Benzoxazinoid-mediated microbiome feedbacks enhance Arabidopsis growth and defence

Summary Plants modulate their surrounding microbiome via root exudates and such conditioned soil microbiomes feed back on the performance of the next generation of plants. How plants perceive altered soil microbiomes and modulate their performance in response to such microbiome feedbacks however remains largely unknown. As tool to condition contrasting microbiomes in soil, we made use of two maize lines, which differ in their ability to exude benzoxazinoids. Based on these differentially conditioned soil microbiomes we have established a model system with Arabidopsis thaliana (Arabidopsis) to investigate the mechanisms of microbiome feedbacks. Arabidopsis plants responding to the benzoxazinoid-conditioned soil microbiome grew better and were developmentally more advanced. Further, these plants harboured differential root bacterial communities, showed enhanced defence signatures in transcriptomes of their shoots and they were more resistant to the fungal pathogen Botrytis cinerea . Intriguingly, Arabidopsis responded with both improved growth and enhanced defence to the benzoxazinoid-conditioned soil microbiome, and we found that this simultaneous increase of growth and defence was mediated by priming of the defences. Further advancing our basic understanding how plants respond to soil microbiomes and mediate their feedbacks is particularly important for the goal to improve crops so they can benefit from their soil microbiome.