A shoot-derived micro RNA orchestrates root organ formation in response to nitrate

Abstract

In a natural soil environment, nitrogen availability is often limiting and not uniformly distributed. To ensure sufficient nitrogen supply, many seed plants adapt their root system architecture in response to nitrogen availability in the substrate, a process known as foraging response. Nitrogen-dependent root system architectural adaptations are shoot dependent and integrate the systemic nitrogen status of the plant. Similarly, the number of root symbiotic nodules in legumes is regulated according to nitrogen availability in a systemic process called Autoregulation of Nodulation (AON). We show that the shoot derived micro RNA miR2111 and its root expressed target TOO MUCH LOVE (TML) regulate both bacterial endosymbiosis and nitrogen-dependent root system adaptation. miR2111 acts as a mobile shoot signal translocating to the root in a nitrogen homeostasis-dependent manner to control lateral root initiation. Intriguingly, this miR2111-TML node is functionally conserved across plant lineages including the asymbiotic ruderal Arabidopsis thaliana and the legume model Lotus japonicus, identifying it as an essential, evolutionarily stable factor facilitating shoot dependent adaptation of root organ formation in response to nitrate availability in plants of divergent lifestyles.