Multiple resistance of Botrytis cinerea from kiwifruit to SDHIs, QoIs and fungicides of other chemical groups

Pest Management Science

Volumn 66, Issue 9, 2010, Pages 967-973

  Bardas, George A ^a   Veloukas, Thomas ^a   Koutita, Olga ^b   Karaoglanidis, George S ^a  

^a ARISTOTLE UNIVERSITY OF THESSALONIKI   (Greece)

^b Hellenic Sugar Industry SA   (Greece)

Author keywords

Boscalid; Botrytis cinerea; Chemical control; Grey mould; Pyraclostrobin

Indexed keywords

2 CHLORO N (4 CHLOROBIPHENYL 2 YL)NICOTINAMIDE; 2-CHLORO-N-(4-CHLOROBIPHENYL-2-YL)NICOTINAMIDE; BIPHENYL DERIVATIVE; CARBAMIC ACID DERIVATIVE; DRUG DERIVATIVE; ENZYME INHIBITOR; FUNGICIDE; NICOTINAMIDE; PYRACHLOSTROBIN; PYRAZOLE DERIVATIVE; SUCCINATE DEHYDROGENASE (UBIQUINONE);

CHEMICAL CONTROL; DISEASE RESISTANCE; FRUIT; FUNGAL DISEASE; FUNGICIDE; PATHOGENICITY; PESTICIDE RESISTANCE; PHENOTYPE; POPULATION STRUCTURE; SENSITIVITY ANALYSIS; TOXICITY;

ARTICLE; BOTRYTIS; DRUG ANTAGONISM; DRUG EFFECT; GENETICS; KIWIFRUIT; MICROBIOLOGY; MULTIDRUG RESISTANCE; POINT MUTATION;

ACTINIDIA; BIPHENYL COMPOUNDS; BOTRYTIS; CARBAMATES; DRUG RESISTANCE, MULTIPLE; ELECTRON TRANSPORT COMPLEX II; ENZYME INHIBITORS; FUNGICIDES, INDUSTRIAL; NIACINAMIDE; POINT MUTATION; PYRAZOLES;

GREECE;

ACTINIDIA DELICIOSA; BACTERIA (MICROORGANISMS); BOTRYOTINIA FUCKELIANA; BOTRYTIS; THESSALONIKI;

EID: 77955992827     PISSN: 1526498X     EISSN: 15264998     Source Type: Journal    
DOI: 10.1002/ps.1968     Document Type: Article

References (44)

1. Michailides TJ and Elmer PAG, Botrytis gray mold of kiwifruit caused by Botrytis cinerea in the United States and New Zealand. Plant Dis 84:208-223 (2000).
2. Baroffio CA, Siegfried W and Hilber UW, Long-term monitoring for resistance of Botrytis cinerea to anilinopyrimidine, phenylpyrrole, and hydroxyanilide fungicide in Switzerland. Plant Dis 87:662-666 (2003).
3. Jiang J, Ding L, Michailides TJ, Li H and Ma Z, Molecular characterization of field azoxystrobin-resistant isolates of Botrytis cinerea. Pestic Biochem Physiol 93:72-76 (2009).
4. Leroux P, Chapeland F, Desbrosses D and Gredt M, Patterns of cross-resistance to fungicides in Botryotinia fuckeliana (Botrytis cinerea) isolates from French vineyards. Crop Prot 18:687-697 (1999).
5. Myresiotis CK, Karaoglanidis GS and Tzavella-Klonari K, Resistance of Botrytis cinerea isolates from vegetable crops to anilinopyrimidine, phenylpyrrole, hydroxyanilide, benzimidazole, and dicarboximide fungicides. Plant Dis 91:407-413 (2007).
6. Pappas AC, Evolution of fungicide resistance in Botrytis cinerea in protected crops in Greece. Crop Prot 16:257-263 (1997).
7. Stammler G, Brix HD, Glättli A, Semar M and Schoefl U, Biological properties of the carboxamide boscalid including recent studies on its mode of action. Proc BCPC XVI Internat Plant Prot Cong, British Crop Protection Council, Alton, Hampshire, UK, pp. 16-21 (2007).
8. Avenot H, Morgan DPand Michailides TJ, Resistance to pyraclostrobin, boscalid and multiple resistance to Pristine (pyraclostrobin + boscalid) fungicide in Alternaria alternata causing alternaria late blight of pistachios in California. Plant Pathol 57:135-140 (2008).
9. Miyamoto T, Ishii H, Seko T, Kobori S and Tomita Y, Occurrence of Corynespora cassiicola isolates resistant to boscalid on cucumber in Ibaraki Prefecture, Japan. Plant Pathol 58:1144-1151 (2009).
10. Stammler G, Brix HD, Nave B, Gold R and Schoefl U, Studies on the biological performance of boscalid and its mode of action, in Modern Fungicides and Antifungal Compounds V. Deutsche Phytomedizinische Gesellschaft, Braunschweig, Germany, pp. 45-51 (2008).
11. Ammermann E, Lorenz G, Schelberger K, Mueller B, Kirstgen R and Sauter H, BAS 500 F-the new broadspectrum strobilurin fungicide. Proc Brighton Crop Prot Conf-Pests and Diseases. Vol. 2, British Crop Protection Council, Farnham, Surrey, UK, pp. 541-548 (2000).
12. Bartlett DW, Clough JM, Godwin JR, Hall AA, Hamer M and Parr-Dobrzanski B, The strobilurinfungicides.PestManagSci 58:649-662 (2002).
13. Baumler S, Felsenstein FG and Schwarz G, CAPS and DHPLC analysis of a single nucleotide polymorphism in the cytochrome b gene conferring resistance to strobilurins in field isolates of Blumeria graminis f. sp. hordei. J Phytopathol 151:149-152 (2003).
14. Fraaije BA, Cools HJ, Fountaine J, Lovell DJ, Motteram J, West JS, et al., Role of ascospores in further QoI-resistant cytochrome b alleles (G143A) in field populations of Mycosphaerella graminicola. Phytopathology 95:933-941 (2005).
15. Ishii H, Fraaije BA, Sugiyama T, Noguchi K, Nishimura K, Takeda T, et al., Occurrence and molecular characterization of strobilurin resistance in cucumber powdery mildew and downy mildew. Phytopathology 91:1166-1171 (2001).
16. Ma Z, Felts D and Michailides TJ, Resistance to azoxystrobin in Alternaria isolates from pistachio in California. Pestic Biochem Physiol 77:66-74 (2003).
17. Banno S, Yamashita K, Fukumori F, Okada K, Uekusa H, Takagaki M, et al., Characterization of QoI resistance in Botrytis cinerea and identification of two types of mitochondrial cytochrome b gene. Plant Pathol 58:120-129 (2009).
18. Stammler G and Speakman J, Microtiter method to test the sensitivity of Botrytis cinerea to boscalid. J Phytopathol 154:508-510 (2006).
19. Kretschmer M and Hahn M, Fungicide resistance and genetic diversity of Botrytis cinerea isolates from a vineyard in Germany. J Plant Dis Prot 115:214-19 (2008).
20. Martinez F, Dubos B and Fermaud M, The role of saprotrophy and virulence in the population dynamics of Botrytiscinerea in vineyards. Phytopathology 95:692-700 (2005).
21. Stehmann C and de Waard MA, Sensitivity of populations of Botrytis cinerea to triazoles, benomyl and vinclozolin. Eur J Plant Pathol 102:171-80 (1996).
22. Hilber UW and Schüepp H, A reliable method for testing the sensitivity of Botryotinia fuckeliana to anilinopyrimidines in vitro. Pestic Sci 47:241-247 (1996).
23. Williams JGK, Kubelik AR, Livak KJ, Rafalsky JA and Tingey SV, DNA polymorphisms amplified by arbitrary primers are useful as genetic markers. Nucl Acid Res 18:6531-6535 (1990).
24. Elad Y, Yunis H and Katan T, Multiple resistance to benzimidazoles, dicarboximides and diethofencarb in field isolates of Botrytis cinerea in Israel. Plant Pathol 41:41-46 (1992).
25. Moyano C, Gomez V and Melgarejo P, Resistance to pyrimethanil and other fungicides in Botrytis cinerea populations collected on vegetable crops in Spain. J Phytopathol 152:484-490 (2004).
26. Myresiotis CK, Bardas GA and Karaoglanidis GS, Baseline sensitivity of Botrytis cinerea to boscalid and pyraclostrobin and control of anilinopyrimidine-and benzimidazole-resistant strains by these fungicides. Plant Dis 92:1427-1431 (2008).
27. Yourman LF, Jeffers SN and Dean RA, Genetic analysis of isolates of Botrytis cinerea sensitive and resistant to benzimidazole and dicarboximide fungicides. Phytopathol 90:851-859 (2000).
28. Gisi U, Sierotzki H, Cook A and McCaffery A, Mechanisms influencing the evolution of resistance to QoI inhibitor fungicides. Pest Manag Sci 58:859-867 (2002).
29. Avenot HF, Sellam A and Michailides TJ, Characterization of mutations in the membrane-anchored subunits AaSDHC and AaSDHD of succinate dehydrogenase from Alternaria alternata isolates conferring field resistance to the fungicide boscalid. Plant Pathol 58:1134-1143 (2009).
30. Avenot HF, Sellam A, Karaoglanidis GS and Michailides TJ, Characterization of mutations in the iron-sulphur subunit of succinate dehydrogenase correlating with boscalid resistance in Alternaria alternata from California pistachio. Phytopathology 98:736-742 (2008).
31. Markoglou AN, Malandrakis AA, Vitoratos AG and Ziogas BN, Characterization of laboratory mutants of Botrytis cinerea resistant to QoI Fungicides. Eur J Plant Pathol 115:149-162 (2006).
32. Zhang CQ, Yuan SK, Sun HY, Qi ZQ, Zhou MG and Zhu GN, Sensitivity of Botrytis cinerea from vegetable greenhouses to boscalid. Plant Pathol 56:646-653 (2007).
33. De Waard MA, Andrade AC, Hayashi K, Schoonbeek 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).
34. Hayashi K, Schoonbeek 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).
35. Kretchmer M, Leroch M, Mosbach A, Walker A-S, Filinger S, Mernke D, et al., Fungicide-driven evolution and molecular basis of multidrug resistance in field populations of the grey mould fungus Botrytis cinerea. PLoS Pathogens 5:e1000696 (2009).
36. Schoonbeek H, Del Sorbo G and De Waard MA, The ABC transporter Bcatr D affects the sensitivity of Botrytis cinerea to the phytoalexin resveratrol and the fungicide fenpiclonil. Molec Plant Microb Internat 14:562-571 (2001).
37. Vermeulen T, Schoonbeek H and De Waard MA, The ABC transporter Bcatr D from Botrytis cinerea is a determinant of the phenylpyrrole fungicide fludioxonil. Pest Manag Sci 57:393-402 (2001).
38. Banno S, Fukumori F, Ichiishi A, Okada K, Uekusa H, Kimura M, et al., Genotyping of benzimidazole-resistant and dicarboximide-resistant mutations in Botrytis cinerea using real-time polymerase chain reaction assays. Phytopathology 98:397-404 (2008).
39. The FRAC Code List. [Online]. Fungicide Resistance Action Committee (2010). Available: http\\www.frac.info. [December 2009].
40. Leroux P, Chemical control of Botrytis and its resistance to chemical fungicides, in: Botrytis: Biology, Pathology and Control, ed. by Elad Y, Williamson B, Tudzynski P and Delen N. Springer, Dordrecht, The Netherlands, pp. 195-222 (2007).
41. Vignutelli A, Hilber-Bodmer M and Hilber UW, Genetic analysis of resistance to the phenylpyrrole fludioxonil and the dicarboximide vinclozolin in Botryotinia fuckeliana (Botrytis cinerea) Mycol Res 106:329-335 (2002).
42. Ziogas BN, Markoglou AN and Spyropoulou V, Effect of phenylpyrrole-resistance mutations on ecological fitness of Botrytis cinerea and their genetical basis in Ustilago maydis. Eur J Plant Pathol 113:83-100 (2005).
43. Fournier E, Levis C, Fortini D, Leroux P, Giraud T and Brygoo Y, Characterization of Bochco, the Botrytis cinerea homolog of the Neurospora crassa het-c vegetative incompatibility locus and its use as a population marker. Mycologia 95:251-261 (2003).
44. Leroux P, Fritz R, Debieu D, Albertini C, Lanen C, Bach J, et al., Mechanisms of resistance to fungicides in field strains of Botrytis cinerea. Pest Manag Sci 58:876-888 (2002).