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Background Cross-resistance, a phenomenon that a pathogen resists to one antimicrobial compound also resists to one or several other compounds, is one of major threats to human health and sustainable food production. It usually occurs among antimicrobial compounds sharing the mode of action. In this study, we determined the sensitivity profiles of Alternaria alternata, a fungal pathogen which can cause diseases in many crops to two fungicides (mancozeb and difenoconazole) with different mode of action using a large number of isolates (234) collected from seven potato fields across China. Results We found that pathogens could also develop cross resistance to fungicides with different modes of action as indicated by a strong positive correlation between mancozeb and difenoconazole tolerances to A. alternata. We also found a positive association between mancozeb tolerance and aggressiveness of A. alternata, suggesting no fitness penalty of developing mancozeb resistance in the pathogen and hypothesize that mechanisms such as antimicrobial compound efflux and detoxification that limit intercellular accumulation of natural/synthetic chemicals in pathogens might account for the cross-resistance and the positive association between pathogen aggressiveness and mancozeb tolerance. Conclusions The detection of cross-resistance among different classes of fungicides suggests that the mode of action alone may not be an adequate sole criterion to determine what components to use in the mixture and/or rotation of fungicides in agricultural and medical sects. Similarly, the observation of a positive association between the pathogen’s aggressiveness and tolerance to mancozeb suggests that intensive application of site non-specific fungicides might simultaneously lead to reduced fungicide resistance and enhanced ability to cause diseases in pathogen populations, thereby posing a greater threat to agricultural production and human health. In this case, the use of evolutionary principles in closely monitoring populations and the use of appropriate fungicide applications are important for effective use of the fungicides and durable infectious disease management. Electronic supplementary material The online version of this article (10.1186/s12866-019-1574-8) contains supplementary material, which is available to authorized users.

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.

Biodiversity plays multifaceted roles in societal development and ecological sustainability. In agricultural ecosystems, using biodiversity to mitigate plant diseases has received renewed attention in recent years but our knowledge of the best ways of using biodiversity to control plant diseases is still incomplete. In term of in-crop diversification, it is not clear how genetic diversity per se in host populations interacts with identifiable resistance and other functional traits of component genotypes to mitigate disease epidemics and what is the best way of structuring mixture populations. In this study, we created a series of host populations by mixing different numbers of potato varieties showing different late blight resistance levels in different proportions. The amount of naturally occurring late blight disease in the mixture populations was recorded weekly during the potato growing seasons. The percentage of disease reduction (PDR) in the mixture populations was calculated by comparing their observed late blight levels relative to that expected when they were planted in pure stands. We found that PDR in the mixtures increased as the number of varieties and the difference in host resistance (DHR) between the component varieties increased. However, the level of host resistance in the potato varieties had little impact on PDR. In mixtures involving two varieties, the optimum proportion of component varieties for the best PDR depended on their DHR, with an increasing skewness to one of the component varieties as the DHR between the component varieties increased. These results indicate that mixing crop varieties can significantly reduce disease epidemics in the field. To achieve the best disease mitigation, growers should include as many varieties as possible in mixtures or, if only two component mixtures are possible, increase DHR among the component varieties.