Shoot nitrate underlies a perception of nitrogen satiety to trigger local and systemic signaling cascades in Arabidopsis thaliana

Nitrate is an important ion for plant growth and development. It serves not only as a building block for amino acid synthesis but also as a signaling molecule. Changes in the exogenous nitrate concentrations affect the expression of nitrate-responsive genes within minutes. Following these rapid transcriptional events, nitrate and its downstream organic nitrogen (N) compounds accumulate in the plant body, inducing secondary responses to the internal N level. Nevertheless, the respective roles of nitrate and organic N in triggering plant responses to internal N remain to be clarified. Several studies have implied that internal nitrate levels regulate root N uptake independent of the levels of N assimilation products. However, little is known about the specific effects of internal nitrate levels on plant growth and gene expression. To manipulate the internal nitrate levels independently of internal organic N, we grew wild-type Arabidopsis and a nitrate reductase (NR)-null mutant under a series of modified N conditions. Using their shoots and roots, we performed analyses of plant growth and RNA sequencing. The results showed that elevated shoot nitrate accumulation in the NR-null mutant was accompanied by increased expression of nitrate assimilatory genes in the shoots, decreased gene expression of high-affinity nitrate and ammonium uptake transporters in the roots, and decreased lateral root growth. Furthermore, the genes normally induced by N deficiency were significantly downregulated both in the shoots and roots of the NR-null mutant, compared with the wild-type. Our transcriptional profiling suggests that the transcription factors NLP7 and NIGT mediate a wide range of these transcriptional responses. Taken together, we conclude that shoot nitrate acts as a N satiety signal to trigger local and systemic signaling cascades in A. thaliana. The present study illustrates an adaptive strategy of plants to survive in N-limited environments, depending on the residual nitrate storage.