Nitrate signaling and early responses in Arabidopsis roots

Abstract

Nitrogen (N) is an essential macronutrient that impacts many aspects of plant physiology, growth, and development. Besides its nutritional role, N nutrient and metabolites act as signaling molecules that regulate the expression of a wide range of genes and biological processes. In this review, we describe recent advances in the understanding of components of the nitrate signaling pathway. Recent evidence posits that in one nitrate signaling pathway, nitrate sensed by NRT1.1 activates a phospholipase C activity that is necessary for increased cytosolic calcium levels. The nitrate-elicited calcium increase presumably activates calcium sensors, kinases, or phosphatases, resulting in changes in expression of primary nitrate response genes. Consistent with this model, nitrate treatments elicit proteome-wide changes in phosphorylation patterns in a wide range of proteins, including transporters, metabolic enzymes, kinases, phosphatases, and other regulatory proteins. Identifying and characterizing the function of the different players involved in this and other nitrate signaling pathways and their functional relationships is the next step to understand N responses in plants.

Keywords: Gene expression; nitrate; nitrogen; phospholipase C; phosphorylation; primary response; signaling..

Fig. 1.

Summary of nitrate signaling and assimilation. Nitrate is sensed and transported by the NRT1.1 transceptor, changing its affinity by modifications of phosphorylation status and triggering a signaling pathway. Under low nitrate conditions, CIPK23 phosphorylates NRT1.1, changing it into a high-affinity transporter. Nitrate sensing elicits changes in the phosphorylation status of NRT1.1, and activates, through PLC, calcium influx, which acts as a second messenger (A). This cascade mediates changes in the expression of transcription factors (TGA1/4*) and genes involved in nitrate transport (NRT2.1, NRT2.2 and NRT3.1) and nitrate assimilation (NIA1 and NiR). On the other hand, AFB3 is regulated by nitrate in a PLC- and calcium-independent pathway (B). ABF3 modulates the expression of NAC4 and OBP4, with subsequent effects on root remodeling. Finally, nitrate assimilation (C) produces organic N, which induces miR393 and represses miR167, regulating the abundance of AFB3 and ARF8, respectively. Nitrate-responsive genes are depicted in lilac, transcription factors in purple, and microRNAs in pink. For clarity purposes, the cell nucleus is not shown. *TGA1 and TGA4 are redundant regulatory factors that mediate nitrate responses in Arabidopsis roots. However, the connection between TGA4 and the PLC–calcium pathway has not been experimentally validated. Other relevant transcription factors, such as HRS1 and NLP7, were not included in this figure because their connection with calcium signaling is currently unknown. (This figure is available in colour at JXB online.)