Curr. Genet. 24:107-113.
39. Rehmany, A. P., Gordon, A., Rose, L. E., Allen, R. L., Armstrong, M. R., Whisson, S. C., Kamoun, S., Tyler, B. M., Birch, P. R. J., and Beynon, J. L. 2005. Differential recognition of highly divergent downy mildew avirulence gene alleles by RPP1 resistance genes from two Arabidopsis lines. Plant Cell 17:1839-1850.
40. Rep, M., van der Does, H. C., Meijer, M., van Wijk, R., Houterman, P. M., Dekker, H. L., de Koster, C. G., and Cornelissen, B. J. 2004. A small, cysteine-rich protein secreted by Fusarium oxysporum during colonization of xylem vessels is required for I-3-mediated resistance in tomato. Mol. Microbiol. 53:1373-1383.
41. Ridout, C. J., Skamnioti, P., Porritt, O., Sacristan, S., Jones, J. D., and Brown, J. K. 2006. Multiple avirulence paralogues in cereal powdery mildew fungi may contribute to parasite fitness and defeat of plant resistance. Plant Cell 18:2402-2414.
42. Rouxel, T., and Balesdent, M. H. 2005. The stem canker (blackleg) fungus, Leptosphaeria maculans, enters the genomic era. Mol. Plant Pathol. 6:225-241.
43. Rouxel, T., Penaud, A., Pinochet, X., Brun, H., Gout, L., Delourme, R., Schmit, J., and Balesdent, M. H. 2003a. A 10-year survey of populations of Leptosphaeria maculans in France indicates a rapid adaptation towards the Rlm1 resistance gene of oilseed rape. Eur. J. Plant Pathol. 109:871-881.
44. Rouxel, T., Willner, E., Coudard, L., and Balesdent, M. H. 2003b. Screening and identification of resistance to Leptosphaeria maculans (stem canker) in Brassica napus accessions. Euphytica 133:219-231. Sacristan, S., and Garcia-Arenal, F. (2008). The evolution of virulence and pathogenicity in plant pathogen populations. Mol. Plant Pathol. 9:369- 384.
45. Sambrook, J., and Russell, D. W. 2001. Molecular Cloning: A Laboratory Manual. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY, U.S.A.
46. Schurch, S., Linde, C. C., Knogge, W., Jackson, L. F., and McDonald, B. A. 2004. Molecular population genetic analysis differentiates two virulence mechanisms of the fungal avirulence gene NIP1. Mol. Plant- Microbe Interact. 17:1114-1125.
47. Somda, I., Delourme, R., Renard, M., and Brun, H. 1999. Pathogenicity of Leptosphaeria maculans isolates on a Brassica napus-B. juncea recombinant line. Phytopathology 89:169-175.
48. Stergiopoulos, I., De Kock, M. J., Lindhout, P., and De Wit, P. J. (2007). Allelic variation in the effector genes of the tomato pathogen Cladosporium fulvum reveals different modes of adaptive evolution. Mol. Plant- Microbe Interact. 20:1271-1283.
49. Watters, M. K., Randall, T. A., Margolin, B. S., Selker, E. U., and Stadler, D. R. 1999. Action of repeat-induced point mutation on both strands of a duplex and on tandem duplications of various sizes in Neurospora. Genetics 153:705-714.
50. Westerink, N., Brandwagt, B. F., de Wit, P. J., and Joosten, M. H. 2004. Cladosporium fulvum circumvents the second functional resistance gene homologue at the Cf-4 locus (Hcr9-4E) by secretion of a stable avr4E isoform. Mol. Microbiol. 54:533-545.
51. Zhou, E., Jia, Y., Singh, P., Correll, J. C., and Lee, F. N. 2007. Instability of the Magnaporthe oryzae avirulence gene AVR-Pita alters virulence. Fungal Genet. Biol. 44:1024-1034.
52. Zipfel, C., and Felix, G. (2005). Plants and animals: A different taste for microbes? Curr. Opin. Plant Biol. 8:353-360.