NRT1.1s in plants: functions beyond nitrate transport

Abstract

Arabidopsis AtNRT1.1 (CHL1/AtNPF6.3) is the first nitrate transporter identified in plants and was initially found to play a role in nitrate uptake and transport. AtNRT1.1 also displays auxin transport activity and mediates nitrate-modulated root development, suggesting that it has transport capacity for multiple substrates. Subsequent work revealed that AtNRT1.1 can respond to environmental nitrate fluctuations by altering its nitrate transport activity, modulated by phosphorylation, leading to the critical finding that AtNRT1.1 acts as a transceptor for nitrate sensing. Recent studies have revealed how OsNRT1.1B, the functional homologue of AtNRT1.1 in rice, mediates nitrate signal transduction from the plasma membrane to the nucleus, and how OsNRT1.1B integrates the nitrate and phosphate signaling networks. OsNRT1.1B has also been shown to be involved in regulating the root microbiota to facilitate organic nitrogen mineralization in soil, thus mediating plant-microbe interactions. Furthermore, the divergent functions of OsNRT1.1A and OsNRT1.1B in regulating nitrogen use in rice suggest that the function of NRT1.1 is still far from fully understood. In this review, we focus on the most recent progress on the molecular mechanisms of NRT1.1s in plants, with the aim of providing an up-to-date view of the versatile functions of NRT1.1 in nitrogen utilization in plants.

Keywords: Arabidopsis; NRT1.1; nitrate transporter; nitrogen use efficiency; rice; signal transduction.

Fig. 1.

Protein sequence analysis of NRT1.1 members in the eudicotyledonous plant Arabidopsis and three monocotyledonous grass species. (A) Phylogeny of NRT1.1 members in Arabidopsis, rice, maize, and sorghum. The phylogenetic tree was constructed by MEGA6 software using the neighbor-joining method with 1000 bootstrap replicates (Tamura et al., 2013). The accession numbers of the NRT1.1 proteins for the different plant species are as follows: AtNRT1.1 (AT1G12110), OsNRT1.1A (LOC_Os08g05910), OsNRT1.1B (LOC_Os10g40600), OsNRT1.1C (LOC_Os03g01290), ZmNRT1.1A (GRMZM2G086496_P01), ZmNRT1.1B (GRMZM2G161459_P02), ZmNRT1.1C (GRMZM2G112154_P01), ZmNRT1.1D (GRMZM2G161483_P01), SbNRT1.1A (Sb07g003690), SbNRT1.1B (Sb01g029470) and SbNRT1.1C (Sb01g050410). At, Arabidopsis thaliana; Os, Oryza sativa; Zm, Zea mays; Sb, Sorghum bicolor. (B) Alignment of conserved amino acid residues in NRT1.1 members in Arabidopsis and rice. T101 is conserved in NRT1.1 proteins in both Arabidopsis and rice, while the nitrate-binding site H356 is absent in OsNRT1.1A and OsNRT1.1C.

Fig. 2.

Integrative model illustrating the roles of NRT1.1s in rice. Plasma membrane-localized OsNRT1.1B (NRT1.1B) functions as a nitrate sensor in response to external nitrate, while tonoplast-localized OsNRT1.1A (NRT1.1A) possibly acts as an intracellular nitrate sensor in the perception of the cell’s nitrogen status. The NRT1.1B–OsSPX4 (SPX4) module is a key node involved in integrating nitrate and phosphate signals in rice. In the presence of nitrate, NRT1.1B senses external nitrate and recruits an E3 ligase, NBIP1, to promote SPX4 ubiquitination and degradation via the 26S proteasome, thereby releasing OsPHR2 and OsNLP3 (NLP3) to concurrently activate downstream phosphate and nitrate responses, respectively. In addition, NRT1.1B can change the rhizosphere microenvironment by modulating root microbes related to nitrogen transformation.