The Compact Root Architecture 2 systemic pathway is required for the induction of cytokinins and of the miR399 in Medicago truncatula N-satisfied plants.

Plants use a combination of sophisticated local and systemic pathways to optimize growth depending on heterogeneous nutrient availability in the soil. Legume plants can acquire mineral nitrogen (N) either through their roots or via a symbiotic interaction with N-fixing rhizobia bacteria housed in so-called root nodules. To identify shoot-to-root systemic signals acting in Medicago truncatula plants at N-deficit or N-satiety, plants were grown in a split-root experimental design, in which either high or low N was provided to a half of the root system, allowing the analysis of systemic pathways independently of any local N response. Among the plant hormone families analyzed, the cytokinin trans-Zeatin accumulated in plants at N-satiety. Cytokinin application by petiole feeding led to an inhibition of both root growth and nodulation. In addition, an exhaustive analysis of miRNAs revealed that miR2111 accumulates systemically under N-deficit in both shoots and non-treated distant roots, whereas a miRNA related to inorganic Phosphate (Pi)-acquisition, the miR399, does so in plants grown at N-satiety. These two accumulation patterns are dependent on CRA2 (Compact Root Architecture 2), a receptor required for CEP (C-terminally Encoded Peptide) signaling. Constitutive ectopic expression of the miR399 reduced nodule numbers and root biomass depending on Pi availability, suggesting that the miR399-dependent Pi-acquisition regulatory module controlled by N-availability affects the development of the whole legume plant root system.

Rhizobium symbiotic efficiency meets CEP signaling peptides.

C-terminally encoded peptides (CEP) signaling peptides are drivers of systemic pathways regulating nitrogen (N) acquisition in different plants, from Arabidopsis to legumes, depending on mineral N availability (e.g. nitrate) and on the whole plant N demand. Recent studies in the Medicago truncatula model legume revealed how root-produced CEP peptides control the root competence for endosymbiosis with N fixing rhizobia soil bacteria through the activity of the Compact Root Architecture 2 (CRA2) CEP receptor in shoots. Among CEP genes, MtCEP7 was shown to be tightly linked to nodulation, and the dynamic temporal regulation of its expression reflects the plant ability to maintain a different symbiotic root competence window depending on the symbiotic efficiency of the rhizobium strain, as well as to reinitiate a new window of root competence for nodulation.