Assessment of fungicide resistance and pathogen diversity in Erysiphe necator using quantitative real-time PCR assays

Pest Management Science

Volumn 67, Issue 1, 2011, Pages 60-69

  Dufour, Marie Cécile ^a   Fontaine, Séverine ^b   Montarry, Josselin ^a,c   Corio Costet, Marie France ^a  

^a BORDEAUX SCIENCES AGRO   (France)

^b Healthy Pigs Production and Experimentation Section   (France)

^c INRA   (France)

Author keywords

Biotype; DMI fungicide; Powdery mildew; Q PCR; QoI; Resistance

Indexed keywords

FUNGICIDE;

ALLELE; ASSAY; ASSESSMENT METHOD; BIOMONITORING; BIOTYPE; ENZYME ACTIVITY; FUNGICIDE; FUNGUS; INHIBITOR; MITOCHONDRION; PATHOGENICITY; PESTICIDE RESISTANCE; POLYMERASE CHAIN REACTION; POPULATION STRUCTURE; QUANTITATIVE ANALYSIS; SPECIES DIVERSITY; VINE; VINEYARD;

ALLELE; ANTIFUNGAL RESISTANCE; ARTICLE; ASCOMYCETES; DRUG EFFECT; GENETIC LINKAGE; GENETICS; GRAPE; METHODOLOGY; MICROBIOLOGY; PEST CONTROL; POLYMERASE CHAIN REACTION; SINGLE NUCLEOTIDE POLYMORPHISM;

ALLELES; ASCOMYCOTA; DRUG RESISTANCE, FUNGAL; FUNGICIDES, INDUSTRIAL; LOD SCORE; PEST CONTROL; POLYMERASE CHAIN REACTION; POLYMORPHISM, SINGLE NUCLEOTIDE; VITIS;

EUROPE; UNITED STATES;

ERYSIPHALES; ERYSIPHE NECATOR; NECATOR; VITIS;

EID: 78650236708     PISSN: 1526498X     EISSN: 15264998     Source Type: Journal    
DOI: 10.1002/ps.2032     Document Type: Article

References (55)

1. Délye C, Laigret F and Corio-Costet MF, RAPD analysis provides insight into the biology and epidemiology of Uncinula necator. Phytopathol 87: 670-677 (1997).
2. Evans KJ, Whisson DL, Stummer BE and Scott ES, DNA markers identify variation in Australian populations of Uncinula necator. Mycol Res 101: 923-932 (1997).
3. Amrani L and Corio-Costet MF, A single nucleotide polymorphism in the beta-tubulin gene distinguishing two genotypes of Erysiphe necator expressing different symptoms on grapevine. Plant Pathol 55: 505-512 (2006).
4. Cortesi P, Pizzati C, Bertocchi B and Milgroom MG, Persistence and spatial autocorrelation of clones of Erysiphe necator overwintering as mycelium in dormant buds in an isolated vineyard in northern Italy. Phytopathology 98: 148-152 (2008).
5. Delye C and Corio-Costet MF, Origin of primary infections of grape by Uncinula necator: RAPD analysis discriminates two biotypes. Mycol Res 102: 283-288 (1998).
6. Miazzi M, Hajjeh H and Faretra F, Observations on the population biology of the grape powdery mildew fungus Uncinula necator. J Plant Pathol 85: 123-129 (2003).
7. Montarry J, Cartolaro P, Delmott F, Jolivet J and Willocquet L, Genetic structure and aggressiveness of Erysiphe necator populations during grapevine powdery mildew epidemics. Appl Envir Microbiol 74: 6327-6332 (2008).
8. Corio-Costet MF, Erysiphe necator. Monograph, Tec/Doc Lavoisier, Paris, France, 132 pp. (2007).
9. Cortesi P, Ottaviani MP and Milgroom MG, Spatial and genetic analysis of flag shoot subpopulations of Erysiphe necator in Italy. Phytopathology 94: 554-550 (2004).
10. Miazzi M, Hajjeh H and Faretra F, Occurrence and distribution of two distinct genetic groups in populations of Erysiphe necator Schw. in southern Italy. J Plant Pathol 90: 563-573 (2008).
11. Corio-Costet MF, Délye C, Stievenard C, Douence L and Ronchi V, Biodiversity fungicide resistance of grape powdery mildew. Proceedings of Meeting on Integrated Control in Viticulture, Florence, Italy, March 1-4, 1999. Bull OILB/SROP 23: 33-36 (2000).
12. Corio-Costet MF, Bouscaut J, Delmotte F, Douence L, Richart-Cervera S and Amrani L, Genetic structure of powdery mildew and fungicide resistance: AFLP and molecular tools of detection. 7th ANPP Int Conf Plant Diseases, France, 3-5 December 2003, pp. 1-8 (2003).
13. Montarry J, Cartolaro P, Richard-Cervera S and Delmotte F, Spatio-temporal distribution of Erysiphe necator genetic groups and their relationships with disease levels in vineyards. Eur J Plant Pathol 123: 61-70 (2009).
14. Peros JP, Troulet C, Guerriero M, Michel-Romiti C and Notteghem JL, Genetic variation and population structure of the grape powdery mildew fungus, Erysiphe necator, in southern France. Eur J Plant Pathol 113: 407-416 (2005).
15. Peros JP, Nguyen TH, Troulet C, Michel-Romiti C and Notteghem JL, Assessment of powdery mildew resistance of grape and Erysiphe necator pathogenicity using a laboratory assay. Vitis 45: 29-36 (2006).
16. Bouscaut J and Corio-Costet MF, Biodiversity of the powdery mildew: role of retrotransposon discriminating by PCR genetic groups of Uncinula necator, in Oenologie 2003, ed. by Lonvaud A, De Revel G and Darriet P. Lavoisier, Paris, France, pp. 40-43 (2003).
17. Stummer BE, Zanker T, Scott ES and Whisson DL, Genetic diversity in populations of Uncinula necator: comparison of RFLP- and PCR-based approaches. Mycol Res 104: 44-52 (2000).
18. Debieu D, Corio-Costet MF, Steva H, Malosse C and Leroux P, Sterol composition of the wine powdery mildew fungus Uncinula necator sensitive or resistant strains to the sterol biosynthesis inhibitor triadimenol. Phytochemistry 39: 293-300 (1995).
19. Erickson EO and Wilcox WF, Distribution of sensitivities to three sterol demethylation inhibitor fungicides among populations of Uncinula necator sensitive and resistant to triadimefon. Phytopathology 87: 784-791 (1997).
20. Halleen F, Holz G and Pringle KL, Resistance in Uncinula necator to triazole fungicides in South African grapevines. South Afric J Enol Vitic 21: 71-80 (2000).
21. Wong FP and Wilcox WF, Sensitivity to azoxystrobin among isolates of Uncinula necator: baseline distribution and relationship to myclobutanil sensitivity. Plant Dis 86: 394-404 (2002).
22. Delye C, Laigret F and Corio-Costet MF, New tools for studying epidemiology and resistance of grape powdery mildew to DMI fungicides. Pestic Sci 51: 309-314 (1997).
23. Delye C, Laigret F and Corio-Costet MF, A mutation in the 14α-demethylase gene of Uncinula necator that correlates with resistance to a sterol biosynthesis inhibitor. Appl Environ Microbiol 63: 2966-2970 (1997).
24. Delye C, Laigret F and Corio-Costet MF, Cloning and sequence analysis of the eburicol 14α-demethylase gene of the obligate biotrophic grape powdery mildew fungus. Gene 195: 29-33 (1997).
25. Delye C, Bousset L and Corio-Costet MF, PCR cloning and detection of point mutations in the eburicol 14 alpha-demethylase (CYP51) gene from Erysiphe graminis f. sp. hordei, a 'recalcitrant' fungus. Curr Genetics 34: 399-403 (1998).
26. Wyand RA and Brown JKM, Sequence variation in the CYP51 gene of Blumeria graminis associated with the resistance to sterol demethylase inhibiting fungicides. Fungal Genet Biol 42: 746-735 (2005).
27. Baudoin A, Olaya AG, Delmontte F, Colcol F and Sierotski H, QoI resistance of Plasmopara viticola and Erysiphe necator in the Mid-Atlantic United States. Plant Manag Network, Plant Health Prog DOI: 10.1094/PHP-2008, p.0211-02 (2008).
28. Kianianmomeni A, Schwarz G, Felsenstein FG and Wenzel G, Validation of a real-time PCR for the quantitative estimation of a G143A mutation in the cytochrome bc(1) gene of Pyrenophora teres. Pest Manag Sci 63: 219-224 (2007).
29. Bäumler S, Sierotski H, Gisi U, Mohler V, Felsentein FG and Schwarz G, Evaluation of Erysiphe graminis f. sp. tritici field isolates for resistance to strobilurin fungicides with different SNP detection systems. Pest Manag Sci 59: 310-314 (2003).
30. Luo Y, Ma Z and Michailides TJ, Quantification of allele E198A in beta-tubulin conferring benzimidazole resistance in Monilia fructicola using real-time PCR. Pest Manag Sci 63: 1178-1184 (2007).
31. Schwarz G, Baumler S, Block A, Felsenstein FG and Wenzel G, Determination of detection and quantification limits for SNP allele frequency estimation in DNA pools using real time PCR-art. no. e24. Nucleic Acids Res 32: E24-E24 (2004).
32. Yan L, Yang Q, Zhou Y, Duan X and Ma Z, A real-PCR assay for quantification of the Y136F allele in the CYP51 gene associated with Blumeria graminis f. sp. tritici resistance to sterol demethylase inhibitors. Crop Prot 28: 376-280 (2009).
33. Chen C, Zhao W, Lu Y, Wang J, Chen Y, Li H, et al, High-throughput detection of highly benzimidazole-resistant allele E189A with mismatch primers in allele-specific real-time polymerase chain reaction. Pest Manag Sci 65: 413-419 (2008).
34. Zhang T and Fang HHP, Applications of real-time polymerase chain reaction for quantification of microorganisms in environmental samples. Appl Microbiol Biotechnol 70: 281-289 (2006).
35. Fraaije BA, Butter JA, Coehlo JM, Jones DR and Hollomon DW, Following the dynamics of strobilurin resistance in Blumeria graminis f. sp. tritici using quantitative allele-specific real-time PCR measurements with the fluorescent dye SYBR Green I. Plant Pathol 51: 45-54 (2002).
36. Valsesia G, Gobbin D, Patocchi A, Vecchione A, Pertot I and Gessler C, Development of a high-throughput method for quantification of Plasmopara viticola DNA in grapevine leaves by means of quantitative Real-Time Polymerase chain reaction. Phytopathology 95: 672-678 (2005).
37. Sirven C, Gonzalez E, Bufflier E, Latorse MP and Beffa R, PCR-based method for detecting mutation allele frequencies for QoI resistance in Plasmopara viticola, Proc BCPC Conference: Pests and Diseases, British Crop Protection Council, Alton, Hants, UK, pp. 823-828 (2002).
38. Toffolatti SL, Serrati L, Sierotzki H, Gisi U and Vercesi A, Assessment of QoI resistance in Plasmopara viticola oospores. Pest Manag Sci 63: 194-201 (2007).
39. Delye C, Ronchi V, Laigret F and Corio-Costet MF, Nested allele-specific PCR primers distinguish genetic groups of Uncinula necator. Appl Envir Microbiol 65: 3950-3954 (1999).
40. Bouscaut J and Corio-Costet MF, Detection of a specific transposon in Erysiphe necator from grapevines in France. J Phytopathol 155: 381-383 (2007).
41. Hajjeh H, Miazzi M, De Guido MA and Faretra F, Specific SCAR primers for the 'flag shoot' and 'ascospore' biotypes of the grape powdery mildew fungus Erysiphe necator. J Plant Pathol 87: 71-74 (2005).
42. Nunez Y, Gallego J, Ponz F and Raposo R, Analysis of population structure of Erysiphe necator using AFLP markers. Plant Pathol 55: 650-656 (2006).
43. Delye C, Corio-Costet MF and Laigret F, A RAPD assay for strain typing of the biotrophic grape powdery mildew fungus Uncinula necator using DNA extracted from the mycelium. Exp Mycol 19: 234-237 (1995).
44. Martinez F, Dubos B and Fermaud M, The role of saprotrophy and virulence in the population dynamics of Botrytis cinerea in vineyards. Phytopathology 95: 692-700 (2005).
45. Leroux P, Albertini C, Gauthier A, Gredt M and Wallker AS, Mutations in the cyp51 gene correlated with changes in sensitivity to sterol 14 alpha-demethylation inhibitors in field isolates of Mycosphaerella graminicola. Pest Manag Sci 63: 688-698 (2007).
46. Hamamoto H, Hasegawa K, Nakaune R, Makizumi YJ, Akutsu K and Hibi T, Tandem repeat of a transcriptional enhancer upstream of the sterol 14 alpha-demethylase (CYP51A1) in Penicillium digitatum. Appl Environ Microbiol 66: 3421-3426 (2000).
47. Luo CX, Cox KD, Amirir A and Schnabel G, Occurrence and detection of the DMI resistance-associated genetic element 'Mona' in Monilia fructicola. Plant Dis 92: 1099-1103 (2008).
48. Lupetti A, Danesi R, Campa M, Del Tacca M and Kelly S, Molecular basis of resistance to azole antifungals. Trends Mol Med 8: 76-81 (2002).
49. Ma ZH, Proffer TJ, Jacobs JL and Sundin GW, Overexpression of the 14 alpha-demethylase target gene (CYP51) mediates fungicide resistance in Blumeriella jaapii. Appl Envir Microbiol 72: 2581-2585 (2006).
50. Schnabel G and Jones AL, The 14 alpha-demethylase (CYP51A1) gene is overexpressed in Venturia inaequalis strains resistant to myclobutanil. Phytopathology 91: 102-110 (2001).
51. De Waard MA, Andrade AC, Hayashi K, Schoonbeck HJ, Stergiopoulos I and Zwiers LH, Impact of fungal drug transporters on fungicide sensitivity, multidrug resistance and virulence. Pest Manag Sci 62: 195-207 (2006).
52. Hayashi K, Schoonbeck H and De Waard MA, Expression of the ABC transporter BcatrD from Botrytis cinerea reduces sensitivity to sterol demethylation inhibitor fungicides. Pestic Biochem Physiol 73: 110-121 (2002).
53. Stergiopoulos I, Van Nistelrooy JGM, Kema GHJ and De Waard MA, Multiple mechanisms account for variation in baseline sensitivity to azole fungicides in field isolates of Mycosphaerella graminicola. Pest Manag Sci 59: 1333-1343 (2003).
54. Sombardier A, Dufour MC, Blancard D and Corio-Costet MF, Sensitivity of Podosphaera aphanis isolates to DMI fungicides: distribution and reduced cross-sensitivity. Pest Manag Sci 66: 35-43 (2010).
55. Bartlett DW, Clough JM, Godwin JR, Hall AA, Hamer J and Parr-Dobrzanski B, The strobilurin fungicides. Pest Manag Sci 58: 649-662 (2002).