Chemical Control of Botrytis and its Resistance to Chemical Fungicides

  • Pierre Leroux

The chemical control of Botrytis spp., and especially B. cinerea the causal agent of grey mould on many crops, can be achieved by several families of fungicides. Among those affecting fungal respiration, the oldest ones are multi-site toxicants (e.g. dichlofluanid, thiram); newer ones are uncouplers (e.g. fluazinam), inhibitors of mitochondrial complex II (e.g. boscalid) or complex III (e.g. strobilurins). Within anti-microtubule botryticides, negative-cross resistance can occur between benzimidazoles (e.g. carbendazim) and phenylcarbamates (e.g. diethofencarb), a phenomenon determined by a mutation in the gene encoding ??-tubulin. Aromatic hydrocarbon fungicides (e.g. dicloran), dicarboximides (e.g. iprodione, procymidone, vinclozolin) and phenylpyrroles (e.g. fludioxonil) affect the fungal content of polyols and resistance to these various compounds can be associated with mutations in a protein histidine kinase, probably involved in osmoregulation. However, dicarboximide-resistant field strains of B. cinerea are sensitive to phenylpyrroles. Anilinopyrimidines (e.g. cyprodinil, mepanipyrim, pyrimethanil) inhibit methionine biosynthesis but their primary target site remains unknown. In few situations, resistance of commercial significance has been recorded. Among sterol biosynthesis inhibitors those inhibiting 14??- demethylase (DMIs) which are widely used against many fungal diseases are of limited interest against Botrytis spp., whereas the hydroxyanilide fenhexamid, which inhibits the 3-keto reductase involved in sterol C4-demethylations, is a powerful botryticide. Monitoring conducted in French vineyards revealed the presence of multi-drug resistant (MDR) strains, a phenomenon probably determined by overproduction of ATP-binding cassette transporters. Resistance towards fungicides of the different groups is described throughout the chapter.


Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

9. References

  1. Albertini C and Leroux P (2004) A Botrytis cinerea putative3-keto reductase gene that is homologous to mammalian 17E-hydroxysteroid dehydrogenase type 7 gene. European Journal of Plant Pathology 110: 723-733Google Scholar
  2. Albertini C, Thébaud C, Fournier E and Leroux P (2003) Eburicol 14D-demethylase gene (CYP51) polymorphism and speciation of Botrytis cinerea. Mycological Research 106: 1171-1178Google Scholar
  3. Anonymous (1988) Fungicide resistance: definitions and use of terms. EPPO Bulletin 18: 569-574Google Scholar
  4. Aravind L and Ponting CP (1999) The cytoplasmic helical linker domain of receptor histidine kinase and methyl-accepting proteins is common to many prokaryotic signalling proteins. FEMS Microbiology Letters 176: 111-116PubMedGoogle Scholar
  5. Balzi E and Goffeau A (1994) Genetics and biochemistry of yeast multidrug resistance. Biochimica et Biophysica Acta 1187: 152-162PubMedGoogle Scholar
  6. Barak E and Edgington LV (1984) Glutathione synthesis in response to captan: a possible mechanism for resistance of Botrytis cinerea to the fungicide. Pesticide Biochemistry and Physiology 21: 412-416Google Scholar
  7. Baroffio CA, Siegfried W and Hilber VW (2003) Long-term monitoring for resistance of Botryotinia fuckeliana to anilinopyrimidine, phenylpyrrole and hydroxyanilide fungicides in Switzerland. Plant Disease 87: 662-666Google Scholar
  8. Bartlett DW, Clough JM, Godwin JR, Hall AA, Hamer M and Parr-Dobrzanski B (2002) The strobilurin fungicides. Pesticide Management Science 58: 659-662CrossRefGoogle Scholar
  9. Birchmore RJ and Forster B (1996) FRAC methods for monitoring the sensitivity of Botrytis cinerea to anilinopyrimidine fungicides. EPPO Bulletin 26: 181-197Google Scholar
  10. Bollen GJ and Scholten G (1971) Acquired resistance to benomyl and some other systemic fungicides in a strain of Botrytis cinerea in cyclamen. Netherlands Journal of Plant Pathology 77: 83-90Google Scholar
  11. Broomfield PLE and Hargreaves J (1992) A single amino-acid change in the iron-sulphur protein subunit of succinate dehydrogenase confers resistance to carboxin in Ustilago maydis. Current Genetic 22: 117-121Google Scholar
  12. Cabral SM and Cabral JP (2000) The primary mode of action of vinclozolin: are oxygen free radicals directly involved? Pesticide Biochemistry and Physiology 66: 145-152Google Scholar
  13. Chapeland F, Fritz R and Leroux P (1999). Inheritance and mechanisms of resistance to anilinopyrimidine fungicides in Botrytis cinerea. Pesticide Biochemistry and Physiology 64: 85- 100Google Scholar
  14. Corbett JR, Wright K and Baillie AC (1984) The Biochemical Mode of Action of Pesticides - 2nd Edition. Academic Press, London, UKGoogle Scholar
  15. Couteux A and Lejeune V (2003) Index phytosanitaire Acta 2003 - 38è edition. ACTA, ParisGoogle Scholar
  16. France Cui W, Beever RE, Parkes SL, Weeds PL and Templeton MD (2002) An osmosensing histidine kinase mediates dicarboximide fungicide resistance in Botryotinia fuckeliana. Fungal Genetics and Biology 36: 187-198Google Scholar
  17. Dacol L, Gibbard M, Hodson MO and Knight S (1998) Azoxystrobin: development on horticultural crops in Europe. Brighton Crop Protection Conference. Pests and Diseases pp. 843-848Google Scholar
  18. Davidse LC and Ishii H (1995) Biochemical and molecular aspects of the mechanisms of action of benzimidazoles, N-phenylcarbamates and N-phenylformamidoximes and the mechanisims of resistance to these compounds in fungi. In: Lyr H (ed.) Modern Selective Fungicides. (pp. 305-322) Gustav Fisher Verlag, Jena, GermanyGoogle Scholar
  19. Debieu D, Bach J, Hugon M, Malosse C and Leroux P (2001) The hydroxyanilide fenhexamid, a new sterol biosynthesis inhibitor fungicide efficient against the plant pathogenic fungus Botryotinia fuckeliana (Botrytis cinerea). Pesticide Management Science 57: 1060-1067Google Scholar
  20. Del Sorbo G (2000) Fungal transporters involved in efflux of natural toxic compounds and fungicides. Fungal Genetics and Biology 30: 1-15PubMedGoogle Scholar
  21. Delen N, Yildiz M and Maraite H (1984) Benzimidazole and dithiocarbamate resistance of Botrytis cinerea on greenhouse crops in Turkey. Medelingen Faculteit Landbouwwetenschappen Rijksuniversiteit Gent 49: 153-161Google Scholar
  22. Delp CJ (1995) Benzimidazole and related fungicides. In: Lyr H (ed.) Modern Selective Fungicides. (pp. 291-303) Gustav Fisher Verlag, Jena, GermanyGoogle Scholar
  23. Edlich W and Lyr H (1992) Target sites of fungicides with primary effects on lipid peroxidation. In: Köller W (ed.) Target Sites of Fungicides Action. (pp. 53-68) CRC Press, Boca Raton, Florida, USAGoogle Scholar
  24. Elad Y (1992) Reduced sensitivity of Botrytis cinerea to two sterol-biosynthesis inhibiting fungicides: fenetrazole and fenethanil. Plant Pathology 41: 47-54Google Scholar
  25. Faretra F and Pollastro S (1991) Genetic basis of resistance to benzimidazole and dicarboximide fungicides in Botryotinia fuckeliana (Botrytis cinerea). Mycological Research 95: 943-951Google Scholar
  26. Faretra F and Pollastro S (1993) Genetics of sexual compatibility and resistance to benzimidazole and dicarboximide fungicides in isolates of Botryotinia fuckeliana from nine countries. Plant Pathology 42: 48-57Google Scholar
  27. Forster B and Staub T (1996) Basis for use strategies of anilinopyrimidine and phenylpyrrole fungicides against Botrytis cinerea. Crop Protection 15: 529-537Google Scholar
  28. Fournier E, Levis C, Fortini D, Leroux P, Giraud T and Brygoo Y (2003) Characterization of Bc-hch, the Botrytis cinerea homolog of the Neurospora crassa het-c vegetative incompatibility locus and its use as a population marker. Mycologia 95: 251-261Google Scholar
  29. Fritz R, Lanen C and Drouhot V (1993) Effects of various inhibitors including carboxin on Botrytis cinerea mitochondria isolated from mycelium. Agronomie 14: 541-554Google Scholar
  30. Fritz R, Lanen C, Chapeland-Leclerc F and Leroux P (2003) Effect of the anilinopyrimidine fungicide pyrimethanil on the cystathionine E-lyase of Botrytis cinerea. Pesticide Biochemistry and Physiology 77: 54-65Google Scholar
  31. Fritz R, Lanen C, Colas V and Leroux P (1997) Inhibition of methionine biosynthesis in Botrytis cinerea by the anilinopyrimidine fungicide pyrimethanil. Pesticide Science 49: 40-46Google Scholar
  32. Fujimura M, Ochiai N, Ichiishi A, Usami R, Horikoshi K and Yamaguchi I (2000a) Sensitivity to phenylpyrrole fungicides and abnormal glycerol accumulation in Os and Cut mutant strains of Neurospora crassa. Japan Pesticide Science 25: 31-36Google Scholar
  33. Fujimura M, Ochiai N, Ichiishi A, Usami R, Horikoshi K and Yamaguchi I (2000b) Fungicide resistance and osmotic stress sensitivity in Os mutants of Neurospora crassa. Pesticide Biochemistry and Physiology 67: 125-133Google Scholar
  34. Fujimura M, Ochiai N, Oshima M, Motoyama T, Ichiishi A, Usami R, Horikoshi K and Yamaguchi I (2003) Putative homologs of SSK22 MAPKK kinase and PBS2 MAPK kinase of Saccharomyces cerevisiae encoded by os-4 and os-5 genes for osmotic sensitivity and fungicide resistance in Neurospora crassa. Bioscience Biotechnology and Biochemistry 67: 186-191Google Scholar
  35. Giraud T, Fortini D, Levis C, Lamarque C, Leroux P, Lobuglio K and Brygoo Y (1999) Two sibling species of the Botrytis cinerea complex transposa and vacuma are found in sympatry on numerous host plants. Phytopathology 89: 967-973PubMedGoogle Scholar
  36. Gisi U, Sierotzki H, Cook A and McCaffery A (2002) Mechanisms influencing the evolution of resistance to Qo inhibitor fungicides. Pest Management Science 58: 859-867PubMedGoogle Scholar
  37. Gouot JM (1988) Characteristics and population dynamics of Botrytis cinerea and other pathogen resistant to dicarboximide. In: Delp CJ (ed.) Fungicide Resistance in North America. (pp. 53-57) American Phytopathological Society Press, St. Paul, Minnesota, USAGoogle Scholar
  38. Griffiths RG, Dancer J, O’Neill E and Harwood JL (2003) Lipid composition of Botrytis cinerea and inhibition of its radiolabelling by the fungicide iprodione. New Phytologist 160: 199-207Google Scholar
  39. Gullino ML and Garibaldi A (1982) Use of mixtures or alternation of fungicides with the aim of reducing the risk of appearance of strains of Botrytis cinerea resistant to dicarboximides. EPPO Bulletin 12: 151-156Google Scholar
  40. Gullino ML and Kuijpers LAM (1994) Social and political implications of managing plant diseases with restricted fungicides in Europe. Annual Review of Phytopathology 32: 559-579PubMedGoogle Scholar
  41. Hayashi K, Schoonbeek HJ, Sugiura H and De Waard MA (2001) Multidrug resistance in Botrytis cinerea with decreased accumulation of the azole fungicide oxoconazole and increased transcription of the ABC transporter gene BcatrD. Pesticide Biochemistry and Physiology 70: 168-179Google Scholar
  42. Hayashi K, Schoonbeek HJ, Sugiura H and De Waard MA (2002a) Expression of the ABC transporter BcatrD from Botrytis cinerea reduces sensitivity to sterol demethylation inhibitors. Pesticide Biochemistry and Physiology 73: 110-121Google Scholar
  43. Hayashi K, Schoonbeek HJ, Sugiura H and De Waard MA (2002b) Bcmfs1 a novel major facilitor superfamily transporter from Botrytis cinerea provides tolerance towards the natural toxic compounds camptothecin and cercosporin and towards fungicides. Applied and Environmental Microbiology 68: 4996-5004Google Scholar
  44. Hilber VW and Hilber-Bodmer M (1998) Genetic basis and monitoring of resistance of Botryotinia fuckeliana to anilinopyrimidines. Plant Disease 82: 496-500Google Scholar
  45. Kalamarakis AE, Petsikos-Paragiotarou N, Mavroides B and Ziogas BN (2000) Activity of fluazinam against strains of Botrytis cinerea resistant to benzimidazoles and/or dicarboximides and to a benzimidazole-phenylcarbamate mixture. Journal of Phytopathology 148: 449-455Google Scholar
  46. Katan T (1982) Resistance to 3,5-dichlorophenyl-N-cyclicimide (dicarboximide) fungicides in the grey mould pathogen Botrytis cinerea on protected crops. Plant Pathology 31: 133-141Google Scholar
  47. Katan T and Ovadia S (1985) Effect of chlorothalonil on resistance of Botrytis cinerea to dicarboximides in cucumber glasshouses. EPPO Bulletin 15: 365-369Google Scholar
  48. Katan T, Elad Y and Yunis H (1989) Resistance to diethofencarb (NPC) in benomyl-resistant field isolates of Botrytis cinerea. Plant Pathology 38: 86-92Google Scholar
  49. Koenraadt H and Jones AL (1992) The use of allele-specific oligonucleotide probes to characterize resistance to benomyl in field strains of Venturia inaequalis. Phytopathology 82: 1354-1358Google Scholar
  50. Kulka M and von Schmeling B (1995) Carboxin fungicides and related compounds. In: Lyr H (ed.) Modern Selective Fungicides. (pp. 133-147) Gustav Fisher Verlag, Jena, GermanyGoogle Scholar
  51. Latorre BA, Spadaro I and Rioja ME (2002) Occurrence of resistant strains of Botrytis cinerea to aminopyrimidine fungicides in table grapes in Chile. Crop Protection 21: 957-961Google Scholar
  52. Leroux P (1994) Influence du pH, d’acides aminés et de diverses substances organiques sur la fongitoxicité du pyriméthanil, du glufosinate, du captafol, du cymoxanil et du fenpiclonil vis-à-vis de certaines souches de Botrytis cinerea. Agronomie 14: 541-554Google Scholar
  53. Leroux P (1995) Progress and problems in the control of Botrytis cinerea in grapevine. Pesticide Outlook, October 1995, pp. 13-19Google Scholar
  54. Leroux P (1996) Recent developments in the mode of action of fungicides. Pesticide Science 47: 191-197Google Scholar
  55. Leroux P and Clerjeau M (1985) Resistance of Botrytis cinerea and Plasmopara viticola to fungicides in French vineyards. Crop Protection 4: 137-160Google Scholar
  56. Leroux P and Fritz R (1984) Antifungal activity of dicarboximides and aromatic hydrocarbons and resistance to these fungicides. In: Trinci APJ and Ryley JF (eds) Mode of Action of Antifungal Agents. (pp. 207-237) Cambridge University Press, Cambridge, UKGoogle Scholar
  57. Leroux P, Chapeland F, Desbrosses D and Gredt M (1999) Patterns of cross-resistance to fungicides in Botryotinia fuckeliana (Botrytis cinerea) isolates from French vineyards. Crop Protection 18: 687-697Google Scholar
  58. Leroux P, Fournier E, Brygoo Y and Panon ML (2002b) Biodiversité et variabilité chez Botrytis cinerea, l’agent de la pourriture grise. Phytoma 554: 38-42Google Scholar
  59. Leroux P, Fritz R and Despreaux D (1987) The mode of action of cymoxanil in Botrytis cinerea. In Greenhalgh R and Roberts TR (eds) Pesticide Science and Biotechnology.(pp.191-196) Blackwell Scientific Publications, Oxford, UKGoogle Scholar
  60. Leroux P, Fritz R, Debieu D, Albertini C, Lanen C, Bach J, Gredt M and Chapeland F (2002a) Mechanisms of resistance to fungicides in field strains of Botrytis cinerea. Pest Management Science 58: 876-888Google Scholar
  61. Leroux P, Gredt M, Arnold A and Bernard T (1997) Etude de la sensibilité de Botrytis cinerea, l'agent de la pourriture grise, vis à vis du fluazinam. In: 5th International Conference on Plant Diseases ANPP, Paris, France, pp. 501-507Google Scholar
  62. Leroux P, Lanen C and Fritz R (1992) Similarities in the antifungal activities of fenpiclonil, iprodione and tolclofos-methyl against Botrytis cinerea and Fusarium nivale. Pesticide Science 36: 325-329Google Scholar
  63. Leroux P, Walker AS and Senechal Y (2003) Etude de la sensibilité de Botrytis cinerea au boscalid. In: 7th International Conference on Plant Diseases(cdROM; AFPP, Paris, France
  64. Lorbeer JW and Vincelli PC (1990) Efficacy of dicarboximide fungicides and fungicide combinations for control of Botrytis leaf blight of union in New York. Plant Disease 74: 235-237Google Scholar
  65. Lorenz G (1988) Dicarboximide fungicides: history of resistance development and monitoring methods. In Delp CJ (ed.) Fungicide Resistance in North America. (pp. 45-51). American Phytopathological Society Press, St. Paul, Minnesota, USAGoogle Scholar
  66. Lorenz G, Becker R and Schelberger K (1994) Strategies to control dicarboximide-resistant Botrytis strains in grapes. In Heaney S, Slawson D, Hollomon DW, Smith M, Russel PE and Parry DW (eds) Fungicide Resistance. (pp. 225-232) BCPC monograph 60, British Crop Protection Council, Farnham, UKGoogle Scholar
  67. Luck JE and Gillings MR (1995) Rapid identification of benomyl resistant strains of Botrytis cinerea using the polymerase chain reaction. Mycological Research 99: 1483-1488Google Scholar
  68. Malathrakis NE (1989) Resistance of Botrytis cinerea to dichlofluanid in greenhouse vegetables. Plant Disease 73: 138-141Google Scholar
  69. Masner P, Muster P and Schmid J (1994) Possible methionine biosynthesis inhibition by pyrimidinamine fungicides in Botrytis cinerea. Pesticide Science 42: 163-166Google Scholar
  70. Miller T, Renault S and Selitrennikoff CP (2002) Molecular dissection of alleles of the osmotic-1 locus of Neurospora crassa. Fungal Genetics and Biology 35: 147-155PubMedGoogle Scholar
  71. Milling RJ and Richardson CJ (1995). Mode of action of the anilinopyrimidine fungicide pyrimethanil. Effects on enzyme excretion in Botrytis cinerea. Pesticide Science 45: 43-48Google Scholar
  72. Miura I, Kamakura T, Maeno S, Hayashi S and Yamaguchi I (1994) Inhibition of enzyme secretion in plant pathogens by mepanipyrim, a novel fungicide. Pesticide Biochemistry and Physiology 48: 222-228Google Scholar
  73. Nakajima M, Suzuki J, Hosaka T, Hibi T and Akutsu K (2001) Functional analysis of an ATP-binding cassette transporter gene in Botrytis cinerea by gene disruption. Journal of General Plant Pathology 67: 212-214Google Scholar
  74. Nakazawa Y and Yamada M (1997) Chemical control of grey mould in Japan. A history of combating resistance. Agrochemicals Japan 71: 2-6Google Scholar
  75. Ochiai N, Fujimura M, Motoyama J, Ichiishi A, Usami R, Horikoshi K and Yamaguchi I (2001) Characterization of mutations in the two-component histidine kinase gene that confer fludioxonil resistance and osmotic sensitivity in the os-1 mutants of Neurospora crassa. Pesticide Management Science 57: 437-442Google Scholar
  76. Oshima M, Fujimura M, Bannos S, Hashimoto C, Motoyama T, Ichiishi A and Yagamushi I (2002) A point mutation in the two component histidine kinase BcoS-1 gene confers dicarboximide resistance in field isolates of Botrytis cinerea. Phytopathology 92: 75-80PubMedGoogle Scholar
  77. Pak HA, Beever RE and Laracy EP (1990) Population dynamics of dicarboximide-resistant strains of Botrytis cinerea on grapevine in New Zealand. Plant Pathology 39: 501-509Google Scholar
  78. Palmer CL, Horst KF and Langbans RW (1997) Use of bicarbonates to inhibit in vitro colony growth of Botrytis cinerea. Plant Disease 81: 1432-1438Google Scholar
  79. Petsikos-Panayotarou N, Markellou E and Kalamarakis AE (2003) In vitro and in vivo activity of cyprodinil and pyrimethanil on Botrytis cinerea resistant to other botryticides and selection of resistance to pyrimethanil in a greenhouse population in Greece. European Journal of Plant Pathology 109: 173-182Google Scholar
  80. Pillonel C and Meyer T (1997) Effect of phenylpyrroles on glycerol accumulation and protein kinase activity of Neurospora crassa. Pesticide Science 49: 229-236Google Scholar
  81. Pollastro S, Faretra F, Di Canio V and De Guido A (1996) Characterization and genetic analysis of field isolates of Botryotinia fuckeliana (Botrytis cinerea) resistant to dichlofluanid. European Journal of Plant Pathology 102: 607-613Google Scholar
  82. Pommer EH and Lorenz G (1995) Dicarboximide fungicides. In: Lyr H (ed.) Modern Selective Fungicides - 2nd Edition. (pp. 99-118).Gustav Fisher Verlag, Jena, GermanyGoogle Scholar
  83. Prins TW, Wagemakers L, Schouten A and Van Kan JAL (2000) Cloning and characterization of a glutathione s-transferase homologue from the plant pathogenic fungus Botrytis cinerea. Molecular Plant Pathology 1: 169-178PubMedGoogle Scholar
  84. Radice S, Ferraris M, Marabini L, Grand S and Chiesara E (2001) Effect of iprodione, a dicarboximide fungicide, on primary cultured rainbow trout hepatocytes. Aquatic Toxicology 54: 51-58PubMedGoogle Scholar
  85. Ramesh MA, Laidlaw RD, Dürrenberger F, Orth AB and Kronstad W. (2001) The cAMP signal transduction pathway mediates resistance to dicarboximides and aromatic hydrocarbon fungicides in Ustilago maydis. Fungal Genetics and Biology 32: 183-193PubMedGoogle Scholar
  86. Raposo R, Gomez V, Urrutia T and Melgarejo P (2000) Fitness of Botrytis cinerea associated with dicarboximide resistance. Phytopathology 90: 1246-1249PubMedGoogle Scholar
  87. Rewal N, Coley-Smith JR and Sealy-Lewis HM (1991) Studies on resistance to dichlofluanid and other fungicides in Botrytis cinerea. Plant Pathology 40: 554-560Google Scholar
  88. Roberts TR, Hutson DH, Jewess PJ, Lec PW, Nicholls PH and Plimmer JR (1999) Metabolic Pathways of Agrochemicals - Part 2: Insecticides and Fungicides. Royal Society of Chemistry, Cambridge, UKGoogle Scholar
  89. Rosslenbroich H-J and Stuebler D (2000) Botrytis cinerea - history of chemical control and novel fungicides for its management. Crop Protection 19: 557-561Google Scholar
  90. Schoonbeek H, Del Sorbo G and De Waard MA (2001) The ABC transporter BcatrB affects the sensitivity of Botrytis cinerea to the phytoalexin resveratrol and the fungicide fenpiclonil. Molecular Plant-Microbe Interactions 14: 562-571PubMedGoogle Scholar
  91. Shtienberg D and Elad Y (1997) Incorporation of weather forecasting in integrated, biological-chemical management of Botrytis cinerea. Phytopathology 87: 332-340PubMedGoogle Scholar
  92. Sierotzki H and Gisi U (2003) Molecular diagnostics for fungicide resistance in plant pathogens. In: Voss G and Ramos G (eds) Chemistry of Crop Protection. (pp. 71-88) Wiley-VCH, Weinheim, GermanyGoogle Scholar
  93. Sierotzki H, Wullschleger J, Alt M, Bruyère T, Pillonel C, Parisi S and Gisi U (2002) Potential mode of resistance to anilinopyrimidine fungicides. In: Dehne HW, Gisi U, Juck KH, Russel PE and Lyr H (eds) Modern Fungicides and Antifungal Compounds III. (pp. 141-148) Agro Concept GmbH, Bonn, GermanyGoogle Scholar
  94. Slawecki RA, Ryan EP and Young DH (2002) Novel fungitoxic assays for inhibition of germination associated adhesion of Botrytis cinerea and Puccinia recondita spores. Applied and Environmental Microbiology 68: 597-601PubMedGoogle Scholar
  95. Smith CM (1988) History of benzimidazole use and resistance. In: Delp CJ (ed.) Fungicide Resistance in North America. (pp. 23-24) American Phytopathological Society Press, St. Paul, Minnesota, USAGoogle Scholar
  96. Stehmann C (1995) Biological activity of triazole fungicides towards Botrytis cinerea. Ph.D. Thesis, University of Wageningen, The NetherlandsGoogle Scholar
  97. Stergiopoulos I, Suviers LH and De Waard MA (2002) Secretion of natural and synthetic toxic compounds from filamentous fungi by membrane transporters of the ATP-binding cassette and major facilitor superfamily. European Journal of Plant Pathology 108: 719-734Google Scholar
  98. Suty A, Pontzen R and Stenzel K (1999) Fenhexamid-sensitivity of Botrytis cinerea: determination of baseline sensitivity and assessment of the risk of resistance. Pflanzenschutz-Nachrichten Bayer 52: 145-157Google Scholar
  99. Tamura O (2000) Resistance development of grey mould on beans towards fluazinam and relevant countermeasures. In: Abstract of the 10th Symposium of Research Committee of Fungicides Resistance, The Phytopathological Society of Japan, April 5, 2000, Okayama, Japan, pp. 7-16Google Scholar
  100. Tamura H, Mizutani A, Yukioka H, Miki N, Ohba K and Masuko M (1999) Effect of the methoxyiminoacetamide fungicide, SSF 129, on respiratory activity in Botrytis cinerea. Pesticide Science 55: 681-686Google Scholar
  101. Tellier F, Fritz R, Leroux P, Carlin-Sinclair A and Cherton JC (2002) Metabolism of cymoxanil and analogs in strains of the fungus Botrytis cinerea using high-performance liquid chromatography and ion-pair high performance thin layer chromatography. Journal of Chromatography B 769: 35-46Google Scholar
  102. Terada M, Mizuhashi F, Tomita T and Murata K (1998) Effects of mepanipyrim on lipid metabolism in rats. The Journal of Toxicological Sciences 23: 235-241PubMedGoogle Scholar
  103. Terry LA and Joyce DC (2000) Suppression of grey mould on strawberry fruit with chemical plant activator acibenzolar. Pesticide Management Science 56: 989-992Google Scholar
  104. Tremblay DM, Talbot BG and Carisse O (2003) Sensitivity of Botrytis squamosa to different classes of fungicides. Plant Disease 87: 573-578Google Scholar
  105. Vermeulen T, Schoonbeek H and De Waard M (2001) The ABC transporter BcatrB from Botrytis cinerea is a determinant of the activity of the phenylpyrrole fungicide fludioxonil. Pesticide Management Science 57: 393-402Google Scholar
  106. Vignutelli A, Hilber-Bodmer M and Hilber UW (2002) Genetic analysis of resistance to the phenylpyrrole fludioxonil and the dicarboximide vinclozolin in Botryotinia fuckeliana. Mycological Research 106: 329-335Google Scholar
  107. White GA and Georgopoulos SG (1992) Target sites of carboxamides. In: Köller W (ed.) Target Sites of Fungicide Action. (pp. 1-29) CRC Press, Boca Raton, USAGoogle Scholar
  108. Wood PM and Hollomon DH (2003) A critical evaluation of the role of alternative oxidase in the performance of strobilurin and related fungicides acting at the Qo site of complex III. Pest Management Science 59: 499-511PubMedGoogle Scholar
  109. Wurms KV, Long PG, Sharrock KR and Greenwood DR (1999) The potential for resistance to Botrytis cinerea by kiwifruit. Crop Protection 18: 427-435Google Scholar
  110. Yarden O and Katan T (1993) Mutations leading to substitutions at amino-acids 198 and 200 of beta-tubulin that correlate with benomyl-resistance phenotypes of field strains of Botrytis cinerea. Phytopathology 83: 1478-1483Google Scholar
  111. Yoder OC and Turgeon BG (2001) Fungal genomics and Pathology. Current Opinion in Plant Biology 4: 315-321PubMedGoogle Scholar
  112. Yourman LF, Jeffers SN and Den RA (2001) Phenotype instability in Botrytis cinerea in the absence of benzimidazole and dicarboximide fungicides. Phytopathology 91: 307-315PubMedGoogle Scholar
  113. Yunis H, Elad Y and Mahrer Y (1991) Influence of fungicide control of cucumber and tomato grey mould (Botrytis cinerea) on fruit yield. Pesticide Science 31: 325-335Google Scholar
  114. Zhang Y, Lamm R, Pillonel C, Lam S and Xu JR (2002) Osmoregulation and fungicide resistance: the Neurospora crassa Os-2 gene encodes a HOG1 mitogen-activated protein kinase homologue. Applied and Environmental Microbiology 68: 532-538PubMedGoogle Scholar

Copyright information

© Springer 2007

Authors and Affiliations

  • Pierre Leroux
    • 1
  1. 1.INRA, Unité de Phytopharmacie et Médiateurs ChimiquesFrance

Personalised recommendations