Estimating frequencies of virulent isolates in field populations of a plant pathogenic fungus, Leptosphaeria maculans, using high-throughput pyrosequencing

Journal of Applied Microbiology

Volumn 113, Issue 5, 2012, Pages 1145-1153

  van de Wouw, A P ^a   Howlett, B J ^a  

^a UNIVERSITY OF MELBOURNE   (Australia)

Author keywords

Avirulence genes; Brassica napus; Leptosphaeria maculans; Pyrosequencing

Indexed keywords

ASSAYS; CROPS; DNA SEQUENCES; PATHOGENS; THROUGHPUT;

AVIRULENCE; AVIRULENCE GENE; BRASSICA NAPUS; FIELD POPULATIONS; HIGH-THROUGHPUT; IN-FIELD; LEPTOSPHAERIA MACULANS; PLANT PATHOGENIC FUNGUS; PYROSEQUENCING; SINGLE NUCLEOTIDE POLYMORPHISMS;

GENES;

ALLELE; CANOLA; FUNGUS; MICROBIAL COMMUNITY; MUTATION; PATHOGEN; PESTICIDE RESISTANCE; POLYMORPHISM; RISK FACTOR; SOIL MICROORGANISM; SPORE; VIRULENCE;

AMINO ACID SUBSTITUTION; ARTICLE; ASCOMYCETES; AVRLM4 GENE; FUNGAL GENE; FUNGAL VIRULENCE; FUNGUS ISOLATION; GENE AMPLIFICATION; GENE FREQUENCY; GENE LOCUS; GENE MUTATION; GENE SEQUENCE; LEPTOSPHAERIA MACULANS; NUCLEOTIDE SEQUENCE; PYROSEQUENCING; RAPESEED; RLM4 GENE; SEQUENCE ANALYSIS; SEXUAL SPORE; SINGLE NUCLEOTIDE POLYMORPHISM;

BRASSICA NAPUS; BRASSICA NAPUS VAR. NAPUS; FUNGI; LEPTOSPHAERIA MACULANS;

EID: 84867731673     PISSN: 13645072     EISSN: 13652672     Source Type: Journal    
DOI: 10.1111/j.1365-2672.2012.05413.x     Document Type: Article

References (38)

1. Alderborn, A., Kristofferson, A. and Hammerling, U. (2000) Determination of single-nucleotide polymorphisms by real-time pyrophosphate DNA sequencing. Genome Res 10, 1249-1258.
2. Balesdent, M.H., Barbetti, M.J., Hua, L., Sivasithamparam, K., Gout, L. and Rouxel, T. (2005) Analysis of Leptosphaeria maculans race structure in a worldwide collection of isolates. Phytopathology 95, 1061-1071.
3. Cools, H.J. and Fraaije, B.A. (2008) Are azole fungicides losing ground against Septoria wheat disease? Resistance mechanisms in Mycosphaerella graminicola. Pest Manag Sci 64, 681-684.
4. Delourme, R., Chevre, A.M., Brun, H., Rouxel, T., Balesdent, M.H., Dias, J.S., Salisbury, P., Renard, M. et al. (2006) Major gene and polygenic resistance to Leptosphaeria maculans in oilseed rape (Brassica napus). Eur J Plant Pathol 114, 41-52.
5. Dilmaghani, A., Balesdent, M.H., Didier, J.P., Wu, C., Davey, J., Barbetti, M.J., Li, H., Moreno-Rico, O. et al. (2009) The Leptosphaeria maculans - Leptosphaeria biglobosa species complex in the American continent. Plant Pathol 58, 1044-1058.
6. Fitt, B.D.L., Brun, H., Barbetti, M.J. and 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.
7. Fudal, I., Ross, S., Gout, L., Blaise, F., Kuhn, M.L., Eckert, M.R., Cattolico, L., Bernard-Samain, S. 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 Int 20, 459-470.
8. Fudal, I., Ross, S., Brun, H., Besnard, A.L., Ermel, M., Kuhn, M.L., Balesdent, M.H. and Rouxel, T. (2009) Repeat-Induced Point mutation (RIP) as an alternative mechanism of evolution toward virulence in Leptosphaeria maculans. Mol Plant Microbe Int 22, 932-941.
9. 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.
10. Gout, L., Kuhn, M.L., Vincenot, L., Bernard-Samain, S., Cattolico, L., Barbetti, M., Moreno-Rico, O., Balesdent, M.H. et al. (2007) Genome structure impacts molecular evolution at the AvrLm1 avirulence locus of the plant pathogen Leptosphaeria maculans. Environ Microbiol 9, 2978-2992.
11. Gruber, J.D., Colligan, P.B. and Wolford, J.K. (2002) Estimation of single nucleotide polymorphism allele frequency in DNA pools by using pyrosequencing. Hum Genet 110, 395-401.
12. Hayford, A.E., Mammel, M.K., Lacher, D.W. and Brown, E.W. (2011) Single nucleotide polymorphism (SNP)-based differentiation of Shigella isolates by pyrosequencing. Infect Genet Evol 11, 1761-1768.
13. Hirst, J.M. and Stedman, O.J. (1962) The epidemiology of apple scab (Venturia inaequalis) II. Observations on the liberation of ascospores. Ann Appl Biol 50, 525-550.
14. Huang, Y.J., Li, Z.Q., Evans, N., Rouxel, T., Fitt, B.D.L. and Balesdent, M.H. (2006) Fitness cost associated with loss of the AvrLm4 avirulence function in Leptosphaeria maculans (phoma stem canker of oilseed rape). Eur J Plant Pathol 114, 77-89.
15. Huang, Y.J., Balesdent, M.H., Li, Z.Q., Evans, N., Rouxel, T. and Fitt, B.D.L. (2010) Fitness cost of virulence differs between the AvrLm1 and AvrLm4 loci in Leptosphaeria maculans (phoma stem canker of oilseed rape). Eur J Plant Pathol 126, 279-291.
16. Koch, E., Song, K., Osborn, T.C. and Williams, P.H. (1991) Relationship between pathogenicity and phylogeny based on restriction fragment length polymorphism in Leptosphaeria maculans. Mol Plant Microbe Int 4, 341-349.
17. Lindner, D.L., Garga, A., Lorch, J.M., Banik, M.T., Glaeser, J., Kunz, T.H. and Blehert, D.S. (2011) DNA-based detection of the fungal pathogen Geomyces destructans in soils from bat hibernacula. Mycologia 103, 241-246.
18. Long, Y., Wang, Z., Sun, Z., Fernando, D.W.G., McVetty, P.B.E. and Li, G. (2011) Identification of two blackleg resistance genes and fine mapping of one of these two genes in a Brassica napus cultivar 'Surpass 400'. Theor Appl Genet 122, 1223-1231.
19. Marcroft, S.M., Elliott, V.L., Cozijnsen, A.J., Salisbury, P.A., Howlett, B.J. and Van de Wouw, A.P. (2012a) Identifying resistance genes to Leptosphaeria maculans in Australian Brassica napus cultivars based on reactions to isolates with known avirulence genotypes. Crop Pasture Sci 63, 338-350.
20. Marcroft, S.M., Van de Wouw, A.P., Salisbury, P.A., Potter, T.D. and Howlett, B.J. (2012b) Effect of rotation of canola (Brassica napus) cultivars with different complements of blackleg resistance genes on disease severity. Plant Pathol, in press. doi: 10.1111/j.1365-3059.2011.02580.x.
21. Newton, C.R., Graham, A., Heptinstall, L.E., Powell, S.J., Summers, C., Kalsheker, N., Smith, J.C. and Markham, A.F. (1989) Analysis of any point mutation in DNA. The amplification refractory mutation system (ARMS). Nucleic Acids Res 17, 2503-2516.
22. Purwantara, A., Salisbury, P.A., Burton, W.A. and Howlett, B.J. (1998) Reaction of Brassica juncea (Indian mustard) lines to Australian isolates of Leptosphaeria maculans under glasshouse and field conditions. Eur J Plant Pathol 104, 895-902.
23. 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 the Rlm4 and Rlm7 resistance genes of oilseed rape, and circumvents Rlm4-mediated recognition through a single amino acid change. Mol Microbiol 71, 851-863.
24. Purwantara, A., Barrins, J.M., Cozijnsen, A.J., Ades, P.K. and Howlett, B.J. (2000) Genetic diversity of isolates of the Leptosphaeria maculans species complex from Australia, Europe and North America using amplified fragment length polymorphism analysis. Mycol Res 104, 772-781.
25. Rimmer, S.R. (2006) Resistance genes to Leptosphaeria maculans in Brassica napus. Can J Plant Pathol 28, S288-S297.
26. Rogers, S.L., Atkins, S.D. and West, J.S. (2009) Detection and quantification of airborne inoculum of Sclerotinia sclerotiorum using quantitative PCR. Plant Pathol 58, 324-331.
27. Selker, E.U. and Garrett, P.W. (1988) DNA sequence duplications trigger gene inactivation in Neurospora crassa. Proc Natl Acad Sci USA 85, 6870-6874.
28. Sexton, A.C. and Howlett, B.J. (2000) Characterisation of a cyanide hydratase gene in the phytopathogenic fungus Leptosphaeria maculans. Mol Gen Genet 263, 463-470.
29. Sprague, S.J., Balesdent, M.H., Brun, H., Hayden, H.L., Marcroft, S.J., Pinochet, X., Rouxel, T. and Howlett, B.J. (2006) Major gene resistance in Brassica napus (oilseed rape) is overcome by changes in virulence of populations of Leptosphaeria maculans in France and Australia. Eur J Plant Pathol 114, 33-40.
30. Stammler, G., Carstensen, M., Koch, A., Semar, M., Strobel, D. and Schlehuber, S. (2008) Frequency of different CYP51-haplotypes of Mycosphaerella graminicola and their impact on epoxiconazole-sensitivity and-field efficacy. Crop Protection 27, 1448-1456.
31. Stergiopoulos, I., De Kock, M.J.D., Lindhout, P. and De Wit, P.J.G.M. (2007) Allelic variation in the effector genes of the tomato pathogen Cladosporium fulvum reveals different modes of adaptive evolution. Mol Plant Microbe Int 20, 1271-1283.
32. Takala, S.L., Smith, D.L., Stine, O.C., Coulibaly, D., Thera, M.A., Doumbo, O.K. and Plowe, C.V. (2006) A high-throughput method for quantifying alleles and haplotypes of the malaria vaccine candidate Plasmodium falciparum merozoite surface protein-I 19 kDa. Malaria J 5, 31.
33. Van de Wouw, A.P., Cozijnsen, A.J., Hane, J.K., Brunner, P.C., McDonald, B.A., Oliver, R.P. and Howlett, B.J. (2010a) Evolution of linked avirulence effectors in Leptosphaeria maculans is affected by genomic environment and exposure to resistance genes in host plants. PLoS Pathog 6, e1001180.
34. Van de Wouw, A.P., Stonard, J.F., Howlett, B.J., West, J.S., Fitt, B.D.L. and Atkins, S.D. (2010b) Determining frequencies of avirulent alleles in airborne Leptosphaeria maculans inoculum using quantitative PCR. Plant Pathol 59, 809-818.
35. Wasson, J., Skolnick, G., Love-Gregory, L. and Permutt, M.A. (2002) Assessing allele frequencies of single nucleotide polymorphisms in DNA pools by pyrosequencing technology. Biotechniques 32, 1144-1146.
36. Ye, S., Dhillon, S., Ke, X., Collins, A.R. and Day, I.N.M. (2001) An efficient procedure for genotyping single nucleotide polymorphisms. Nucleic Acids Res 29, e88.
37. Yu, F., Lydiate, D.J. and Rimmer, S.R. (2005) Identification of two novel genes for blackleg resistance in Brassica napus. Theor Appl Genet 110, 969-979.
38. Yu, F., Lydiate, D.J. and Rimmer, S.R. (2008) Identification and mapping of a third blackleg resistance locus in Brassica napus derived from B. rapa subsp. sylvestris. Genome 51, 64-72.