Nitrogen-Dependent Control of CLE Signaling Pathway and Root System Architecture in Plants

Morphological plasticity of the plant root system architecture is critical for efficient nutrient acquisition. Among the essential elements, nitrogen (N) strongly affects root development. Lateral roots are developed to obtain N in the soil environment, although their growth can be restricted when plants are chronically deprived of N. This mechanism economizes the cost for root development and prevents the risk of extending roots into N-poor environments. A signaling module composed of N-responsive CLE (CLAVATA3/ESR-related) peptides and the CLAVATA1 (CLV1) leucine-rich repeat receptor-like kinase was found to play a crucial role in regulating the expansion of root system in Arabidopsis thaliana under N-deficient conditions. CLE1, 3, 4 and 7 were induced by N deficiency in roots, and their over-expression repressed the emergence of lateral root primordia from the primary root. By contrast, clv1 mutants showed progressive outgrowth of lateral root primordia into lateral roots under N-deficient conditions. When CLE3 was over-expressed in roots under control of CLE3 promoter, the inhibitory effect of CLE3 on lateral root emergence was observed in the wild-type background plants but was abolished in the clv1 mutants. The N-responsive CLEs were predominantly expressed in root pericycle cells, while the receptor CLV1 was present in phloem companion cells, suggesting a systemic mechanism for regulation of the signaling module. The N-responsive CLE-CLV1 signaling module was demonstrated as an essential mechanism regulating the outgrowth of lateral roots in N-deficient environments.