Fungicides disrupt total and endophytic phyllosphere bacterial communities but a salicylic acid hyperimmune mutant shows microbiome resilience

Abstract Stable colonisation of plants by beneficial microbes enhances disease resistance, nutrient uptake, and stress tolerance. Disruption of these communities often reduces plant fitness. The phyllosphere microbiome is especially vulnerable to agrochemicals. In this study we examined how synthetic fungicides affect the phyllosphere bacterial community of Arabidopsis thaliana. Application of several widely-used fungicides led to a pronounced decrease in bacterial diversity and depletion of beneficial taxa in both surface and internal leaf microbial communities. Moreover, these microbial responses were influenced by the host plant's genetic background. We previously showed that the phyllosphere microbiomes of plants exhibiting heightened salicylic acid-driven immune responses are enriched in xenobiotic degradation traits. We, therefore, examined whether the disrupted phyllosphere of one such line, the fhy3 far1 mutant, is buffered against fungicide-induced dysbiosis. The fhy3 far1 mutant showed reduced fungicide-induced microbiome disruption in both surface and endophytic microbiomes across both systemic and contact fungicides, supporting the hypothesis that innate plant immunity may help buffer against collateral damage from chemical treatments. Our identification of fungicide-resilient microbial taxa holds promise for the development of next-generation biostimulant products and, additionally, our findings raise the possibility that salicylic acid-mediated immunity could be strategically leveraged as a complementary tool alongside traditional fungicides.