Abstract
ABSTRACTNitrate 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.
Highlights
Most plants utilize nitrate and ammonium from the soil as their primary sources of nitrogen (N)
Increasing the supply of exogenous nitrate to nitrate-depleted plants transiently changes the expression of nitrate-responsive genes within minutes; this is known as the primary nitrate response (PNR) (Medici and Krouk 2014)
In Arabidopsis thaliana, the PNR is mediated via central regulators, including the plasma membrane transceptor NITRATE TRANSPORTER1.1 (NRT1.1/NPF6.3/ CHL1) (Ho et al 2009), the subgroup III protein kinase CALCIUM SENSOR PROTEIN KINASEs (Liu et al 2017), the transcription factor NIN-LIKE PROTEINs (NLPs) (Castaings et al 2009; Konishi and Yanagisawa 2013; Marchive et al 2013), and the nuclear protein NITRATE REGULATORY GENE2 (NRG2) (Xu et al 2016)
Summary
Most plants utilize nitrate and ammonium from the soil as their primary sources of nitrogen (N). Hu et al (2009) reported that the transcript levels of several nitrateresponsive genes are positively correlated with nitrate concentrations in A. thaliana roots One such gene is the transcriptional repressor NIGT1.4, the translational product of which downregulates the expression of high-affinity N uptake transporters (Medici et al 2015; Kiba et al 2018; Maeda et al 2018). In Nicotiana tabacum plants with various nitrate reductase (NR) activities grown under different N concentrations, the shoot-to-root biomass ratios are positively correlated with foliar nitrate levels (Scheible et al 1997). This is consistent with data from another study on A. thaliana showing that a systemic nitrate signaling pathway represses lateral root growth (Zhang et al 1999). These observations suggest that the Supplemental data for this article can be accessed here
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