Herbicide residues in soil decrease microbe-mediated plant protection

The residues of glyphosate are found to remain in soils longer than previously reported, affecting rhizosphere microbes. This may adversely affect crop and other non-target plants because the plant's resilience and resistance largely rely on plant-associated microbes. Ubiquitous glyphosate residues in soil and how they impact mutualistic microbes inhabiting the aboveground plant parts are largely unexplored. We studied the effects of herbicide residues in soil on Epichloë sp., which are common endophytic symbionts inhabiting aerial parts of cool-season grasses. In this symbiosis, the obligate symbiont subsists entirely on its host plant, and in exchange, it provides alkaloids conferring resistance to herbivores for the host grass that invests little in its own chemical defence. We first show decreased growth of Epichloë endophytes in vitro when directly exposed to two concentrations of glyphosate or glyphosate-based herbicides. Second, we provide evidence for a reduction of Epichloë-derived, insect-toxic loline alkaloids in endophyte-symbiotic meadow fescue (F. pratensis) plants growing in soil with a glyphosate history. Plants were grown for 2 years in an open field site, and natural herbivore infestation was correlated with the glyphosate-mediated reduction of loline alkaloid concentrations. Our findings indicate that herbicides residing in soil not only affect rhizosphere microbiota but also aerial plant endophyte functionality, which emphasizes the destructive effects of glyphosate on plant symbiotic microbes, here with cascading effects on plant-pest insect interactions.