Rhizospheric miRNAs affect the plant microbiota

Abstract

MicroRNAs (miRNAs) are small non-coding RNAs that control target gene expression, through sequence complementarity. Their roles in plants vary from regulating developmental processes to responding to abiotic and biotic stresses. 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. Thus, we hypothesised that the same process happens in the rhizosphere which contributes to shaping plant microbial communities. To explore these questions, we performed small RNA sequencing in search of miRNAs in the rhizosphere of evolutionarily distant plants, Arabidopsis thaliana and Brachypodium distachyon. This revealed the presence of specific and shared rhizospheric plant miRNAs, which were all absent in unplanted soils. A subset of these miRNAs were also detected inside rhizospheric bacteria, but were missing in bacteria from unplanted soils, suggesting bacterial uptake of surrounding plant miRNAs. Furthermore, an in silico analysis indicated potential targets of these rhizospheric miRNAs in plant-associated bacterial genomes. To examine the function of these miRNAs, A. thaliana mutants, affected in their miRNA and/or siRNA (small interfering RNA) biosynthesis, were grown. Their rhizospheric microbial communities were significantly disrupted in comparison with wild-type plants. This work makes an important contribution to the field of rhizospheric plant-microbe interactions and offers some significant insights into the potential of plant miRNAs for microbiota engineering.

Extracellular RNA: mechanisms of secretion and potential functions

“…A more recent preprint provides further support for this hypothesis, reporting that Arabidopsis secretes sRNAs into the rhizosphere that were then taken up by root-associated bacteria ( Middleton et al , 2022 , Preprint). That this could have functional consequences was supported by the finding that Arabidopsis mutants deficient in sRNA biogenesis were found to have dramatically altered root microbiomes.…”

A journey into the world of small RNAs in the arbuscular mycorrhizal symbiosis

“…Investigations with computational, cellular, molecular and genetic tools should clarify the functional role of the plethora of plant sRNAs which are differentially expressed in the host plants during the AM symbiosis. Do they have a biological function at local (root) level, likely in the presymbiotic dialogue (Middleton et al ., 2023) or during fungal accommodation and the activation of metabolic pathways involved in nutrient exchanges? Are they mobile molecules that travel toward epigean organs and are involved in the systemic effect?…”