Co-option of a conserved lateral-root development program by symbiotic signals.

Abstract

Nod factors (NFs) are microbial signals originally identified for their key role in the nitrogen-fixing root nodule symbiosis in legumes. Beyond symbiosis, NFs also possess a conserved capacity to induce lateral-root formation across diverse plant species, including non-legumes. It is now well established that the nodule organogenesis program has co-opted several molecular mechanisms involved in root development, which raises the question of the developmental pathway controlled by NFs to trigger lateral-root formation and how it overlaps with nodule organogenesis in legumes. In Medicago truncatula, NF stimulation of lateral-root formation is independent of the cytokinin receptor CYTOKININ RESPONSE 1 (CRE1), a negative regulator of lateral-root formation. Here, we show that this stimulation is also independent of the NODULE INCEPTION (NIN) transcription factor, a major regulator of nodule organogenesis acting downstream of cytokinin perception. Instead, NFs stimulate lateral-root formation by influencing auxin biosynthesis and modulating auxin signaling, notably through Auxin/INDOLE-3-ACETIC ACID 7 (Aux/IAA7) in M. truncatula. Using reverse genetics and cross-species complementation, we show that orthologs of MtIAA7, AtIAA29 in Arabidopsis thaliana and SlIAA29 in tomato share a conserved role in lateral-root formation. MtIAA7 also interacts with AUXIN RESPONSE FACTOR (ARF) orthologs of AtARF7 and AtARF19, which are known to control lateral-root formation in Arabidopsis. Altogether, our findings show that NFs control a true lateral-root formation pathway, independent of the nodule organogenesis pathway in M. truncatula, by acting through a conserved auxin signaling module.