Integrating Nitrate and Symbiosis: Evolutionary Rewiring of Conserved Nitrogen-Signalling Modules in Arabidopsis and Medicago

Abstract

Nitrogen is a major limiting nutrient for plant growth and a central driver of fertilizer use in agriculture. In many agricultural soils, nitrate is the main form of available nitrogen, but it is highly mobile and unevenly distributed, forcing plants to continuously adjust root growth to local supply. Legumes add an extra layer of complexity because they can also obtain ammonium through symbiotic nitrogen fixation in root nodules, which are carbon-expensive organs that must be regulated according to both external nitrate levels and internal nitrogen status. This review compares nitrogen signalling in the non-legume Arabidopsis thaliana and the model legume Medicago truncatula. Our aim is to understand how conserved pathways have been rewired to support these different nitrogen acquisition strategies. We focus on three core modules: CLE–CLV1/SUNN signalling, the NIN–NLP transcriptional module and the miR2111–TML pathway. In Arabidopsis, CLE–CLV1 acts mainly as a local low-nitrogen checkpoint that restricts lateral root emergence in nitrate-poor zones, while NLP7 integrates nitrate availability with root architectural responses. In Medicago, orthologous components have been recruited into the autoregulation of nodulation (AON) pathway, where nitrate-induced CLE peptides, NIN–NLP interactions and the systemic miR2111–TML module together integrate nitrate supply and rhizobial infection to coordinate nodulation with whole-plant nitrogen status and carbon cost. Within this network, the CLV1 ortholog SUNN acts as a central integration point. It responds to rhizobia-induced CLE peptides and to nitrogen-dependent systemic signals, including nitrate-induced CLE peptides, that influence lateral root growth in the absence of symbiosis. By contrasting these modules in Arabidopsis and Medicago, we show how legumes have layered symbiotic regulation onto ancestral nitrogen-signalling circuits that were first characterised in non-legume nitrate responses. This evolutionary perspective provides a mechanistic basis for future efforts to improve nitrogen use efficiency in crops by adjusting how CLE signalling, NIN/NLP activity and miR2111–TML-like modules link nitrogen status to root and nodule development.