Plants release miRNAs in the rhizosphere, targeting microbial genes

Abstract

Recently, small RNAs have been shown to play important roles in cross-kingdom communication, notably in plant-pathogen relationships. Plant miRNAs were even shown to regulate gene expression in the gut microbiota. But what impact do they have on the plant microbiota? Here we hypothesized that plant miRNAs can be found in the rhizosphere of plants, where they are taken up by rhizosphere bacteria, influencing their gene expression, thereby shaping the rhizosphere bacterial community. We found plant miRNAs in the rhizosphere of Arabidopsis thaliana and Brachypodium distachyon. These plant miRNAs were also found in rhizosphere bacteria, and fluorescent synthetic miRNAs were taken up by cultivated bacteria. A mixture of five plant miRNAs modulated the expression of more than a hundred genes in Variovorax paradoxus, whereas no effect was observed in Bacillus mycoides. Similarly, when V. paradoxus was grown in the rhizosphere of Arabidopsis that overexpressed a miRNA, it changed its gene expression profile. The rhizosphere bacterial communities of Arabidopsis mutants that were impaired in their miRNA or small RNA pathways differed from wildtype plants. Similarly, bacterial communities of Arabidopsis overexpressing specific miRNAs diverged from control plants. Finally, the growth and the abundance of specific ASVs of a simplified soil community were affected by exposure to a mixture of synthetic plant miRNAs. Taken together, our results support a paradigm shift in plant-bacteria interactions in the rhizosphere, adding miRNAs to the plant tools shaping microbial assembly.