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The rising threat of fungicide resistance in plant pathogenic fungi: Botrytis as a case study

Journal of Chemical Biology volume 7, pages 133–141 (2014)Cite this article

Abstract

The introduction of site-specific fungicides almost 50 years ago has revolutionized chemical plant protection, providing highly efficient, low toxicity compounds for control of fungal diseases. However, it was soon discovered that plant pathogenic fungi can adapt to fungicide treatments by mutations leading to resistance and loss of fungicide efficacy. The grey mould fungus Botrytis cinerea, a major cause of pre- and post-harvest losses in fruit and vegetable production, is notorious as a ‘high risk’ organism for rapid resistance development. In this review, the mechanisms and the history of fungicide resistance in Botrytis are outlined. The introduction of new fungicide classes for grey mould control was always followed by the appearance of resistance in field populations. In addition to target site resistance, B. cinerea has also developed a resistance mechanism based on drug efflux transport. Excessive spraying programmes have resulted in the selection of multiresistant strains in several countries, in particular in strawberry fields. The rapid erosion of fungicide activity against these strains represents a major challenge for the future of fungicides against Botrytis. To maintain adequate protection of intensive cultures against grey mould, strict implementation of resistance management measures are required as well as alternative strategies with non-chemical products.

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References

  1. Alekshun MN, Levy SB (2007) Molecular mechanisms of antibacterial multidrug resistance. Cell 128:1037–1050

    Article  CAS  Google Scholar 

  2. Amiri A, Heath SM, Peres NA (2013) Phenotypic characterization of multifungicide resistance in Botrytis cinerea isolates from strawberry fields in Florida. Plant Dis 97:393–401

    Article  Google Scholar 

  3. Amiri A, Heath SM, Peres NA (2014) Resistance to fluopyram, fluxapyroxad, and penthiopyrad in Botrytis cinerea from strawberry. Plant Dis 98:532–539

    Article  CAS  Google Scholar 

  4. Angelini RM, Rotolo C, Masiello M, Gerin D, Pollastro S, Faretra F (2014) Occurrence of fungicide resistance in populations of Botryotinia fuckeliana (Botrytis cinerea) on table grape and strawberry in southern Italy. Pest Manag Sci. doi:10.1002/ps.3711

  5. Avenot H, Simoneau P, Iacomi-Vasilescu B, Bataille-Simoneau N (2005) Characterization of mutations in the two-component histidine kinase gene AbNIK1 from Alternaria brassicicola that confer high dicarboximide and phenylpyrrole resistance. Curr Genet 47:234–243

    Article  CAS  Google Scholar 

  6. Banno S, Fukumori F, Ichiishi A, Okada K, Uekusa H, Kimura M, Fujimura M (2008) Genotyping of benzimidazole-resistant and dicarboximide-resistant mutations in Botrytis cinerea using real-time polymerase chain reaction assays. Phytopathology 98:397–404

    Article  CAS  Google Scholar 

  7. Banno S et al (2009) Characterization of QoI resistance in Botrytis cinerea and identification of two types of mitochondrial cytochrome b gene. Plant Pathol 58:120–129

    Article  CAS  Google Scholar 

  8. Barak E, Edgington LV (1984) Cross-resistance of Botrytis cinerea to captan, thiram, chlorothalonil, and related fungicides. Can J Plant Pathol 6:318–320

    Article  CAS  Google Scholar 

  9. Bardas GA, Myresiotis CK, Karaoglanidis GS (2008) Stability and fitness of anilinopyrimidine-resistant strains of Botrytis cinerea. Phytopathology 98:443–450

    Article  CAS  Google Scholar 

  10. Bardas GA, Veloukas T, Koutita O, Karaoglanidis GS (2010) Multiple resistance of Botrytis cinerea from kiwifruit to SDHIs, QoIs and fungicides of other chemical groups. Pest Manag Sci 66:967–973

    Article  CAS  Google Scholar 

  11. Beever RE (1983) Osmotic sensitivity of fungal variants resistant to dicarboximide fungicides. Trans Br Mycol Soc 80:327–331

    Article  Google Scholar 

  12. Beever RE, Brien HMR (1983) A survey of resistance to the dicarboximide fungicides in Botrytis cinerea. N Z J Agric Res 26:391–400

    Article  CAS  Google Scholar 

  13. Bernard BK, Gordon EB (2000) An evaluation of the common mechanism approach to the Food Quality Protection Act: captan and four related fungicides, a practical example. Int J Toxicol 19:43–61

    Article  CAS  Google Scholar 

  14. Billard A, Fillinger S, Leroux P, Lachaise H, Beffa R, Debieu D (2012) Strong resistance to the fungicide fenhexamid entails a fitness cost in Botrytis cinerea, as shown by comparisons of isogenic strains. Pest Manag Sci 68:684–691

    Article  CAS  Google Scholar 

  15. Bollen GJ, Scholten G (1971) Acquired resistance to benomyl and some other systemic fungicides in a strain of Botrytis cinerea in cyclamen. Neth J Plant Pathol 77:83–90

    Article  CAS  Google Scholar 

  16. Brent KJ, Hollomon DW (1998) Fungicide resistance: the assessment of risk. FRAC Monograph Nr. 2. GCPF, Brussels

    Google Scholar 

  17. Brent KJ, Hollomon DW (1995) Fungicide resistance in crop pathogens: how can it be managed. FRAC Monograph No. 1 (second, revised edition). Fungicide Resistance Action Committee. Monogr. 1 GCPF, FRAC, Brussels, p 1–48

  18. Chapeland F, Fritz R, Lanen C, Gredt M, Leroux P (1999) Inheritance and mechanisms of resistance to anilinopyrimidine fungicides in Botrytis cinerea (Botryotinia fuckeliana). Pestic Biochem Physiol 64:85–100

  19. Cools HJ, Fraaije BA (2008) Are azole fungicides losing ground against Septoria wheat disease? Resistance mechanisms in Mycosphaerella graminicola. Pest Manag Sci 64:681–684

    Article  CAS  Google Scholar 

  20. Dean R et al (2012) The top 10 fungal pathogens in molecular plant pathology. Mol Plant Pathol 13:414–430

    Article  Google Scholar 

  21. Elad Y, Yunis H, Katan T (1992) Multiple fungicide resistance to benzimidazoles, dicarboximides and diethofencarb in field isolates of Botrytis cinerea in Israel. Plant Pathol 41:41–46

    Article  CAS  Google Scholar 

  22. Esterio M, Ramos C, Walker AS, Fillinger S, Leroux P, Auger J (2011) Phenotypic and genetic characterization of Chilean isolates of Botrytis cinerea with different levels of sensitivity to fenhexamid. Phytopathol Mediterr 50:414–420

    CAS  Google Scholar 

  23. Fernandez-Ortuno D, Chen FP, Schnabel G (2013) Resistance to cyprodinil and lack of fludioxonil resistance in Botrytis cinerea isolates from strawberry in North and South Carolina. Plant Dis 97:81–85

    Article  CAS  Google Scholar 

  24. Fillinger S, Ajouz S, Nicot PC, Leroux P, Bardin M (2012) Functional and structural comparison of pyrrolnitrin- and iprodione-induced modifications in the class III histidine-kinase Bos1 of Botrytis cinerea. PLoS One 7:e42520

    Article  CAS  Google Scholar 

  25. Fillinger S, Leroux P, Auclair C, Barreau C, Al HC, Debieu D (2008) Genetic analysis of fenhexamid-resistant field isolates of the phytopathogenic fungus Botrytis cinerea. Antimicrob Agents Chemother 52:3933–3940

    Article  CAS  Google Scholar 

  26. Fournier E, Giraud T (2008) Sympatric genetic differentiation of a generalist pathogenic fungus, Botrytis cinerea, on two different host plants, grapevine and bramble. J Evol Biol 21:122–132

    CAS  Google Scholar 

  27. Fournier E et al (2002) Characterization of nine polymorphic microsatellite loci in the fungus Botrytis cinerea (Ascomycota). Mol Ecol Notes 2:253–255

    Article  CAS  Google Scholar 

  28. Giraud T, Fortini D, Levis C, Lamarque C, Leroux P, LoBuglio K, Brygoo Y (1999) Two sibling species of the Botrytis cinerea complex, transposa and vacuma, are found in sympatry on numerous host plants. Phytopathology 89:967–973

    Article  CAS  Google Scholar 

  29. Grabke A, Fernandez-Ortuno D, Schnabel G (2013) Fenhexamid resistance in Botrytis cinerea from strawberry fields in the Carolinas is associated with four target gene mutations. Plant Dis 97:271–276

    Article  CAS  Google Scholar 

  30. Grasso V, Palermo S, Sierotzki H, Garibaldi A, Gisi U (2006) Cytochrome b gene structure and consequences tor resistance to Qo inhibitor fungicides in plant pathogens. Pest Manag Sci 62:465–472

    Article  CAS  Google Scholar 

  31. Hilber UW, Hilber-Bodmer M (1998) Genetic basis and monitoring of resistance of Botryotinia fuckeliana to anilinopyrimidines. Plant Dis 82:496–500

    Article  CAS  Google Scholar 

  32. Johnson KB, Sawyer TL, Powelson ML (1994) Frequency of benzimidazole-resistant and dicarboximide-resistant strains of Botrytis cinerea in Western Oregon small fruit and snap bean plantings. Plant Dis 78:572–577

    Article  Google Scholar 

  33. Kanetis L, Forster H, Jones CA, Borkovich KA, Adaskaveg JE (2008) Characterization of genetic and biochemical mechanisms of fludioxonil and pyrimethanil resistance in field isolates of Penicillium digitatum. Phytopathology 98:205–214

    Article  CAS  Google Scholar 

  34. Kojima K, Takano Y, Yoshimi A, Tanaka C, Kikuchi T, Okuno T (2004) Fungicide activity through activation of a fungal signalling pathway. Mol Microbiol 53:1785–1796

    Article  CAS  Google Scholar 

  35. Kretschmer M et al (2009) Fungicide-driven evolution and molecular basis of multidrug resistance in field populations of the grey mould fungus Botrytis cinerea. PLoS Pathog 5:e1000696

    Article  Google Scholar 

  36. Lalève A, Gamet S, Walker AS, Debieu D, Toquin V, Fillinger S (2013) Site-directed mutagenesis of the P225, N230 and H272 residues of succinate dehydrogenase subunit B from Botrytis cinerea highlights different roles in enzyme activity and inhibitor binding. Environ Microbiol. doi:10.1111/1462-2920.12282

  37. Leroch M, Kretschmer M, Hahn M (2011) Fungicide resistance phenotypes of Botrytis cinerea isolates from commercial vineyards in South West Germany. J Phytopathol 159:63–65

  38. Leroch M, Plesken C, Weber RW, Kauff F, Scalliet G, Hahn M (2013) Gray mold populations in german strawberry fields are resistant to multiple fungicides and dominated by a novel clade closely related to Botrytis cinerea. Appl Environ Microbiol 79:159–167

    Article  CAS  Google Scholar 

  39. Leroux P, Chapeland F, Desbrosses D, Gredt M (1999) Patterns of cross-resistance to fungicides in Botryotinia fuckeliana (Botrytis cinerea) isolates from French vineyards. Crop Prot 18:687–697

    Article  CAS  Google Scholar 

  40. Leroux P, Clerjeau M (1985) Resistance of Botrytis cinerea Pers. and Plasmopara viticola (Berk. & Curt.) Berl. and de Toni to fungicides in French vineyards. Crop Prot 4:137–160

    Article  CAS  Google Scholar 

  41. Leroux P et al (2002) Mechanisms of resistance to fungicides in field strains of Botrytis cinerea. Pest Manag Sci 58:876–888

    Article  CAS  Google Scholar 

  42. Li X, Fernandez-Ortuno D, Chen S, Grabke A, Luo C-X, Bridges WC, Schnabel G (2014) Location-specific fungicide resistance profiles 1 and evidence for stepwise accumulation of resistance in Botrytis cinerea. Plant Dis. doi:10.1094/PDIS-10-13-1019-RE

  43. Ma ZH, Michailides TJ (2005) Advances in understanding molecular mechanisms of fungicide resistance and molecular detection of resistant genotypes in phytopathogenic fungi. Crop Prot 24:853–863

  44. Mernke D, Dahm S, Walker AS, Lalève A, Fillinger S, Leroch M, Hahn M (2011) Two promoter rearrangements in a drug efflux transporter gene are responsible for the appearance and spread of multidrug resistance phenotype MDR2 in Botrytis cinerea isolates in French and German vineyards. Phytopathology 101:1176–1183

    Article  CAS  Google Scholar 

  45. Morschhauser J (2010) Regulation of multidrug resistance in pathogenic fungi. Fungal Genet Biol 47:94–106

    Article  Google Scholar 

  46. Morton V, Staub T (2008) A short history of fungicides. Online, APSnet Features. doi:10.1094/APSnetFeature2008-0308

  47. Moyano C, Alfonso C, Gallego J, Raposo R, Melgarejo P (2003) Comparison of RAPD and AFLP marker analysis as a means to study the genetic structure of Botrytis cinerea populations. Eur J Plant Pathol 109:515–522

  48. Oshima M et al (2006) Survey of mutations of a histidine kinase gene BcOS1 in dicarboximide-resistant field isolates of Botrytis cinerea. J Gen Plant Pathol 72:65–73

    Article  CAS  Google Scholar 

  49. Pappas AC (1997) Evolution of fungicide resistance in Botrytis cinerea in protected crops in Greece. Crop Prot 16:257–263

    Article  CAS  Google Scholar 

  50. Samuel S, Papayiannis LC, Leroch M, Veloukas T, Hahn M, Karaoglanidis GS (2011) Evaluation of the incidence of the G143A mutation and cytb intron presence in the cytochrome bc-1 gene conferring QoI resistance in Botrytis cinerea populations from several hosts. Pest Manag Sci 67:1029–1036

    Article  CAS  Google Scholar 

  51. Sierotzki H, Scalliet G (2013) A review of current knowledge of resistance aspects for the next-generation succinate dehydrogenase inhibitor fungicides. Phytopathology 103:880–887

    Article  CAS  Google Scholar 

  52. Veloukas T, Kalogeropoulou P, Markoglou AN, Karaoglanidis GS (2014) Fitness and competitive ability of Botrytis cinerea field isolates with dual resistance to SDHI and QoI fungicides, associated with several sdhB and the cytb G143A mutations. Phytopathology 104:347–356

    Article  CAS  Google Scholar 

  53. Veloukas T, Markoglou AN, Karaoglanidis GS (2013) Differential effect of sdhB gene mutations on the sensitivity to SDHI fungicides in Botrytis cinerea. Plant Dis 97:118–122

    Article  CAS  Google Scholar 

  54. Vignutelli A, Hilber-Bodmer M, Hilber UW (2002) Genetic analysis of resistance to the phenylpyrrole fludioxonil and the dicarboximide vinclozolin in Botryotinia fuckeliana (Botrytis cinerea). Mycol Res 106:329–335

    Article  CAS  Google Scholar 

  55. Walker AS, Gautier A, Confais J, Martinho D, Viaud M, Le Pêcheur P, Dupont J, Fournier E (2011) Botrytis pseudocinerea, a new cryptic species causing gray mold in French vineyards in sympatry with Botrytis cinerea. Phytopathology 101:1433–1445

    Article  Google Scholar 

  56. Walker AS, Micoud A, Remuson F, Grosman J, Gredt M, Leroux P (2013) French vineyards provide information that opens ways for effective resistance management of Botrytis cinerea (grey mould). Pest Manag Sci 69:667–678

    Article  CAS  Google Scholar 

  57. Weber RWS (2011) Resistance of Botrytis cinerea to multiple fungicides in Northern German small-fruit production. Plant Dis 95:1263–1269

    Article  CAS  Google Scholar 

  58. Wood PM, Hollomon DW (2003) A critical evaluation of the role of alternative oxidase in the performance of strobilurin and related fungicides acting at the Q(o) site of complex III. Pest Manag Sci 59:499–511

    Article  CAS  Google Scholar 

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Acknowledgments

I am grateful to George Karaoglanidis for the helpful comments to the manuscript, and to him and Roland Weber for sharing unpublished data.

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  1. Department of Biology, University of Kaiserslautern, P.O. box 3049, Kaiserslautern, Germany

    Matthias Hahn

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Hahn, M. The rising threat of fungicide resistance in plant pathogenic fungi: Botrytis as a case study. J Chem Biol 7, 133–141 (2014). https://doi.org/10.1007/s12154-014-0113-1

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