Upregulated jasmonate signaling shifts Arabidopsis microbiota interactions and stress adaptations through a positive feedback loop.

The model plant Arabidopsis thaliana hosts diverse microbial communities collectively known as the microbiota. The plant microbiota is generally taxonomically structured and, in many cases, confers benefits to the plant host including plant growth promotion and enhanced stress tolerance. However, microbial imbalance can also result in deleterious effects, a phenomenon termed dysbiosis that was first coined in the gut microbiome field. To uncover the regulatory mechanism maintaining healthy plant homeostatic interactions with microbiota, we conducted screening using defined synthetic bacterial communities. We identified an Arabidopsis mutant displaying altered microbial profiles with an overall increase of microbial load and microbiota-dependent growth defects. Transcriptomic analyses combined with phytohormone quantification revealed that these phenotypes are attributed to an upregulation of the jasmonic acid (JA) signaling pathway in this mutant upon microbiota colonization. Furthermore, chemical treatment with different JA inducers reproduced similar phenotypes in wild-type plants, suggesting regulation through a positive feedback loop. Although activation of the JA pathway is typically associated with enhanced plant stress responses, our mutant exhibited reduced pathogen load at the expense of reduced plant growth and impaired salt tolerance. Together, our findings demonstrate that JA signaling not only orchestrates plant growth and defense but also plays a pivotal role in shaping plant-microbiota interactions. Controlled regulation of the JA signaling pathway is therefore essential to maintain balanced plant response to multiple environmental stressors.