Fungicides are widely used in developed agricultural systems to control disease and safeguard crop yield and quality. Over time, however, resistance to many of the most effective fungicides has emerged and spread in pathogen populations, compromising disease control. This review describes the development of resistance using case histories based on four important diseases of temperate cereal crops: eyespot (Oculimacula yallundae and Oculimacula acuformis), Septoria tritici blotch (Zymoseptoria tritici), powdery mildew (Blumeria graminis), and Fusarium ear blight (a complex of Fusarium and Microdochium spp). The sequential emergence of variant genotypes of these pathogens with reduced sensitivity to the most active single-site fungicides, methyl benzimidazole carbamates, demethylation inhibitors, quinone outside inhibitors, and succinate dehydrogenase inhibitors illustrates an ongoing evolutionary process in response to the introduction and use of different chemical classes. Analysis of the molecular mechanisms and genetic basis of resistance has provided more rapid and precise methods for detecting and monitoring the incidence of resistance in field populations, but when or where resistance will occur remains difficult to predict. The extent to which the predictability of resistance evolution can be improved by laboratory mutagenesis studies and fitness measurements, comparison between pathogens, and reconstruction of evolutionary pathways is discussed. Risk models based on fungal life cycles, fungicide properties, and exposure to the fungicide are now being refined to take account of additional traits associated with the rate of pathogen evolution. Experimental data on the selection of specific mutations or resistant genotypes in pathogen populations in response to fungicide treatments can be used in models evaluating the most effective strategies for reducing or preventing resistance. Resistance management based on robust scientific evidence is vital to prolong the effective life of fungicides and safeguard their future use in crop protection.

The evolution of fungicide resistance.

Surveys of 528 randomly selected commercial fields in England and Wales in 1983 showed that isolates of Pseudocercosporella herpotrichoides resistant to benomyl were common and widespread on winter wheat and winter barley. During June and July resistant strains were recovered from 16 to 66% of fields and the proportion of resistant isolates was 37–52%. The frequency of occurrence of resistant isolates was positively correlated with the number of applications of carbendazimgenerating (MBC) fungicides during the previous 8 years. Benomyl resistance was found in 21–48% of fields where it was claimed that MBC had never been used, and 7–28% of isolates from those fields, were resistant. Resistance was more frequent in R-type than in W-type isolates of the pathogen. The proportion of R-type isolates decreased as the number of previous winter wheat crops rose and increased with the number of winter barley crops grown and with the number of MBC sprays applied to crops in previous years. The implications of these findings for the control of eyespot in England and Wales are discussed.

Survey of benomyl resistance in Pseudocercosporella herpotrichoides on winter wheat and barley in England and Wales in 1983

Eyespot (Pseudocercosporella herpotrichoides) epidemiology in relation to prediction of disease severity and yield loss in winter wheat—a review

Empirical evidence indicates that fungicide-resistant and sensitive strains can coexist for prolonged periods. Coexistence has important practical implications, for example, for the posttreatment recovery of sensitivity and consequently the life expectancy of fungicide products. Despite this, the factors influencing coexistence remain relatively unexplored. Ecological studies have shown that environmental heterogeneity can facilitate the coexistence of different species and subspecific groups. Here we use a simple differential equation model and show that fungicide spray heterogeneity per se is not sufficient for coexistence but that the outcome depends crucially on the competitive relationship between resistant and sensitive strains. The model incorporates the competition between resistant and sensitive pathogen strains for a limited supply of susceptible host tissue on a crop which has received an incomplete coverage of fungicide. We use a combination of invasibility analysis and model simulations to explore the conditions under which coexistence can occur. We further show that the maximum density of healthy host tissue is realized when resistant and sensitive pathogen strains coexist. A set of key influencing parameters are identified and analyzed, and the consequences of the results for disease and resistance management are discussed.

https://apsjournals.apsnet.org/doi/pdf/10.1094/PHYTO-95-0632

Small-scale fungicide spray heterogeneity and the coexistence of resistant and sensitive pathogen strains.

Changing fungicide sensitivities in populations of Oculimacula yallundae and O. acuformis, the species responsible for cereal eyespot in Western Europe, were determined over a 17 year period between 1984 and 2000. The data were collected by Aventis Crop Science as part of their long-term survey to monitor changes in sensitivity to prochloraz and the methyl benzimidazole carbamate (MBC) fungicides in eyespot populations. The results show evidence for reduced sensitivity to both fungicides over the period of the survey. The decline in MBC sensitivity is in agreement with reports of practical resistance (a detectable loss of disease control in the field) to this fungicide which were widely reported from the mid 1980s onward. Prochloraz sensitivity was more complex, with the emergence of a higher resistance category of isolates in the late 1980s and early 1990s which then decreased in frequency towards the end of the survey. This may be partly explained by the introduction and increased use of cyprodinil in the mid 1990s. Although all trends were similar across Europe, differences were observed between the two eyespot species. A higher frequency of O. yallundae isolates showed decreased sensitivity to MBC, whereas decreased sensitivity to prochloraz was at a higher frequency in O. acuformis populations. The relative abundance of the two eyespot species was influenced by their differential levels of fungicide sensitivity, with the ratio increasing toward the species with the highest level of resistance to the prevailing fungicide.

Changes in fungicide sensitivity and relative species abundance in Oculimacula yallundae and O. acuformis populations (eyespot disease of cereals) in Western Europe

Five years' results from a long-term field experiment on carbendazim resistance of Pseudocercosporella herpotrichoides (Fron) Deighton

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Five years' results from a long-term field experiment on carbendazim resistance of Pseudocercosporella herpotrichoides (Fron) Deighton