A Widespread Glutamine-Sensing Mechanism in the Plant Kingdom

Abstract

Glutamine is the primary metabolite of nitrogen assimilation from inorganic nitrogen sources in microorganisms and plants. The ability to monitor cellular nitrogen status is pivotal for maintaining metabolic homeostasis and sustaining growth. The present study identifies a glutamine-sensing mechanism common in the entire plant kingdom except Brassicaceae. The plastid-localized PII signaling protein controls, in a glutamine-dependent manner, the key enzyme of the ornithine synthesis pathway, N-acetyl-l-glutamate kinase (NAGK), that leads to arginine and polyamine formation. Crystal structures reveal that the plant-specific C-terminal extension of PII, which we term the Q loop, forms a low-affinity glutamine-binding site. Glutamine binding alters PII conformation, promoting interaction and activation of NAGK. The binding motif is highly conserved in plants except Brassicaceae. A functional Q loop restores glutamine sensing in a recombinant Arabidopsis thaliana PII protein, demonstrating the modular concept of the glutamine-sensing mechanism adopted by PII proteins during the evolution of plant chloroplasts.

The Emergence of 2-Oxoglutarate as a Master Regulator Metabolite

“…A recombinant form of A. thaliana P II containing a functional Q loop from C. reinhardtii exhibited glutamine dependency in the NAGK interaction, confirming that the plant-specific C-terminal extension mediates the glutamine response. These observations suggest that glutamine sensing is a conserved feature of P II signaling in most plant chloroplasts (154).…”

“…Surprisingly, however, a recent study revealed that the structural features of P II proteins from members of the Brassicaceae, such as A. thaliana, are atypical compared with those found in most of the plant kingdom. In contrast to A. thaliana, green plant and algal P II proteins contain a plant-specific C-terminal extension that forms a novel loop in the structure, termed the Q loop, which confers a low-affinity glutamine binding site (154). In vitro studies with Chlamydomonas reinhardtii P II demonstrated that it binds NAGK in a glutamine-dependent manner, in addition to the 2-OG-regulated interaction.…”

Nitrogen Nutrition of Trees in Temperate Forests—The Significance of Nitrogen Availability in the Pedosphere and Atmosphere

“…Provided cycling glutamine constitutes a systemic signal, the down-regulation of nitrate uptake would require homeostasis between the cycling pool of glutamine and the glutamine pool at the site of nitrate uptake as a means to monitor the whole plant N status by the roots. Recently, a cellular mechanism of glutamine-sensing has been identified that seems to be widespread in the plant kingdom [78]. The plastid-localized PII signaling proteins can sense and integrate metabolic signals by conformational changes, thereby exerting control at all levels of metabolic regulation, including transport activity, metabolic reactions and gene expression.…”

Plastidial glycolytic glyceraldehyde-3-phosphate dehydrogenase is an important determinant in the carbon and nitrogen metabolism of heterotrophic cells in Arabidopsis

“…Gln is the primary product of nitrogen assimilation in plants and a central metabolite of nitrogen metabolism. Although as yet unknown, a Gln-sensing mechanism similar to that recently identified in other plant families (Chellamuthu et al, 2014) could play a pivotal role in coordinating nitrogen metabolism in response to the general metabolic state of the cell. In this regard, Gln along with Asn are the main organic nitrogen forms transported between roots and the AP.…”