Occurrence of Fungicide Resistance in Botrytis cinerea from Greenhouse Tomato in Hubei Province, China

During the early summer of 2012 and 2013, samples of gray mold were collected from greenhouse tomato at eight locations in Hubei Province, and 221 isolates of Botrytis cinerea were obtained and evaluated for the sensitivity to fungicides carbendazim, diethofencarb, boscalid, fludioxonil, and cyprodinil. Results showed that isolates with resistance to carbendazim and cyprodinil were widespread, whereas isolates with resistance to carbendazim and diethofencarb were found at only two locations. No isolates with resistance to boscalid or fludioxonil were detected. Altogether, four resistant phenotypes were determined (i.e., CarRDieSCypS, CarRDieRCypS, CarRDieSCypR, and CarRDieRCypR). Among them, CarRDieSCypS and CarRDieSCypR were widely distributed, and there was a dominant resistant phenotype at each location. Interestingly, isolates resistant only to cyprodinil were not obtained because the resistance to cyprodinil was always associated with the resistance to carbendazim, demonstrating that a phenotype of multiple fungicide resistance of B. cinerea was more likely to have evolved from previously resistant subpopulations. Stability of resistance to carbendazim, diethofencarb, and cyprodinil was assessed, and the resistance was stable. Fitness tests showed that, as a group, the carbendazim-resistant isolates were not significantly different from sensitive isolates. However, the mycelial growth and virulence of the carbendazim, diethofencarb, and cyprodinil triple-resistant group were significantly lower than the sensitive group, indicating that the triple-resistant isolates suffered from the disability of colonizing the hosts. It should be noted that there was no significant difference for other fitness components (e.g., sporulation or osmotic sensitivity to NaCl), suggesting that the triple-resistant isolates were still competitive in these traits. To investigate the mechanisms of resistance to carbendazim and diethofencarb, partial β-tubulin genes of 10 carbendazim-resistant isolates and 5 isolates resistant to carbendazim and diethofencarb were sequenced, and all 10 carbendazim-resistant isolates harbored the mutation E198V or E198A. For the 5 isolates resistant to carbendazim and diethofencarb, all of them possessed the mutation E198K, and no other mutations were detected. The location-specific resistance profiles found in this study are crucial in designing proper gray mold management strategies in these areas.

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Fungicide resistance characterised across seven chemical classes in a Botrytis cinerea population isolated from Australian vineyards

10.1101/2021.03.31.437981 ◽

2021 ◽

Author(s):

Lincoln A. Harper ◽

Scott Paton ◽

Barbara Hall ◽

Suzanne McKay ◽

Richard P. Oliver ◽

...

Keyword(s):

Adverse Effect ◽

Botrytis Cinerea ◽

Fungicide Resistance ◽

Chemical Control ◽

Management Strategies ◽

Resistance Management ◽

Gray Mold ◽

Chemical Groups ◽

Important Disease ◽

Selection Of

AbstractGray mold, caused by Botrytis cinerea, is an economically important disease of grapes in Australia and across grape growing regions worldwide. Control of this disease relies heavily on canopy management and the application of single site fungicides. Fungicide application can lead to the selection of fungicide resistant B. cinerea populations, which has an adverse effect on the chemical control of the disease. Characterising the distribution and severity of resistant B. cinerea populations is needed to inform resistance management strategies. In this study, 725 isolates were sampled from 75 Australian vineyards during 2013 – 2016 and were screened against seven fungicides with different MOAs. The resistance frequencies for azoxystrobin, boscalid, fenhexamid, fludioxonil, iprodione, pyrimethanil and tebuconazole were 5, 2.8, 2.1, 6.2, 11.6, 7.7 and 2.9% respectively. Nearly half of the resistant isolates (43.7%) were resistant to more than one of the fungicides tested. The frequency of vineyards with at least one isolate simultaneously resistant to 1, 2, 3, 4 or 5 fungicides was 19.5, 7.8, 6.5, 10.4 and 2.6%.Resistance was associated with previously published genotypes in CytB (G143A), SdhB (H272R/Y), Erg27 (F412S), Mrr1 (D354Y), Os1 (I365S, N373S + Q369P, I365S + D757N) and Pos5 (P319A, L412F). Expression analysis was used to characterise fludioxonil resistant isolates exhibiting overexpression (6.3 - 9.6-fold) of the ABC transporter encoded by AtrB (MDR1 phenotype). Novel genotypes were also described in Mrr1 (S611N, D616G) and Cyp51 (P357S). Resistance frequencies were lower when compared to most previously published surveys of both grape and non-grape B. cinerea resistance. Nonetheless, continued monitoring of critical chemical groups used in Australian vineyards is recommended.

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Multiple Fungicide Resistance in Botrytis cinerea from Greenhouse Strawberries in Hubei Province, China

Plant Disease ◽

10.1094/pdis-09-16-1227-re ◽

2017 ◽

Vol 101 (4) ◽

pp. 601-606 ◽

Cited By ~ 30

Author(s):

F. Fan ◽

M. S. Hamada ◽

N. Li ◽

G. Q. Li ◽

C. X. Luo

Keyword(s):

Botrytis Cinerea ◽

Management Strategies ◽

Hubei Province ◽

Early Summer ◽

Initial Generation ◽

Succinate Dehydrogenase Subunit B ◽

The Stability ◽

First Time

Two hundred and forty isolates of Botrytis cinerea were collected during the early summer of 2012 and 2013 from strawberry greenhouses in 10 locations in Hubei Province and examined for sensitivity to five fungicides, most of which were commonly used to control this fungus. High frequency of resistance to carbendazim (Car, 63.63%) and cyprodinil (Cyp, 42.42%) was detected. Boscalid-resistant (BosR) isolates were detected for the first time in China, whereas no fludioxonil-resistant isolates were identified. Dual resistance to carbendazim and diethofencarb (Die) was also detected. There were six phenotypes of resistance profile (i.e., CarRDieSBosSCypS, CarRDieRBosSCypS, CarRDieSBosSCypR, CarRDieSBosRCypS, CarRDieRBosSCypR, and CarRDieSBosRCypR). CarRDieSBosSCypS and CarRDieSBosSCypR were the most common phenotypes, occurring at eight and seven locations, respectively. After 10 successive transfers on fungicide-free potato dextrose agar, tested resistant isolates retained levels of resistance similar to or comparative with the initial generation, indicating the stability of these resistances. Fitness evaluations based on investigation of mycelial growth, osmotic sensitivity, sporulation in vitro and in vivo, and virulence revealed the uncompromising fitness in resistant isolates, except that decreased virulence was observed in BosR isolates. The molecular basis of carbendazim, diethofencarb, and boscalid resistance was investigated. Results showed that all 13 sequenced carbendazim-resistant isolates harbored the mutation E198V or E198A in the β-tubulin gene and the five isolates with dual resistance to carbendazim and diethofencarb showed the mutation E198K in the same gene. BosR isolates possessed the H272R mutation in succinate dehydrogenase subunit B gene. The results achieved in this study challenge the current management strategies for B. cinerea, which largely depend on applications of these fungicides.

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Resistance to Pyraclostrobin and Boscalid in Botrytis cinerea Isolates from Strawberry Fields in the Carolinas

Plant Disease ◽

10.1094/pdis-12-11-1049-re ◽

2012 ◽

Vol 96 (8) ◽

pp. 1198-1203 ◽

Cited By ~ 80

Author(s):

Dolores Fernández-Ortuño ◽

Fengping Chen ◽

Guido Schnabel

Keyword(s):

North Carolina ◽

South Carolina ◽

Botrytis Cinerea ◽

Fungicide Resistance ◽

Pathogenic Fungi ◽

Gray Mold ◽

Early Summer ◽

Polymorphism Analysis ◽

Single Spore ◽

Resistant Strains

Botrytis cinerea, the causal agent of gray mold disease, is one of the most important plant-pathogenic fungi affecting strawberry. During the last decade, control of gray mold disease in the southeastern United States has largely been dependent on captan and the use of at-risk fungicides with single-site modes of action, including a combination of the quinone outside inhibitor (QoI) fungicide pyraclostrobin and succinate dehydrogenase inhibitor (SDHI) fungicide boscalid formulated as Pristine 38WG. Reports about loss of efficacy of Pristine in experimental fields in North Carolina prompted us to collect and examine 216 single-spore isolates from 10 conventional fields and 1 organic field in North Carolina and South Carolina in early summer 2011. Sensitivity to pyraclostrobin or boscalid was determined using a conidial germination assay with previously published discriminatory doses. Pyraclostrobin- and pyraclostrobin+boscalid-resistant isolates were found in all conventional fields (with some populations revealing no sensitive isolates) and in the organic field. Among the isolates collected, 66.7% were resistant to pyraclostrobin and 61.5% were resistant to both pyraclostrobin and boscalid. No isolates were identified that were resistant to boscalid but sensitive to pyraclostrobin, indicating that dual resistance may have derived from a QoI-resistant population. The molecular basis of QoI and SDHI fungicide resistance was determined in a subset of isolates. Polymerase chain reaction–restriction fragment length polymorphism analysis of the partial cytochrome b (CYTB) gene showed that pyraclostrobin-resistant isolates possessed the G143A mutation known to confer high levels of QoI fungicide resistance in fungi. Boscalid-resistant isolates revealed point mutations at codon 272 leading to the substitution of histidine to arginine (H272R) or tyrosine (H272Y), affecting the third Fe-S cluster region of the iron-sulfur protein (SdhB) target of SDHIs. The results of the study show that resistance to QoI fungicides and dual resistance to QoI and SDHI fungicides is common in B. cinerea from strawberry fields in the Carolinas. Resistant strains were more frequent in locations heavily sprayed with QoI and SDHI fungicides. However, resistance to both fungicides was also found in the unsprayed, organic field, indicating that some resistant strains may have been introduced from the nursery.

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First Report of Botrytis cinerea Causing Gray Mold Disease on Peach from Pakistan

International Journal of Phytopathology ◽

10.33687/phytopath.007.03.2668 ◽

2018 ◽

Vol 7 (3) ◽

pp. 131-131

Author(s):

Raees Ahmed ◽

Amjad S. Gondal ◽

Muhammad Tariq Khan ◽

Shazia Shahzaman ◽

Sajjad Hyder

Keyword(s):

Botrytis Cinerea ◽

Mycelial Growth ◽

Agar Medium ◽

Management Strategies ◽

Gray Mold ◽

First Report ◽

Average Production ◽

Conducive Environment ◽

Hyphal Tip ◽

Important Disease

Gray mold caused by Botrytis cinerea is an important disease that attacks fruits, leaves and twigs of peach. Peach is grown on an area of 18,008 ha with an average production of 72,085 tons per year in Pakistan (FAO, 2017). During May 2017, brown spots on 33% of the peach fruits examined were observed in Swat district of KPK province of Pakistan. Infected fruits were incubated at 25±2 °C in a humid chamber resulted in greyish mycelial growth with light brown lesions. Hyphal growths on infected fruits were cultured on PDA media and purified by hyphal tip method. Morphologically whitish grey growth was observed on PDA and later on dark sclerotia were observed after 6-7 days of incubation. Hyphae were found septate with branched hyaline conidiophores having a bunch of ovoid conidia at their tips. Further confirmations were done by amplifying internal transcribed spacer regions (Andrew et al., 2009) and glyceraldehyde-3-phosphate dehydrogenase (G3PDH) region of the isolates (Li et al., 2012). Amplicons sequenced from Macrogen Korea were blasted and submitted in NCBI showed that ITS sequences (Accessions MH049690 and MH049691) were 99% identical with already reported (MG878388 and MG654661) sequences and the G3PDH gene sequences (Accessions MH560352 and MH560353) were 99 % identical with already reported (Accessions MG204876) sequences of B. cinerea. Pathogenicity was confirmed on healthy peach fruits disinfected with 50% ethanol, inoculated by placing a plug of about 1cm2 taken from the edge of actively growing B. cinerea isolate (BTS-16). Fruits were incubated at 25±2 °C in a humid chamber (Abata et al., 2016). A set of healthy fruits mock-inoculated with a plug of agar medium were used as control. Three days after inoculation, inoculated fruits showed sunken lesions with cottony greyish mycelial growth on their surface. Fungus isolated from these infections was re-confirmed as B. cinerea. Conducive environment for the disease progression in nearby areas can result into a huge loss in peach produce so there is a need to devise management strategies to cope with the pathogen. This is the first report of gray mold disease of peach caused by B. cinerea from Pakistan.

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Characterization of Botrytis cinerea From Commercial Cut Flower Roses

Plant Disease ◽

10.1094/pdis-09-18-1623-re ◽

2019 ◽

Vol 103 (7) ◽

pp. 1577-1583 ◽

Cited By ~ 7

Author(s):

M. Muñoz ◽

J. E. Faust ◽

G. Schnabel

Keyword(s):

Botrytis Cinerea ◽

Fungicide Resistance ◽

Management Practices ◽

Cultural Practices ◽

Disease Incidence ◽

Resistance Management ◽

Gray Mold ◽

Economic Losses ◽

Cut Flower ◽

Aspergillus Brasiliensis

Botrytis cinerea Pers. infects cut flower roses (Rosa × hybrida L.) during greenhouse production and gray mold symptoms are often expressed in the postharvest environment, resulting in significant economic losses. Disease management is based on cultural practices and preventative chemical treatments; however, gray mold outbreaks continue to occur. Rose tissues from six commercial shipments from two greenhouses in Colombia were evaluated to determine the Botrytis species composition as well as identify other pathogens present, gray mold incidence and severity, and fungicide resistance profiles. Botrytis isolates (49 total) were grouped into six morphological phenotypes, and all were identified to be B. cinerea sensu stricto. Disease incidence was higher in the petals than in the stem, stamen, ovary, sepal, or leaf tissues. Other fungi were isolated infrequently and included Alternaria alternata, Cladosporium cladosporioides, Epicoccum nigrum, Penicillium citrinum, Aspergillus brasiliensis, and Diplodia sp. Fungicide resistance profiles were determined using previously established discriminatory doses. Isolates resistant to thiophanate-methyl, iprodione, boscalid, and cyprodinil were found frequently in all shipments and in both greenhouses. The frequency of resistance to penthiopyrad, fenhexamid, fluopyram, isofetamid, and fludioxonil varied between shipments and greenhouses. No resistance to pydiflumetofen was observed at the discriminatory doses tested. Isolates with resistance to multiple chemical classes were commonly found. These results indicate that fungicide resistance management practices may improve preharvest and postharvest gray mold control of cut flower roses.

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Population Genetics and Fungicide Resistance of Botrytis cinerea on Vitis and Prunus spp. in California

Phytopathology ◽

10.1094/phyto-09-19-0362-r ◽

2020 ◽

Vol 110 (3) ◽

pp. 694-702 ◽

Cited By ~ 2

Author(s):

Jeffery A. DeLong ◽

Seiya Saito ◽

Chang-Lin Xiao ◽

Rachel P. Naegele

Keyword(s):

Botrytis Cinerea ◽

Fungicide Resistance ◽

Gray Mold ◽

Broad Host Range ◽

Multilocus Genotype ◽

Postharvest Diseases ◽

High Genetic Diversity ◽

Action Committee ◽

Vitis Sp ◽

Prunus Spp

Botrytis cinerea, the causal agent of gray mold, has high genetic diversity and a broad host range. In Vitis sp. and Prunus spp., B. cinerea causes pre- and postharvest diseases, and fungicides are routinely applied to prevent yield loss. In total, 535 isolates of B. cinerea collected from Vitis sp. and Prunus spp. in 2012, 2016, and 2017 were genotyped using 18 microsatellite markers and the transposable elements (TEs) Boty and Flipper. Only nine of the polymorphic markers and the two TEs were considered informative and retained for the final analyses. Of the 532 isolates, 297 were tested for resistance to seven fungicides representing six Fungicide Resistance Action Committee classes. After clone correction, 295 multilocus genotype groups were retained across the 3 years in 326 individuals, and four genetic subpopulations were detected. High levels of clonality were observed across the dataset. Significant pairwise differentiation was detected among years, locations, and TE composition. However, most of the diversity observed was within a subpopulation and not among subpopulations. No genetic differentiation was detected among resistant and sensitive isolates for individual fungicide classes. When resistance to the total number of fungicides was compared, regardless of the fungicide class, significant differentiation was detected among isolates that are resistant to two fungicide classes and those resistant to three or four fungicide groups. Fungicide resistance frequencies were stable for most chemistries evaluated with the exception of fluopyram, which increased from 2012 to 2016/2017.

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Gray mold in strawberries in the Paraná state of Brazil is caused by Botrytis cinerea and its isolates exhibit multiple-fungicide resistance

Crop Protection ◽

10.1016/j.cropro.2020.105415 ◽

2021 ◽

Vol 140 ◽

pp. 105415

Author(s):

Juliana Nicolau Maia ◽

Giovana Beger ◽

Wagner Vicente Pereira ◽

Louise Larissa May De Mio ◽

Henrique da Silva Silveira Duarte

Keyword(s):

Botrytis Cinerea ◽

Fungicide Resistance ◽

Gray Mold

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Resistance to Thiophanate-Methyl in Botrytis cinerea Isolates From Californian Vineyards and Pistachio and Pomegranate Orchards

Plant Disease ◽

10.1094/pdis-02-19-0353-re ◽

2020 ◽

Vol 104 (4) ◽

pp. 1069-1075

Author(s):

Hervé F. Avenot ◽

David P. Morgan ◽

Joel Quattrini ◽

Themis J. Michailides

Keyword(s):

Botrytis Cinerea ◽

Mycelial Growth ◽

Gray Mold ◽

Fitness Components ◽

Thiophanate Methyl ◽

Significant Difference ◽

Shoot Blight ◽

Growth Assay ◽

Free Media ◽

Weak Resistance

In this study, a mycelial growth assay was used to evaluate the sensitivity to thiophanate-methyl of 144 Botrytis cinerea isolates (collection A) from Californian vineyards and pistachio and pomegranate orchards. Based on the effective concentration that inhibits 50% of growth (EC50) values for mycelial growth inhibition on fungicide-amended media, 3, 28, 10, and 58% of the isolates showed sensitivity (SS; EC50 < 1 µg/ml), low resistance (LR; 1 < EC50 < 10 µg/ml), weak resistance (WR; 10 < EC50 < 50 µg/ml), and high resistance (HR; EC50 > 100 µg/ml) toward thiophanate-methyl, respectively. The LR and HR phenotypes were observed in pistachio and pomegranate orchards, even though pomegranate was not sprayed with thiophanate-methyl. Sensitivity to thiophanate-methyl of a historical collection of 257 B. cinerea isolates (collection B) isolated from pistachio orchards in 1992, 2005, and 2006 was assessed on potato dextrose agar amended with thiophanate-methyl at the discriminatory concentration of 10 µg/ml. Average percentages of thiophanate-methyl–resistant isolates were 50, 72, and 64% in the orchards in 1992, 2005, and 2006, respectively. A study of fitness components of selected thiophanate-methyl–resistant (LR, WR, and HR) and –sensitive (SS) isolates from collection A did not reveal any significant difference between them with respect to mycelial growth on fungicide-free media and pathogenicity on cultivar Crimson Seedless berries. Comparison of β-tubulin sequences from resistant and sensitive phenotypes revealed that a glutamic acid at position 198 was changed to alanine in all HR isolates and three LR isolates. The occurrence of thiophanate-methyl resistance in B. cinerea populations should be considered when designing spray programs against blossom and shoot blight of pistachio and gray mold of grape.

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Fungicide Resistance Profiling in Botrytis cinerea Populations from Blueberry in California and Washington and Their Impact on Control of Gray Mold

Plant Disease ◽

10.1094/pdis-02-16-0229-re ◽

2016 ◽

Vol 100 (10) ◽

pp. 2087-2093 ◽

Cited By ~ 25

Author(s):

S. Saito ◽

T. J. Michailides ◽

C. L. Xiao

Keyword(s):

Botrytis Cinerea ◽

Fungicide Resistance ◽

Resistance Management ◽

Central Valley ◽

Gray Mold ◽

Postharvest Disease ◽

Quinone Outside Inhibitor ◽

Development Of Resistance ◽

Western Washington ◽

Moderately Resistant

Gray mold caused by Botrytis cinerea is a major postharvest disease of blueberry grown in the Central Valley of California and western Washington State. Sensitivities to boscalid, cyprodinil, fenhexamid, fludioxonil, and pyraclostrobin, representing five different fungicide classes, were examined for 249 (California) and 106 (Washington) B. cinerea isolates recovered from decayed blueberry fruit or flowers. In California and Washington, 7 and 17 fungicide-resistant phenotypes, respectively, were detected: 66 and 49% of the isolates were resistant to boscalid, 20 and 29% were moderately resistant to cyprodinil, 29 and 29% were resistant to fenhexamid, and 66 and 55% were resistant to pyraclostrobin. All isolates from California were sensitive to fludioxonil, whereas 70% of the isolates from Washington showed reduced sensitivity to fludioxonil. In California, 26 and 30% of the isolates were resistant to two and three classes of fungicides, respectively. In Washington, 31, 14, 16, and 9% of the isolates were resistant to two, three, four, and five classes of fungicides, respectively. Inherent risk of the development of resistance to quinone outside inhibitor (QoI) fungicides was assessed by detecting the presence of the Bcbi-143/144 intron in gene cytb. The intron was detected in 11.8 and 40% of the isolates in California and Washington, respectively, suggesting that the risk of QoI resistance is higher in California than in Washington. On detached blueberry fruit inoculated with 11 isolates exhibiting different fungicide-resistant phenotypes, most fungicides failed to control gray mold on fruit inoculated with the respective resistant phenotypes but the mixture of cyprodinil and fludioxonil was effective against all fungicide-resistant phenotypes tested. Our findings would be useful in designing and implementing fungicide resistance management spray programs for control of gray mold in blueberry.

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Resistance to the SDHI Fungicides Boscalid, Fluopyram, Fluxapyroxad, and Penthiopyrad in Botrytis cinerea from Commercial Strawberry Fields in Spain

Plant Disease ◽

10.1094/pdis-01-17-0067-re ◽

2017 ◽

Vol 101 (7) ◽

pp. 1306-1313 ◽

Cited By ~ 23

Author(s):

Dolores Fernández-Ortuño ◽

Alejandro Pérez-García ◽

Manuel Chamorro ◽

Eduardo de la Peña ◽

Antonio de Vicente ◽

...

Keyword(s):

Amino Acid ◽

Botrytis Cinerea ◽

Fungicide Resistance ◽

Mycelial Growth ◽

Growing Season ◽

Gray Mold ◽

Effective Concentration ◽

Site Specific ◽

Resistance Patterns ◽

Succinate Dehydrogenase Inhibitors

Gray mold, caused by the necrotrophic fungus Botrytis cinerea., is one of the most economically important diseases of strawberry. Gray mold control involves the application of fungicides throughout the strawberry growing season; however, B. cinerea isolates resistant to multiple classes of site-specific fungicides have been recently reported in the Spanish gray mold population. Succinate dehydrogenase inhibitors (SDHI) constitute a relatively novel class of fungicides registered for gray mold control representing new alternatives for strawberry growers. In the present study, 37 B. cinerea isolates previously characterized for their sensitivity to boscalid and amino acid changes in the SdhB protein were used to determine the effective concentration that reduces mycelial growth by 50% (EC50) to fluopyram, fluxapyroxad, and penthiopyrad. The present study was also conducted to obtain discriminatory doses to monitor SDHI fungicide resistance in 580 B. cinerea isolates collected from 27 commercial fields in Spain during 2014, 2015, and 2016. The EC50 values ranged from 0.01 to >100 μg/ml for fluopyram, <0.01 to 4.19 μg/ml for fluxapyroxad, and, finally, <0.01 to 59.65 μg/ml for penthiopyrad. Based on these results, as well as findings from a previous publication, the discriminatory doses chosen to examine sensitivities to boscalid, fluopyram, fluxapyroxad, and penthiopyrad were 100, 15, 1, and 6 μg/ml, respectively. Over the course of the 3-year monitoring period, the overall frequencies of resistance to the four SDHI were 56.9, 6.9, 12.9, and 24.6%, respectively. The frequency of boscalid-resistant isolates decreased from 73 to 41% over the years; however, the fluopyram-resistant isolates increased from 5 to 10% after 1 year of registration. Four SDHI resistance patterns were observed in our population, which included patterns I (30%; resistance to boscalid), II (13.8%; resistance to boscalid and penthiopyrad), III (5.7%; boscalid, fluxapyroxad, and penthiopyrad), and IV (7.9%; resistance to boscalid, fluopyram, fluxapyroxad, and penthiopyrad). Patterns I and II were associated with the amino acid substitutions H272R and H272Y; pattern III was associated only with the H272Y mutation; and, finally, pattern IV was associated with the N230I allele in the SdhB subunit. For gray mold management, it is suggested that the simultaneous use of boscalid and penthiopyrad should be limited to one application per season; however, fluxapyroxad and, especially, fluopyram could be used as valid SDHI alternatives for gray mold control, although they should be applied with caution.

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