Slow and temperature‐mediated pathogen adaptation to a nonspecific fungicide in agricultural ecosystem

Abstract

The spread of antimicrobial resistance and global change in air temperature represent two major phenomena that are exerting a disastrous impact on natural and social issues but investigation of the interaction between these phenomena in an evolutionary context is limited. In this study, a statistical genetic approach was used to investigate the evolution of antimicrobial resistance in agricultural ecosystem and its association with local air temperature, precipitation, and UV radiation. We found no resistance to mancozeb, a nonspecific fungicide widely used in agriculture for more than half a century, in 215 Alternaria alternata isolates sampled from geographic locations along a climatic gradient and cropping system representing diverse ecotypes in China, consistent with low resistance risk in many nonspecific fungicides. Genetic variance accounts for ~35% of phenotypic variation, while genotype–environment interaction is negligible, suggesting that heritability plays a more important role in the evolution of resistance to mancozeb in plant pathogens than phenotypic plasticity. We also found that tolerance to mancozeb in agricultural ecosystem is under constraining selection and significantly associated with local air temperature, possibly resulting from a pleiotropic effect of resistance with thermal and other ecological adaptations. The implication of these results for fungicide and other antimicrobial management in the context of global warming is discussed.

Temperature-Mediated Plasticity Regulates the Adaptation of Phytophthora infestans to Azoxystrobin Fungicide

“…Our result suggests that elevated air temperature associated with global warming in the future may increase the effectiveness of the fungicide. This result also supports the hypothesis that temperature can regulate both pathogen sensitivity to fungicides and the toxicity of chemical compounds [25,27]. The result further showed that an increase in fungicide doses could leads to a decrease in sensitivity among the pathogens (Figure 4).…”

“…No pairwise correlation between Q ST and F ST across the populations and significantly higher overall Q ST than overall F ST is an indication that evolution of azoxystrobin resistance was under diversifying selection driven by local adaptation. This type of selection can only be possible when some of the phenotypic traits are favored by local environments such as climatic conditions or agricultural practices [58], for example, the density of fungicide application or trade-offs associated with fungicide resistant mutants [27,59]. Previous studies demonstrated that Q ST -F ST comparisons are a powerful approach to infer the importance of diversifying selection in the evolution of quantitative traits [44,60], and revealed that the evolutionary mechanism serves as main driver for the development of fungicide resistance and other ecological traits in pathogen populations including virulence, pesticide resistance, and temperature tolerance in Puccinia striiformis, Mycosphaerella graminicola, P. infestans, and Parastagonospora nodorum, [38,45,61,62].…”

“…Many genetic and environmental factors including chemical property, pathogen biology, fungicide operational scheme, and climatic conditions can affect the types and intensity of natural selection and, therefore, influence the development of fungicide resistance in pathogens [23]. Temperature, a stronghold abiotic environmental factor that influences all biological and biochemical activities of species, could affect the evolution of fungicide resistance in pathogen populations by regulating the generation and maintenance of genetic variation in target genes, metabolic and enzymatic activities of cells, as well as types and intensity of natural selection [24][25][26][27].…”

Rapid adaptation of the Irish potato famine pathogen Phytophthora infestans to changing temperature

“…Arrows represent the transfer of isolates to fresh rye B plates after 10 days (one generation), and orange circles indicate the stages when aggressiveness of acclimated isolates was tested. The acclimation lasted for 20 generations (transfers) with 10 days in each generation as described previously (He et al, 2018;Yang et al, 2016;Zhan & McDonald, 2011). Association between colony size and aggressiveness in both the acclimated and unacclimated parental isolates was evaluated by Pearson's correlation (Lawrence & Lin, 1989).…”

Cross-resistance of the pathogenic fungus Alternaria alternata to fungicides with different modes of action

“…In addition, A. alternata has a broad host range including many grasses. A continuous influx of sensitive isolates from other wild hosts which are usually not exposed to the fungicides is likely to dilute selective pressures and prevent the buildup of resistance level in potato populations of A. alternata [32].…”