Genome structure impacts molecular evolution at the AvrLm1 avirulence locus of the plant pathogen Leptosphaeria maculans

Environmental Microbiology

Volumn 9, Issue 12, 2007, Pages 2978-2992

  Gout, Lilian ^a   Kuhn, Marie Line ^a   Vincenot, Lucie ^a   Bernard Samain, Sylvie ^b   Cattolico, Laurence ^b   Barbetti, Martin ^c   Moreno Rico, Onésimo ^d   Balesdent, Marie Hélène ^a   Rouxel, Thierry ^a  

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

^b CENTRE NATIONAL DE SÉQUENÇAGE   (France)

^c UNIVERSITY OF WESTERN AUSTRALIA   (Australia)

^d UNIVERSIDAD AUTÓNOMA DE AGUASCALIENTES   (Mexico)

Author keywords

[No Author keywords available]

Indexed keywords

FUNGAL PROTEIN;

ARTICLE; ASCOMYCETES; DNA SEQUENCE; GENE DELETION; GENETIC SELECTION; GENETICS; GENOME; METABOLISM; MICROBIOLOGY; MOLECULAR EVOLUTION; MOLECULAR GENETICS; NUCLEOTIDE SEQUENCE; PATHOGENICITY; PLANT DISEASE; POPULATION GENETICS; RAPESEED; VIRULENCE;

ASCOMYCOTA; BASE SEQUENCE; BRASSICA NAPUS; EVOLUTION, MOLECULAR; FUNGAL PROTEINS; GENE DELETION; GENETICS, POPULATION; GENOME, FUNGAL; MOLECULAR SEQUENCE DATA; PLANT DISEASES; SELECTION (GENETICS); SEQUENCE ANALYSIS, DNA; VIRULENCE;

BRASSICA NAPUS; FUNGI; LEPTOSPHAERIA MACULANS;

EID: 35948986776     PISSN: 14622912     EISSN: 14622920     Source Type: Journal    
DOI: 10.1111/j.1462-2920.2007.01408.x     Document Type: Article

References (60)

1. Allen, R.L., Bittner-Eddy, P.D., Grenville-Briggs, L.J., Meitz, J.C., Rehmany, A.P., Rose, L.E. Beynon, J.L. (2004) Host-parasite coevolutionary conflict between Arabidopsis and Downy mildew. Science 306 : 1957 1960.
2. Ansan-Melayah, D., Balesdent, M.H., Buée, M. Rouxel, T. (1995) Genetic characterization of AvrLm1, the first avirulence gene of Leptosphaeria maculans. Phytopathology 85 : 1525 1529.
3. Armstrong, M.R., Whisson, S.C., Pritchard, L., Bos, J.I.B., Venter, E., Avrova, A.O., et al. (2005) An ancestral oomycete locus contains late blight avirulence gene Avr3a, encoding a protein that is recognized in the host cytoplasm. Proc Natl Acad Sci USA 102 : 7766 7771.
4. Attard, A., Gourgues, M., Gout, L., Schmit, J., Roux, J., Narcy, J.P., et al. (2001) Molecular characterisation and polymorphism of MinLm1, a minisatellite from the phytopathogenic ascomycete Leptosphaeria maculans. Curr Genet 40 : 54 64.
5. Attard, A., Gout, L., Gourgues, M., Kuhn, M.L., Schmit, J., Laroche, S., et al. (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.
6. Attard, A., Gout, L., Ross, S., Parlange, F., Cattolico, L., Balesdent, M.H. Rouxel, T. (2005a) Truncated and RIP-degenerated copies of the LTR retrotransposon Pholy are clustered in a pericentrorneric region of the Leptosphaeria maculans genome. Fungal Genet Biol 42 : 30 41.
7. Attard, A., Gout, L., Ross, S., Parlange, F., Cattolico, L., Balesdent, M.H. Rouxel, T. (2005b) 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.
8. Balesdent, M.H., Gall, C., Robin, P. Rouxel, T. (1992) Intraspecific variation in soluble mycelial protein and esterase patterns of Leptosphaeria maculans French isolates. Mycol Res 96 : 677 684.
9. Balesdent, M.H., Attard, A., Ansan-Melayah, D., Delourme, R., Renard, M. Rouxel, T. (2001) Genetic control and host range of avirulence toward Brassica napus cultivars Quinta and Jet Neuf in Leptosphaeria maculans. Phytopathology 91 : 70 76.
10. Balesdent, M.H., Attard, A., Kuhn, M.L. Rouxel, T. (2002) New avirulence genes in the phytopathogenic fungus Leptosphaeria maculans. Phytopathology 92 : 1122 1133.
11. Balesdent, M.H., Barbetti, M.J., Li, H., Sivasithamparam, K., Gout, L. Rouxel, T. (2005) Analysis of Leptosphaeria maculans race structure in a worldwide collection of isolates. Phytopathology 95 : 1061 1071.
12. Balesdent, M.H., Louvard, K., Pinochet, X. 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.
13. Barrins, J.M., Ades, P.K., Salisbury, P.A. Howlett, B.J. (2004) Genetic diversity of Australian isolates of Leptosphaeria maculans, the fungus that causes blackleg of canola (Brassica napus). Australas Plant Pathol 33 : 529 536.
14. Catanzariti, A.M., Dodds, P.N., Lawrence, G.J., Ayliffe, M.A. Ellis, J.G. (2006) Haustorially expressed secreted proteins from flax rust are highly enriched for avirulence elicitors. Plant Cell 18 : 243 256.
15. Chisholm, S.T., Coaker, G., Day, B. Staskawicz, B.J. (2006) Host-microbe interactions: shaping the evolution of the plant immune response. Cell 124 : 803 814.
16. Daboussi, M.J. Capy, P. (2003) Transposable elements in filamentous fungi. Annu Rev Microbiol 57 : 275 299.
17. Delourme, R., Chevre, A.M., Brun, H., Rouxel, T., Balesdent, M.H., Dias, J.S., et al. (2006) Major gene and polygenic resistance to Leptosphaeria maculans in oilseed rape (Brassica napus). Eur J Plant Pathol 114 : 41 52.
18. Dodds, P.N., Lawrence, G.J., Catanzariti, A.-M., Ayliffe, M.A. Ellis, J.G. (2004) The Melampsora lini AvrL567 avirulence genes are expressed in haustoria and their products are recognized inside plant cells. Plant Cell 16 : 755 768.
19. Dodds, P.N., Lawrence, G.J., Catanzariti, A.-M., Teh, T., Wang, C.-I.A., Ayliffe, M.A., et al. (2006) Direct protein interaction underlies gene-for-gene specificity and coevolution of the flax resistance genes and flax rust avirulence genes. Proc Natl Acad Sci USA 103 : 8888 8893.
20. Ewing, B. Green, P. (1998) Base calling of automated sequencer traces using Phred. II. Error probabilities. Genome Res 8 : 186 194.
21. Farman, M.L., Eto, Y., Nakao, T., Tosa, Y., Nakayashiki, H., Mayama, S. 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.
22. Fitt, B.D.L., Brun, H., Barbetti, M.J. Rimmer, S.R. (2006) World-wide importance of phoma stem canker (Leptosphaeria maculans and L. biglobosa) on oilseed rape (Brassica napus). Eur J Plant Pathol 114 : 3 15.
23. Flor, H.H. (1971) Current status of the sene-for-fene concept. Annu Rev Phytopathol 9 : 275 296.
24. Fudal, I., Ross, S., Gout, L., Blaise, F., Kuhn, M.L., Eckert, M., et al. (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.
25. Funnell, D.L., Matthews, P.S. Van Etten, H.D. (2002) Identification of new pisatin demethylase genes (PDA5 and PDA7) in Nectria haematococca and non-Mendelian segregation of pisatin demethylating ability and virulence on pea due to loss of chromosomal elements. Fungal Genet Biol 37 : 121 133.
26. Gout, L., Fudal, I., Kuhn, M.L., Blaise, F., Cattolico, L., Balesdent, M.H. Rouxel, T. (2006a) Lost in the middle of nowhere: the AvrLm1 avirulence gene of Leptosphaeria maculans. Mol Microbiol 60 : 67 80.
27. Gout, L., Eckert, M., Rouxel, T. Balesdent, M.-H. (2006b) Genetic variability and distribution of mating type alleles in field populations of Leptosphaeria maculans from France. Appl Environ Microbiol 72 : 185 191.
28. Hatta, R., Ito, K., Hosaki, Y., Tanaka, T., Tanaka, A., Yamamoto, M., et al. (2002) A conditionally dispensable chromosome controls host-specific pathogenicity in the fungal plant pathogen Alternaria alternata. Genetics 161 : 59 70.
29. Howlett, B.J., Idnurm, A. Pedras, M.S.C. (2001) Leptosphaeria maculans, the causal agent of blackleg disease of Brassicas. Fungal Genet Biol 33 : 1 14.
30. Huang, Y.J., Li, Z.Q., Evans, N., Rouxel, T., Fitt, B.D.L. Balesdent, M.H. (2006) Fitness cost associated with the loss of the AvrLm4 avirulence function in Leptosphaeria maculans (Phoma stem canker of oilseed rape). Eur J Plant Pathol 114 : 77 89.
31. Joosten, M.H.A.J., Vogelsang, R., Cozijnsen, T.J., Verberne, M.C. DeWit, P.J.G.M. (1997) The biotrophic fungus Cladosporium fulvum circumvents Cf-4-mediated resistance by producing unstable AVR4 elicitors. Plant Cell 9 : 367 379.
32. Kang, S., Lebrun, M.H., Farall, L. Valent, B. (2001) Gain of virulence caused by insertion of a Pot3 transposon in a Magnaporthe grisea gene. Mol Plant Microbe Interact 14 : 671 674.
33. Kuhn, M.L., Gout, L., Howlett, B.J., Melayah, D., Meyer, M., Balesdent, M.H. Rouxel, T. (2006) Genetic linkage maps and genomic organization in Leptosphaeria maculans. Eur J Plant Pathol 114 : 17 31.
34. Kumar, A. Bennetzen, J.L. (1999) Plant retrotransposons. Annu Rev Genet 33 : 479 532.
35. Li, H., Sivasithamparam, K. Barbetti, M.J. (2003) Breakdown of a Brassica rapa subsp. sylvestris single dominant blackleg resistance gene in B. napus rapeseed by Leptosphaeria maculans field isolates in Australia. Plant Dis 87 : 752 752.
36. Luderer, R., Takken, F.L.W., de Wit, P.J.G.M. Joosten, M.H.A.J. (2002) Cladosporium fulvum overcomes Cf-2-mediated resistance by producing truncated AVR2 elicitor proteins. Mol Microbiol 45 : 875 884.
37. McDonald, B.A. Linde, C. (2002) Pathogen population genetics, evolutionary potential, and durable resistance. Annu Rev Phytopathol 40 : 349 379.
38. Mendes-Pereira, E., Balesdent, M.H., Brun, H. Rouxel, T. (2003) Molecular phylogeny of the Leptosphaeria maculans-L. biglobosa species complex. Mycol Res 107 : 1287 1304.
39. Morales, V.M., Seguin Swartz, G. Taylor, J.L. (1993) Chromosome size polymorphism in Leptosphaeria maculans. Phytopathology 83 : 503 509.
40. Moreno-Rico, O., Frias-Trevino, A.G., Luna-Ruiz, J.J., Manzano-Flores, D.E., Romero-Cova, S. Séguin-Swartz, G. (2001) Characterization and pathogenicity of isolates of Leptosphaeria maculans from Aguascalientes and Zacatecas, Mexico. Can J Plant Pathol 23 : 270 278.
41. Mudgett, M.B. (2005) New insights to the function of phytopathogenic bacterial type III effectors in plants. Annu Rev Plant Biol 56 : 509 531.
42. Orbach, M.J., Farrall, L., Sweigard, J.A., Chumley, F.G. Valent, B. (2000) A telomeric avirulence gene determines efficacy for the rice blast resistance gene Pi-ta. Plant Cell 12 : 2019 2032.
43. Parlange, F. (2006) Analyse de l'environnement et clonage du gène Avrlm4-7 Chez l'ascomycète Leptosphaeria maculans. Orsay, France : Université Paris-Sud-Orsay.
44. Pink, D.A.C. (2002) Strategies using genes for non-durable disease resistance. Euphytica 124 : 227 236.
45. Pitkin, J.W., Nikolskaya, A., Ahn, J.-H. Walton, J.D. (2000) Reduced virulence caused by meiotic instability of the TOX2 chromosome of the maize pathogen Cochliobolus carbonum. Mol Plant Microbe Interact 13 : 80 87.
46. Plummer, K.M. Howlett, B.J. (1993) Major chromosomal length polymorphisms are evident after meiosis in the phytopathogenic fungus Leptosphaeria maculans. Curr Genet 24 : 107 113.
47. Rehmany, A.P., Gordon, A., Rose, L.E., Allen, R.L., Armstrong, M.R., Whisson, S.C., et al. (2005) Differential recognition of highly divergent downy mildew avirulence gene alleles by RPP1 resistance genes from two Arabidopsis lines. Plant Cell 17 : 1839 1850.
48. Rep, M. (2005) Small proteins of plant-pathogenic fungi secreted during host colonization. FEMS Microbiol Lett 253 : 19 27.
49. Rep, M., van der Does, H.C., Meijer, M., van Wijk, R., Houterman, P.M., Dekker, H.L., et al. (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.
50. Ridout, C.J., Skamnioti, P., Porritt, O., Sacristan, S., Jones, J.D.G. Brown, J.K.M. (2006) Multiple avirulence paralogues in cereal powdery mildew fungi may contribute to parasite fitness and defeat of plant resistance. Plant Cell 18 : 2402 2414.
51. Rouxel, T. Balesdent, M.H. (2005) The stem canker (blackleg) fungus, Leptosphaeria maculans, enters the genomic era. Mol Plant Pathol 6 : 225 241.
52. Rouxel, T., Penaud, A., Pinochet, X., Brun, H., Gout, L., Delourme, R., et al. (2003a) A 10-year survey of populations of Leptosphaeria maculans. France indicates a rapid adaptation towards the Rlm1 resistance gene of oilseed rape. Eur J Plant Pathol 109 : 871 881.
53. Rouxel, T., Willner, E., Coudard, L. Balesdent, M.H. (2003b) Screening and identification of resistance to Leptosphaeria maculans (stem canker) in Brassica napus accessions. Euphytica 133 : 219 231.
54. Sambrook, J. Russell, D.W. (2001) Molecular Cloning: A Laboratory Manual. Cold Spring Harbor, NY, USA : Cold Spring Harbor Laboratory Press.
55. Schürch, S., Linde, C.C., Knogge, W., Jackson, L.F. 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.
56. Shan, W.X., Cao, M., Dan, L.U. Tyler, B.M. (2004) The Avr1b locus of Phytophthora sojae encodes an elicitor and a regulator required for avirulence on soybean plants carrying resistance gene Rps1b. Mol Plant Microbe Interact 17 : 394 403.
57. Stahl, E.A. Bishop, J.G. (2000) Plant-pathogen arms races at the molecular level. Curr Opin Plant Biol 3 : 299 304.
58. Van Der Biezen, E.A. Jones, J.D.G. (1998) Plant disease-resistance proteins and the gene-for-gene concept. Trends Biochem Sci 23 : 454 456.
59. Van Kan, J.A.L., Van Den Ackerveken, G.F.J.M. De Wit, P.J.G.M. (1991) Cloning and characterization of cDNA of avirulence gene Avr9 of the fungal tomato pathogen Cladosporium fulvum, causal agent of tomato leaf mold. Mol Plant Microbe Interact 4 : 52 59.
60. Westerink, N., Brandwagt, B.F., de Wit, P.J.G.M. Joosten, M.H.A.J. (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.