A Central Role for the Nitrate Transporter NRT2.1 in the Integrated Morphological and Physiological Responses of the Root System to Nitrogen Limitation in Arabidopsis

Abstract

Up-regulation of the high-affinity transport system (HATS) for NO3− and stimulation of lateral root (LR) growth are two important adaptive responses of the root system to nitrogen limitation. Up-regulation of the NO3− HATS by nitrogen starvation is suppressed in the atnrt2.1-1 mutant of Arabidopsis (Arabidopsis thaliana), deleted for both NRT2.1 and NRT2.2 nitrate transporter genes. We then used this mutant to determine whether lack of HATS stimulation affected the response of the root system architecture (RSA) to low NO3− availability. In Wassilewskija (Ws) wild-type plants, transfer from high to low NO3− medium resulted in contrasting responses of RSA, depending on the level of nitrogen limitation. Moderate nitrogen limitation (transfer from 10 mm to 1 or 0.5 mm NO3−) mostly led to an increase in the number of visible laterals, while severe nitrogen stress (transfer from 10 mm to 0.1 or 0.05 mm NO3−) promoted mean LR length. The RSA response of the atnrt2.1-1 mutant to low NO3− was markedly different. After transfer from 10 to 0.5 mm NO3−, the stimulated appearance of LRs was abolished in atnrt2.1-1 plants, whereas the increase in mean LR length was much more pronounced than in Ws. These modifications of RSA mimicked those of Ws plants subjected to severe nitrogen stress and could be fully explained by the lowered NO3− uptake measured in the mutant. This suggests that the uptake rate of NO3−, rather than its external concentration, is the key factor triggering the observed changes in RSA. However, the mutation of NRT2.1 was also found to inhibit initiation of LR primordia in plants subjected to nitrogen limitation independently of the rate of NO3− uptake by the whole root system and even of the presence of added NO3− in the external medium. This indicates a direct stimulatory role for NRT2.1 in this particular step of LR development. Thus, it is concluded that NRT2.1 has a key dual function in coordinating root development with external NO3− availability, both indirectly through its role as a major NO3− uptake system that determines the nitrogen uptake-dependent RSA responses, and directly through a specific action on LR initiation under nitrogen-limited conditions.

Earthworms influence the production of above- and belowground biomass and the expression of genes involved in cell proliferation and stress responses in Arabidopsis thaliana

“…In addition, earthworm-induced high nitrate concentrations were probably responsible for the significant reduction in the number of fine roots observed in the poor soil plants, as was previously reported (Zhang and Forde, 2000;Remans et al, 2006). Since decaying earthworms were not a possible source of additional N (worms survival rates were 100%), the majority of the extra N was probably formed through mineralization of soil organic matter by gut-associated and cast-associated micro-organisms, in accordance with Brown's hypothesis that earthworms mostly increase plant growth through N mineralization .…”

“…Compared to those growing in the rich soil, the plants cultivated in the poor soil without earthworms showed phenotypic and developmental responses typical of mineral -particularly nitrogen (N)-deficiency: early reproductive switch, smaller shoot to root ratio, as a result of a higher allocation of assimilates to the roots and severely reduced seed yield (Eaton, 1935;Scheible et al, 1997;Hirai et al, 2004;Hermans et al, 2006;Mantelin et al, 2006;Remans et al, 2006). The almost complete depletion of the initial NO 3 À content in the poor soil by the end of the experiment support the hypothesis of N-starvation.…”

Nitrogen use efficiency in rapeseed. A review

“…More recently, the N-responsive CLAVATA3/ESR (CLE) peptides and the CLAVATA1 (CLV1) leucine-rich repeat receptor-like kinase signaling module were identified as playing a crucial role in the development of the lateral root system in N-poor environments (Araya et al 2013). Additionally, the nitrate transporters NRT1.1 (Remans et al 2006a;Krouk et al 2010) and NRT2.1 (Little et al 2005;Remans et al 2006b) are known to be crucial in nitrate sensing, independent of their uptake function (Malamy and Ryan 2001;Miller et al 2007). Our studies indicate that different winter rapeseed varieties show different reactions to low and high nitrogen concentrations (Fig.…”

Chitinase-Like Protein CTL1 Plays a Role in Altering Root System Architecture in Response to Multiple Environmental Conditions

“…NRT2.1 seems to be directly involved in the regulation of LR initiation when nitrate is limiting and Suc is abundant. It has also been reported that the dual-affinity nitrate transporter NRT1.1 acts upstream of ANR1 in mediating the stimulatory effect of a localized nitrate supply on LR proliferation (Liu et al, 1999;Remans et al, 2006).…”