Systemic control of nodule formation by the plant N demand requires autoregulation dependent and independent mechanisms

In legumes interacting with rhizobia the formation of symbiotic organs involved in the acquisition of atmospheric nitrogen is depending of the plant nitrogen (N) demand. We used Medicago truncatula plants cultivated in split-root systems to discriminate between responses to local and systemic N signalings. We evidenced a strong control of nodule formation by systemic N-signaling but obtained no clear evidence of a local control by mineral nitrogen. Systemic signaling of the plant N demand controls numerous transcripts involved in the root transcriptome reprogramming associated to early rhizobia interaction and nodule formation. SUNN has an important role in this control but major systemic N signaling responses remained active in the sunn mutant. Genes involved in the activation of nitrogen fixation are regulated by systemic N signaling in the mutant, explaining why the hypernodulation phenotype is not associated to a higher nitrogen fixation of the whole plant. The control of the transcriptome reprogramming of nodule formation by systemic N signaling requires other pathway(s) that parallel the SUNN/CLE pathway.