Evaluation of a matrix to calculate fungicide resistance risk
2013; Wiley; Volume: 70; Issue: 6 Linguagem: Inglês
10.1002/ps.3646
ISSN1526-4998
AutoresM. K. Grimmer, Frank van den Bosch, Stephen J. Powers, N. D. Paveley,
Tópico(s)Plant Pathogens and Resistance
ResumoPest Management ScienceVolume 70, Issue 6 p. 1008-1016 Research Article Evaluation of a matrix to calculate fungicide resistance risk Michael K Grimmer, Michael K Grimmer ADAS Boxworth, Cambridge, UKSearch for more papers by this authorFrank van den Bosch, Frank van den Bosch Department of Computational and Systems Biology, Rothamsted Research, Harpenden, UKSearch for more papers by this authorStephen J Powers, Stephen J Powers Department of Computational and Systems Biology, Rothamsted Research, Harpenden, UKSearch for more papers by this authorNeil D Paveley, Corresponding Author Neil D Paveley ADAS High Mowthorpe, Duggleby, Malton, UKCorrespondence to: Neil Paveley, ADAS High Mowthorpe, Duggleby, Malton YO17 8BP, UK. E-mail: [email protected]Search for more papers by this author Michael K Grimmer, Michael K Grimmer ADAS Boxworth, Cambridge, UKSearch for more papers by this authorFrank van den Bosch, Frank van den Bosch Department of Computational and Systems Biology, Rothamsted Research, Harpenden, UKSearch for more papers by this authorStephen J Powers, Stephen J Powers Department of Computational and Systems Biology, Rothamsted Research, Harpenden, UKSearch for more papers by this authorNeil D Paveley, Corresponding Author Neil D Paveley ADAS High Mowthorpe, Duggleby, Malton, UKCorrespondence to: Neil Paveley, ADAS High Mowthorpe, Duggleby, Malton YO17 8BP, UK. E-mail: [email protected]Search for more papers by this author First published: 06 September 2013 https://doi.org/10.1002/ps.3646Citations: 33Read the full textAboutPDF ToolsRequest permissionExport citationAdd to favoritesTrack citation ShareShare Give accessShare full text accessShare full-text accessPlease review our Terms and Conditions of Use and check box below to share full-text version of article.I have read and accept the Wiley Online Library Terms and Conditions of UseShareable LinkUse the link below to share a full-text version of this article with your friends and colleagues. Learn more.Copy URL Share a linkShare onEmailFacebookTwitterLinkedInRedditWechat Abstract BACKGROUND In the European Union, assessments of resistance risk are required by the regulatory authorities for each fungicide product and are used to guide the extent of anti-resistance strategies. This paper reports an evaluation of a widely used 'risk matrix', to determine its predictive value. Sixty-seven unique cases of fungicide resistance in Europe were identified for testing the risk assessment scheme, where each case was the first occurrence of resistance in a pathogen species against a fungicide group. RESULTS In most cases, high-, moderate- and low-risk categories for fungicide, pathogen and agronomic systems were each associated with significant differences in the number of years from fungicide introduction to the first detection of resistance (FDR time). The combined risk, calculated by multiplying the individual risk factors using the risk matrix, had useful predictive power (72.8% of FDR time variance accounted for; VAF) for all fungicides, but only limited predictive power (25.8% VAF) for single-site acting fungicides (the predominant type). CONCLUSION The resistance risk matrix has significant, but limited, predictive value. New fungicide modes of action, or pathogens that have become newly prevalent, cannot be assigned to risk categories until new methods of resistance risk assessment are developed. © 2013 Society of Chemical Industry REFERENCES 1Steffens JJ, Pell EJ and Tien M, Mechanisms of fungicide resistance in phytopathogenic fungi. Curr Opin Biotechnol 7: 348–365 (1996). 2Ma Z and Michailides TJ, Advances in understanding molecular mechanisms of fungicide resistance and molecular detection of resistant genotypes in phytopathogenic fungi. Crop Protect 24: 853–863 (1995). 3van den Bosch F, Paveley N, Shaw M, Hobbelen P and Oliver R, The dose rate debate: does the risk of fungicide resistance increase or decrease with dose? Plant Pathol 4: 597–606 (2011). 4Anon., Regulation (EC) No 1107/2009 of the European Parliament and of the Council of 21 October 2009 concerning the placing of plant protection products on the market and repealing Council Directives 79/117/EEC and 91/414/EEC, in Official Journal of the European Union L 309 24.11.2009 p. 1 (2009). 5Kuck K-H and Russell PE, FRAC: combined resistance risk assessment. Asp Appl Biol 78: 3–10 (2006). 6Brent KJ and Hollomon DW, Fungicide Resistance in Crop Pathogens: How Can it be Managed? FRAC Monograph No. 1 (second, revised edition). Fungicide Resistance Action Committee, Brussels, Belgium, 57 pp. (2007). 7Brent KJ and Hollomon DW, Fungicide Resistance: The Assessment of Risk. FRAC Monograph No. 2 (second, revised edition). Fungicide Resistance Action Committee, Brussels, Belgium, 53 pp. (2007). 8Georgopoulos SG, Case study 1: Cercospora beticola of sugar beets, in Fungicide Resistance in Crop Protection, ed. by J Dekker and SG Georgopoulos. Pudoc, Wageningen, Netherlands, pp. 187–194 (1982). 9Phillips AN and Locke T, Carbendazim resistance in Rhynchosporium secalis in England and Wales, in Fungicide Resistance. BCPC Monograph Number 60, ed. by S Heaney, D Slawson, DW Hollomon, M Smith, PE Russell and DW Parry. British Crop Protection Council, Farnham, UK, pp. 251–254 (1994). 10Hide GA and Hall SM, Development of resistance to thiabendazole in Helminthosporium solani (silver scurf) as a result of potato seed tuber treatment. Plant Pathol 42: 707–714 (1993). 11Olvang H, Benomyl resistance in Gerlachia nivalis. I. Survey of diseased plants in the field. J Plant Dis Protect 91: 294–300 (1984). 12Locke T, Current incidence of fungicide resistance in pathogens of cereals in the UK, in British Crop Protection Conference Pests and Diseases. The British Crop Protection Council, Farnham, UK, pp. 781–786 (1986). 13Malathrakis NE and Vakalounakis DJ, Resistance to benzimidazole fungicides in the gummy stem blight pathogen Didymella bryoniae on cucurbits. Plant Pathol 32: 395–399 (1983). 14Magnus HA, Fungicide resistance. Present situation and fungicide strategy in Norway. Vaextskyddsrapporter, Jordbruk 48: 36–40 (1987). 15Fletcher JT, Tolerance of fungal pathogens to systemic fungicides in relation to disease control, in 8th British Insecticide and Fungicide Conference, The British Crop Protection Council, London, UK, pp. 751–762 (1975). 16Hollomon DW, Resistance to azole fungicides in the field. Biochem Soc Trans 21: 1047–1051 (1993). 17Kendall SJ, Hollomon DW, Cooke LR and Jones DR, Changes in sensitivity to DMI fungicides in Rhynchosporium secalis. Crop Protect 12: 357–362 (1993). 18de Waard MA, Kipp EMC, Horn NM and van Nistelrooy JGM, Variation in sensitivity to fungicides which inhibit ergosterol biosynthesis in wheat powdery mildew. Neth J Plant Pathol 92: 21–32 (1986). 19Dyer PS, Hansen J, Delaney A and Lucas JA, Genetic control of resistance to the sterol 14α-demethylase inhibitor fungicide prochloraz in the cereal eyespot pathogen Tapesia yallundae. Appl Environ Microb 66: 4599–4604 (2000). 20Karaoglanidis GS, Karadimos DA, Ioannidis PM and Ioannidis PI, Sensitivity of Cercospora beticola populations to fentin-acetate, benomyl and flutriafol in Greece. Crop Protect 22: 735–740 (2003). 21Staub T, Early experiences with phenylamide resistance and lessons for continued successful use, in Fungicide Resistance. BCPC Monograph Number 60, ed. by S Heaney, D Slawson, DW Hollomon, M Smith, PE Russell and DW Parry. British Crop Protection Council, Farnham, UK, pp. 131–138 (1994). 22Crute IR, Norwood JM and Gordon PL, The occurrence, characteristics and distribution in the United Kingdom of resistance to phenylamide fungicides in Bremia lactucae (lettuce downy mildew). Plant Pathol 36: 297–315 (1987). 23Locke T, Scrace J and Peace JM, Resistance of Phytophthora porri to metalaxyl. Pest Sci 51: 371–374 (1997). 24Brown JKM, Slater SE and See KA, Sensitivity of Erysiphe graminis f.sp. hordei to morpholine and piperidine fungicides. Crop Protect 10: 445–454 (1991). 25Lorenz G, Saur R, Schelberger K, Forster B, Küng R and Zobrist P, Long term monitoring results of wheat powdery mildew sensitivity towards fenpropimorph and strategies to avoid the development of resistance, in Brighton Crop Protection Conference Pests and Diseases. The British Crop Protection Council, Farnham, UK, pp. 171–176 (1992). 26Dekker J and Gielink JA, Decreased sensitivity to pyrazophos of cucumber and gherkin powdery mildew. Neth J Plant Pathol 85: 137–142 (1979). 27Gisi U, Sierotzki H, Cook A and McCaffery A, Mechanisms influencing the evolution of resistance to Qo inhibitor fungicides. Pest Manag Sci 58: 859–867 (2002). 28Heaney SP, Hall AA, Davies SA and Olaya G, Resistance to fungicides in the QoI-STAR cross-resistance group, in The BCPC Conference Pests and Diseases. The British Crop Protection Council, Farnham, UK, pp. 755–762 (2000). 29Fontaine S, Remuson F, Fraissinet-Tachet L, Micoud A, Marmeisseb R and Melayahb D, Monitoring of Venturia inaequalis harbouring the QoI resistance G143A mutation in French orchards as revealed by PCR assays. Pest Manag Sci 65: 74–81 (2009). 30Skorda EA, Resistance of wheat bunt to hexachlorobenzene and quintozene (pentachloronitrobenzene) in Greece, in British Crop Protection Conference Pests and Diseases. The British Crop Protection Council, London, UK, pp. 67–71 (1977). 31Gullino ML, Mescalchin E and Mezzalama M, Sensitivity to cymoxanil in populations of Plasmopara viticola in northern Italy. Plant Pathol 46: 729–736 (1997). 32Giannopolitis CN and Chrysayi-Tokousbalides M, Biology of triphenyltin-resistant strains of Cercospora beticola from sugar beet. Plant Dis 64: 940–942 (1980). 33Meszka B, Broniarek-Niemiec A and Bielenin A, The status of dodine resistance of Venturia inaequalis populations in Poland. Phytopathol Pol 47: 57–61 (2008). 34Noble M, Maggarvie QD, Hams AF and Leaf LL, Resistance to mercury of Pyrenophora avenae in Scottish seed oats. Plant Pathol 15: 23–28 (1966). 35Locke T and Phillips AN, The occurrence of carbendazim resistance in Rhynchosporium secalis on winter barley in England and Wales in 1992 and 1993. Plant Pathol 44: 294–300 (1995). 36Harrison JG, The biology of Botrytis spp. on Vicia beans and chocolate spot disease—a review. Plant Pathol 37: 168–201 (1988). 37Sutherland KG, Griffin-Walker V and Oxley SJP, Resistance of light leaf spot (Pyrenopeziza brassicae) of winter oilseed rape to MBC fungicides, in Brighton Crop Protection Conference Pests and Diseases. The British Crop Protection Council, Farnham, UK, pp. 463–468 (1994). 38Choiseul JW and Bannon E, Fusarium spp. associated with dry rot of potato in Ireland, in 7th International Congress of Plant Patholology, BSPP, Birmingham, UK (1998). 39Peters JC, Lees AK, Cullen DW, Sullivan L, Stroud GP and Cunnington AC, Characterization of Fusarium spp. responsible for causing dry rot of potato in Great Britain. Plant Pathol 57: 262–271 (2008). 40Hide GA, Read PJ and Hall SM, Resistance to thiabendazole in Fusarium species isolated from potato tubers affected by dry rot. Plant Pathol 41: 745–748 (1992). 41Hide GA, Hall SM and Boorer KJ, Resistance to thiabendazole in isolates of Helminthosporium solani, the cause of silver scurf disease of potatoes. Plant Pathol 37: 377–380 (1988). 42Carnegie SF and Cameron AM, Resistance to thiabendazole in isolates of Polyscytalum pustulans (skin spot) and Fusarium solani var. coeruleum (dry rot) in Scotland. Plant Pathol 41: 606–610 (1992). 43Berrie AM and Koomen I, Benzimidazole and dicarboximide resistance in pathogens of stored apples and pears, in Fungicide Resistance. BCPC Monograph Number 60, ed. by S Heaney, D Slawson, DW Hollomon, M Smith, PE Russell and DW Parry. British Crop Protection Council, Farnham, UK, pp. 207–217 (1994). 44Gladders P, Carter MA and Owen WF, Resistance to benomyl in Botrytis allii from shallots. Plant Pathol 43: 410–411 (1994). 45Presly AH and Maude RB, Control of Botrytis cinerea and Botrytis squamosa in overwintered salad onions by fungicide sprays. Ann Appl Biol 94: 197–204 (1979). 46Locke T, Moon LM and Evans J, Survey of benomyl resistance in Fusarium species on winter wheat in England and Wales in 1986. Plant Pathol 36: 589–593 (1987). 47Munro JM, Dolan A and Williamson B, Cane spot (Elsinoë veneta) in red raspberry: infection periods and fungicidal control. Plant Pathol 37: 390–396 (1988). 48Penaud A, Huguet B, Wilson V and Leroux P, Benzimidazole resistance of Sclerotinia sclerotiorum in French oilseed rape crops, in Proceedings of Sclerotinia 2001—The XI International Sclerotinia Workshop, BSPP and ISPP, York, UK, pp. 117–118 (2001). 49Mercer PC and Cooke LR, Resistance to iprodione in Alternaria linicola, in Fungicide Resistance. BCPC Monograph Number 60, ed. by S Heaney, D Slawson, DW Hollomon, M Smith, PE Russell and DW Parry, British Crop Protection Council, Farnham, UK, pp. 243–250 (1994). 50Entwistle AR, The effect of dicarboximide fungicides on Sclerotium cepivorum, in 10th International Congress of Plant Protection, The British Crop Protection Council, Croydon, UK, p. 629 (1983). 51Alberoni G, Collina M, Cavallini D and Brunelli A, Stemphylium vesicarium resistance to fungicides on pear in Italy, in Modern Fungicides and Antifungal Compounds V Conference, 15th International Reinhardsbrunn Symposium, Friedrichroda, Germany, pp. 167–172 (2007). 52Iacomi-Vasilescu B, Avenot H, Bataillé-Simoneau N, Laurent E, Guénard M and Simoneau P, In vitro fungicide sensitivity of Alternaria species pathogenic to crucifers and identification of Alternaria brassicicola field isolates highly resistant to both dicarboximides and phenylpyrroles. Crop Protect 23: 481–488 (2004). 53Locke T and Fletcher JT, Incidence of benomyl and iprodione resistance in isolates of Botrytis cinerea in tomato crops in England and Wales in 1986. Plant Pathol 37: 381–384 (1988). 54Burnett FJ, Light leaf spot (Pyrenopeziza brassicae) in oilseed rape: extent of triazole fungicide resistance in Scotland; fungicide strategies, HGCA Project Report Number OS63e. Home Grown Cereals Authority, Kenilworth, UK, 70 pp. (2003). 55Leroux P, Gredt M, Lebrun M-H, and Walker A-S, Resistance to DMI fungicides in French populations of Mycosphaerella graminicola, the causal agent of wheat leaf blotch, 7th International Mycosphaerella and Stagonospora Symposium, Ascona, Switzerland (2008). 56Parnell S, Gilligan CA, Lucas JA, Bock CH and van den Bosch F, Changes in fungicide sensitivity and relative species abundance in Oculimacula yallundae and O. acuformis populations (eyespot disease of cereals) in Western Europe. Plant Pathol 57: 509–517 (2008). 57Steva H, Evaluating anti-resistance strategies for control of Uncinula necator, in Fungicide Resistance. BCPC Monograph Number 60, ed. by S Heaney, D Slawson, DW Hollomon, M Smith, PE Russell and DW Parry. British Crop Protection Council, Farnham, UK, pp. 59–66 (1994). 58Ohl L and Gisi U, Sensitivity of brown and yellow rust populations on wheat to cyproconazole, in Fungicide Resistance. BCPC Monograph Number 60, ed. by S Heaney, D Slawson, DW Hollomon, M Smith, PE Russell and DW Parry. British Crop Protection Council, Farnham, UK, pp. 125–128 (1994). 59Goszczynski W, Cimanowski J and Bachnaki R, First note on the occurrence of a strain of Sphaerotheca mors-uvae Schw.-Berk. with decreased sensitivity to triadimefon. Fruit Science Reports (Skierniewice) 15:181–184 (1988). 60Crute IR, Gordon PL and Moss NA, Variation for response to phenylamides in UK populations of Bremia lactucae (lettuce downy mildew) and Peronospora parasitica (brassica downy mildew), in Fungicide Resistance. BCPC Monograph Number 60, ed. by S Heaney, D Slawson, DW Hollomon, M Smith, PE Russell and DW Parry. British Crop Protection Council, Farnham, UK, pp. 155–162 (1994). 61Pappas AC, Metalaxyl resistance in Phytophthora infestans on greenhouse tomatoes in Greece. Plant Pathol 34: 293–296 (1985). 62Leroux P and Clerjeau M, Resistance of Botrytis cinerea Pers. and Plasmopara viticola (Berk. & Curt.) Berl. and de Toni to fungicides in French vineyards. Crop Protect 4: 137–160 (1985). 63Hollomon DW, Genetic control of ethirimol resistance in a natural population of Erysiphe graminis f.sp. hordei. Phytopathology 71: 536–540 (1981). 64Napier BAS, Bayles RA, Stigwood PL and Burnett FJ, Sensitivity of powdery mildew and yellow rust to DMI, morpholine and strobilurin fungicides in England and Scotland, in The BCPC Conference Pests and Diseases, The British Crop Protection Council, Farnham, UK pp. 427–434 (2000). 65Lucas J, Resistance to Qol fungicides: implications for cereal disease management in Europe. Pestic Outlook 14: 268–270 (2003). 66Lesemann SS, Schimpke S, Dunemann F and Deising HB, Mitochondrial heteroplasmy for the cytochrome b gene controls the level of strobilurin resistance in the apple powdery mildew fungus Podosphaera leucotricha (Ell. & Ev.) E.S. Salmon. J Plant Dis Protect 113: 259–266 (2006). 67Olvang H and Kroeker G, Fungicide resistance. Present situation and strategies in Sweden. Växtskyddsrapporter, Jordbruk 48: 29–35 (1987). 68Hobbelen PHF, Paveley ND, van den Bosch F, Delaying selection for fungicide insensitivity by mixing fungicides at a low and high risk of resistance development a modeling analysis. Phytopathology 101: 1224–1233 (2011). 69 The UK Pesticide Guide 2013, ed. by MA Lainsbury. CAB International, Wallingford, UK and British Crop Production Council, Alton, UK (2013). Citing Literature Volume70, Issue6June 2014Pages 1008-1016 ReferencesRelatedInformation
Referência(s)