Systemic control of symbiotic competence through mobile miRNAs

Legume plants balance symbiotic interactions with nitrogen-fixing rhizobial bacteria via a systemic feedback system tightly controlling rates of bacterial infection and nodulation events. This host regulatory system, termed autoregulation of nodulation (AON), prevents nutritional misbalances and is key to maintaining the association at a mutualistic state. We identified a riboregulator, micro RNA miR2111, that undergoes shoot-to-root translocation to control infection (1) through specific post-transcriptional regulation of the Kelch-repeat F-box gene TOO MUCH LOVE (TML), a root-acting repressor of infection and nodulation. Our results reveal miR2111 as a key systemic activator of symbiosis that maintains a susceptible default status in noninfected hosts. Looking beyond symbiotic legumes, we found this regulon to be involved in root system architectural control across plant lineages (2). This suggests that bacterial endosymbiosis recruited functional elements from core developmental processes (2). Excitingly, we identified another miRNA, miRSDI1, as a second mediator of systemic symbiosis control, counteracting the miR2111-TML node and balancing shoot control of root symbiosis to optimize host plant benefits (Fröschel et al., unpublished).

(1) Tsikou et al. (2018) Science 362: 233-236

(2) Sexauer et al. (2023) Nature Comm 14:8083