Plant diversity ameliorates the evolutionary development of fungicide resistance in an agricultural ecosystem

1. The evolution of fungicide resistance in agricultural and natural ecosystems is associated with the biology of pathogens, the chemical property and application strategies of the fungicides. The influence of ecological factors such as host diversity on the evolution of fungicide resistance has been largely overlooked but is highly relevant to social and natural sustainability. In this study, we used an experimental evolution approach to understand how host population heterogeneity may affect the evolution of fungicide resistance in the associated pathogens. 2. Potato populations with six levels of genetic heterogeneity were grown in the same field and naturally infected by Phytophthora infestans. Pathogen isolates (similar to 1,200) recovered from the field experiment were molecularly genotyped. Genetically distinct isolates were selected from each population and 142 isolates were assayed for their tolerance to two fungicides differing in the mode of action. Tolerance was determined by calculating the relative growth rate of the isolates in the presence and absence of fungicides and the effective concentration for 50% inhibition. 3. The evolution of fungicide resistance in P. infestans was affected by the genetic variation of host populations. Higher potato diversification increased the sensitivity of P. infestans to both fungicides and reduced genetic variation of the pathogen available for the development of fungicide resistance. These mitigating effects are independent of biochemical properties of fungicides and are likely caused by host selection for pathogen strains differing in the ability of fungicide influxes, effluxes or detoxification rather than mutations in fungicide target genes. 4. Synthesis and applications. The development of fungicide resistance greatly threatens food security and ecological sustainability, and it is urgent need to develop agricultural practices which can ameliorate this problem. Our results show that potato crop with a higher genetic diversity is associated with a late blight pathogen of higher fungicide sensitivity and lower potential of developing fungicide resistance, indicating that agricultural diversification such as through cultivar mixture can reduce the application dose and frequency of fungicides needed to achieve the same level of disease control, which, in turn, further reduce the selection pressure acting on the pathogen populations and the evolutionary risk of developing fungicide resistance in pathogens. Together with benefits documented in other studies, our results indicate that crop diversification is an eco-friendly approach that not only ameliorate fungicide resistance but also help achieve social and ecological sustainability by balancing the interaction among food security, socio-economic development and ecological resilience and should be promoted.

Automated summary

This study shows that genetic diversity of potato populations influences the evolution of fungicide resistance in Phytophthora infestans, resulting in increased sensitivity to fungicides and reduced genetic variation available for developing resistance. These effects are independent of fungicide biochemical properties and are likely due to host selection for pathogen strains with different fungicide responses. Agricultural practices promoting crop diversification can reduce fungicide usage and mitigate the risk of fungicide resistance development in pathogens, contributing to food security and ecological sustainability.