A guanosine tetraphosphate (ppGpp) mediated brake on photosynthesis is required for acclimation to nitrogen limitation in Arabidopsis

Abstract

Guanosine pentaphosphate and tetraphosphate (together referred to as ppGpp) are hyperphosphorylated nucleotides found in bacteria and the chloroplasts of plants and algae. In plants and algae artificial ppGpp accumulation can inhibit chloroplast gene expression, and influence photosynthesis, nutrient remobilisation, growth, and immunity. However, it is so far unknown whether ppGpp is required for abiotic stress acclimation in plants. Here, we demonstrate that ppGpp biosynthesis is necessary for acclimation to nitrogen starvation in Arabidopsis. We show that ppGpp is required for remodeling the photosynthetic electron transport chain to downregulate photosynthetic activity and for protection against oxidative stress. Furthermore, we demonstrate that ppGpp is required for coupling chloroplastic and nuclear gene expression during nitrogen starvation. Altogether, our work indicates that ppGpp is a pivotal regulator of chloroplast activity for stress acclimation in plants.

Retrograde and anterograde signaling in the crosstalk between chloroplast and nucleus

“…In plants subjected to nitrogen limitation the chloroplast with its photosynthetic machinery represents a major potential nitrogen source for metabolic remobilization. Under these conditions ppGpp was indeed induced and shown to be important for remodeling the photosynthetic electron transport chain, thereby down-regulating photosynthetic activity and providing protection against oxidative stress and cell damage (Romand et al, 2022). Moreover ppGpp was shown to promote the coordinated down-regulation of both chloroplast and nuclear genes of chloroplast proteins and thus to couple chloroplast and nuclear gene expression during nitrogen starvation (Romand et al, 2022).…”

“…Under these conditions ppGpp was indeed induced and shown to be important for remodeling the photosynthetic electron transport chain, thereby down-regulating photosynthetic activity and providing protection against oxidative stress and cell damage (Romand et al, 2022). Moreover ppGpp was shown to promote the coordinated down-regulation of both chloroplast and nuclear genes of chloroplast proteins and thus to couple chloroplast and nuclear gene expression during nitrogen starvation (Romand et al, 2022). Thus ppGpp appears to be a key regulator of chloroplast activity with a photoprotective role for the adaptation of plants to environmental stress conditions.…”

Relative flux trade-offs and optimization of metabolic network functionalities

“…Comparison of the reactions in relative trade-offs with respect to growth based on the metabolic network of A. thaliana ( Table S13 ) with published phenotypes on growth indicated that: (1) guanylate kinase 3, chloroplastic is required for optimal growth [32] and is also required for acclimation to nitrogen limitations [33] , (2) overexpression of the genes encoding nucleoside diphosphate kinase leads to enhanced growth in poplar [34] and alfalfa [35] , overexpression of the bifunctional dihydrofolate reductase-thymidylate synthase 1 leads to delayed development, without differences in biomass and rosette size at the compared times with wild-type, suggesting larger final biomass [36] . These findings demonstrate that the predictions of the approach for Arabidopsis are partly in line with the existing experimental evidence.…”

Coordination of Chloroplast Activity with Plant Growth: Clues Point to TOR

“…Thus, although ppGpp is only metabolized in the chloroplast, both the synthetases and hydrolases that allow fine control of ppGpp homeostasis must be imported [ 57 , 58 ]. This is particularly important under stress conditions, such as nitrogen deprivation or virus infection, where ppGpp accumulation plays an important role [ 59 , 60 , 61 ].…”