Occurrence of fungicide resistance in populations of Botryotinia fuckeliana (Botrytis cinerea) on table grape and strawberry in southern Italy.

BACKGROUND Botryotinia fuckeliana (Botrytis cinerea) is a pathogen with a high risk of development of resistance to fungicides. Fungicide resistance was monitored during 2008-2011 in B. fuckeliana populations from both table-grape vineyards and greenhouse-grown strawberries in southern Italy. RESULTS Isolates showing different levels of resistance to anilinopyrimidines (APs) were detected at high frequency (up to 98%) in fields treated intensively with APs (4-7 sprays season(-1) ). A slight decrease in sensitivity to fludioxonil, always combined with AP resistance, was generally found at lower frequencies. The repeated use of fenhexamid on grapevine (3-8 sprays season(-1) ) led to a strong selection of highly resistant isolates (up to 100%). Boscalid-resistant mutants were detected at very variable frequencies (0-73%). Occurrence of resistance to quinone outside inhibitors (QoIs) was also ascertained. Multiple fungicide resistance to 2-6 different modes of action were frequently recovered. Single nucleotide polymorphisms (SNPs) in the target genes Erg27, SdhB and cytb were associated with resistance to fenehexamid, boscalid and QoIs respectively. CONCLUSION Resistance to the fungicides commonly used against grey mould on table grape and strawberry is quite common in southern Italy. This is an outcome of the incorrect use of fungicides, often because of the maximum number of detectable residues of plant protection products imposed by big international retailers, and underlines the crucial role of antiresistance strategies in integrated pest management.

[1]  F. Faretra,et al.  Molecular characterisation and detection of resistance to succinate dehydrogenase inhibitor fungicides in Botryotinia fuckeliana (Botrytis cinerea). , 2014, Pest management science.

[2]  G. Schnabel,et al.  Fenhexamid Resistance in Botrytis cinerea from Strawberry Fields in the Carolinas Is Associated with Four Target Gene Mutations. , 2013, Plant disease.

[3]  G. Schnabel,et al.  Resistance to Cyprodinil and Lack of Fludioxonil Resistance in Botrytis cinerea Isolates from Strawberry in North and South Carolina. , 2013, Plant disease.

[4]  B. Latorre,et al.  Prevalence of isolates of Botrytis cinerea resistant to multiple fungicides in Chilean vineyards , 2012 .

[5]  H. Ishii,et al.  Genetic analysis and molecular characterisation of laboratory and field mutants of Botryotinia fuckeliana (Botrytis cinerea) resistant to QoI fungicides. , 2012, Pest management science.

[6]  N. Zapata,et al.  Isolation and Selection of Epiphytic Yeast for Biocontrol of Botrytis cinerea Pers. on Table Grapes , 2012 .

[7]  G. Schnabel,et al.  Resistance to Pyraclostrobin and Boscalid in Botrytis cinerea Isolates from Strawberry Fields in the Carolinas. , 2012, Plant disease.

[8]  M. Combina,et al.  Biocontrol of Botrytis cinerea in table grapes by non-pathogenic indigenous Saccharomyces cerevisiae yeasts isolated from viticultural environments in Argentina , 2012 .

[9]  F. Faretra,et al.  Genetics of fungicide resistance in Botryotinia fuckeliana (Botrytis cinerea). , 2012 .

[10]  M. Hahn,et al.  Detection and Molecular Characterization of Boscalid-Resistant Botrytis cinerea Isolates from Strawberry. , 2011, Plant disease.

[11]  R. Weber.  Resistance of Botrytis cinerea to Multiple Fungicides in Northern German Small-Fruit Production. , 2011, Plant disease.

[12]  L. Papayiannis,et al.  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. , 2011, Pest management science.

[13]  C. Xiao,et al.  Molecular characterization of boscalid resistance in field isolates of Botrytis cinerea from apple. , 2011, Phytopathology.

[14]  J. Usall,et al.  Field applications of improved formulations of Candida sake CPA-1 for control of Botrytis cinerea in grapes , 2011 .

[15]  I. Barchia,et al.  First report of anilinopyrimidine-resistant phenotypes in Botrytis cinerea on grapevines in Australia , 2002, Australasian Plant Pathology.

[16]  A. Markoglou,et al.  Molecular characterization of benzimidazole-resistant B. cinerea field isolates with reduced or enhanced sensitivity to zoxamide and diethofencarb , 2011 .

[17]  M. Hahn,et al.  Fungicide Resistance Phenotypes of Botrytis cinerea Isolates from Commercial Vineyards in South West Germany , 2011 .

[18]  Y. Elad,et al.  Screening of Botrytis cinerea isolates from vineyards in Israel for resistance to fungicides , 2011, European Journal of Plant Pathology.

[19]  G. Bardas,et al.  Multiple resistance of Botrytis cinerea from kiwifruit to SDHIs, QoIs and fungicides of other chemical groups. , 2010, Pest management science.

[20]  N. Čadež,et al.  Biocontrol of Grey Mould Disease on Grape Caused by Botrytis cinerea with Autochthonous Wine Yeasts , 2010 .

[21]  M. Leroch,et al.  Exploring Mechanisms of Resistance to Respiratory Inhibitors in Field Strains of Botrytis cinerea, the Causal Agent of Gray Mold , 2010, Applied and Environmental Microbiology.

[22]  R. Weber.  Occurrence of Hyd R3 fenhexamid resistance among Botrytis isolates in Northern German soft fruit production , 2010 .

[23]  T. Michailides,et al.  Progress in understanding molecular mechanisms and evolution of resistance to succinate dehydrogenase inhibiting (SDHI) fungicides in phytopathogenic fungi , 2010 .

[24]  F. Faretra,et al.  Selection, characterization and genetic analysis of laboratory mutants of Botryotinia fuckeliana (Botrytis cinerea) resistant to the fungicide boscalid , 2010, European Journal of Plant Pathology.

[25]  Ming-guo Zhou,et al.  Multiple Resistance of Botrytis cinerea from Vegetable Crops to Carbendazim, Diethofencarb, Procymidone, and Pyrimethanil in China. , 2010, Plant disease.

[26]  J. Mercier,et al.  Fungicide resistance among Botrytis cinerea isolates from California strawberry fields. , 2010 .

[27]  G. Zhu,et al.  Detection and characterization of benzimidazole resistance of Botrytis cinerea in greenhouse vegetables , 2010, European Journal of Plant Pathology.

[28]  Wen-Hsin Chung,et al.  Characterisation of QoI-resistant field isolates of Botrytis cinerea from citrus and strawberry. , 2009, Pest management science.

[29]  M. Kimura,et al.  Characterization of QoI resistance in Botrytis cinerea and identification of two types of mitochondrial cytochrome b gene , 2009 .

[30]  T. Michailides,et al.  Molecular characterization of field azoxystrobin-resistant isolates of Botrytis cinerea , 2009 .

[31]  S. Topolovec-Pintarić.  Resistance risk to new botryticides in Botrytis cinerea Pers.:Fr. in winegrowing areas in Croatia , 2009 .

[32]  M. Hahn,et al.  Fungicide resistance and genetic diversity of Botrytis cinerea isolates from a vineyard in Germany , 2008 .

[33]  C. Myresiotis,et al.  Baseline Sensitivity of Botrytis cinerea to Pyraclostrobin and Boscalid and Control of Anilinopyrimidine- and Benzimidazole-Resistant Strains by These Fungicides. , 2008, Plant disease.

[34]  S. Fillinger,et al.  Genetic Analysis of Fenhexamid-Resistant Field Isolates of the Phytopathogenic Fungus Botrytis cinerea , 2008, Antimicrobial Agents and Chemotherapy.

[35]  A. de Vicente,et al.  Mechanisms of resistance to QoI fungicides in phytopathogenic fungi. , 2008, International microbiology : the official journal of the Spanish Society for Microbiology.

[36]  P. E. Russell,et al.  Studies on the biological performance of boscalid and its mode of action. , 2008 .

[37]  M. Gullino,et al.  Resistance of Botrytis cinerea to fungicides in Italian vineyards. , 2008, Communications in agricultural and applied biological sciences.

[38]  M. Esterio,et al.  First Report of Fenhexamid Resistant Isolates of Botrytis cinerea on Grapevine in Chile. , 2007, Plant disease.

[39]  G. Karaoglanidis,et al.  Resistance of Botrytis cinerea Isolates from Vegetable Crops to Anilinopyrimidine, Phenylpyrrole, Hydroxyanilide, Benzimidazole, and Dicarboximide Fungicides. , 2007, Plant disease.

[40]  P. Leroux.  Chemical Control of Botrytis and its Resistance to Chemical Fungicides , 2007 .

[41]  S. Pollastro,et al.  Characterization and genetic analysis of field isolates ofBotryotinia fuckeliana (Botrytis cinerea) resistant to dichlofluanid , 1996, European Journal of Plant Pathology.

[42]  P. Melgarejo,et al.  Resistance to Pyrimethanil and other Fungicides in Botrytis cinerea Populations Collected on Vegetable Crops in Spain , 2004 .

[43]  P. Leroux,et al.  A Botrytis cinerea Putative 3-keto Reductase Gene (ERG27) that is Homologous to the Mammalian 17β-Hydroxysteroid Dehydrogenase type 7 gene (17β-HSD7) , 2004, European Journal of Plant Pathology.

[44]  U. Hilber,et al.  Long-Term Monitoring for Resistance of Botryotinia fuckeliana to Anilinopyrimidine, Phenylpyrrole, and Hydroxyanilide Fungicides in Switzerland. , 2003, Plant disease.

[45]  B. Latorre,et al.  Occurrence of resistant strains of Botrytis cinerea to anilinopyrimidine fungicides in table grapes in Chile , 2002 .

[46]  R. Beever,et al.  An osmosensing histidine kinase mediates dicarboximide fungicide resistance in Botryotinia fuckeliana (Botrytis cinerea). , 2002, Fungal genetics and biology : FG & B.

[47]  I. Yamaguchi,et al.  A Point Mutation in the Two-Component Histidine Kinase BcOS-1 Gene Confers Dicarboximide Resistance in Field Isolates of Botrytis cinerea. , 2002, Phytopathology.

[48]  M. Gullino,et al.  Sensitivity to Anilinopyrimidines and Phenylpyrroles in "Botrytis cinerea" in North-Italian Vineyards. , 2000 .

[49]  P. Leroux,et al.  Inheritance and Mechanisms of Resistance to Anilinopyrimidine Fungicides in Botrytis Cinerea (Botryotinia Fuckeliana) , 1999 .

[50]  L. Yourman,et al.  Resistance to Benzimidazole and Dicarboximide Fungicides in Greenhouse Isolates of Botrytis cinerea. , 1999, Plant disease.

[51]  J. LaMondia,et al.  Sensitivity of Botrytis cinerea from Connecticut Greenhouses to Benzimidazole and Dicarboximide Fungicides. , 1997, Plant disease.

[52]  F. Faretra,et al.  Isolation, characterization and genetic analysis of laboratory mutants of Botryotinia fuckeliana resistant to the phenylpyrrole fungicide CGA 173506. , 1993 .

[53]  F. Faretra,et al.  Genetics of sexual compatibility and resistance to benzimidazole and dicarboximide fungicides in isolates of Botryotinia fuckeliana (Botrytis cinerea) from nine countries , 1993 .

[54]  O. Yarden.  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 , 1993 .

[55]  F. Faretra,et al.  Genetic basis of resistance to benzimidazole and dicarboximide fungicides in Botryotinia fuckeliana (Botrytis cinerea) , 1991 .

[56]  R. Beever,et al.  Strains of Botrytis cinerea resistant to dicarboximide and benzimidazole fungicides in New Zealand vineyards , 1989 .

[57]  S. Pollastro,et al.  New natural variants of Botryotinia fuckeliana (Botrytis cinerea) coupling benzimidazole-resistance to insensitivity toward the N-phenylcarbamate diethofencarb. , 1989 .

[58]  P. Leroux,et al.  Resistance of Botrytis cinerea Pers. and Plasmopara viticola (Berk. & Curt.) Berl. and de Toni to fungicides in French vineyards , 1985 .

[59]  J. F. Ryley,et al.  Mode of action of antifungal agents , 1984 .

[60]  R. Beever,et al.  A survey of resistance to the dicarboximide fungicides in Botrytis cinerea , 1983 .

[61]  K. Sanderson,et al.  HETEROKARYOSIS AND PARASEXUALITY IN THE FUNGUS ASCOCHYTA IMPERFECTA. , 1965, American journal of botany.