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 remobilization, 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.
Highlights
Plants cannot escape harsh environmental fluctuations, and so their survival hinges on facing each threat
We found that ppGpp biosynthesis by RSH2 and RSH3 is 94 necessary for acclimation to nitrogen starvation in Arabidopsis
Under nitrogen-deprivation conditions strong autoluminescence was observed only in the OX:RSH1 and rshQM low ppGpp lines, while high ppGpp rsh1-1 plants showed almost no autoluminescence (Fig. 1C). Quantification of lipid peroxidation products by HPLC further supported these findings: HOTEs increased in the wild-type in response to nitrogen deprivation, and this increase was significantly larger in the ppGpp deficient lines (Fig. 1D). These results indicate that nitrogen deprivation promotes reactive-oxygen species (ROS) accumulation, and that ppGpp is required to prevent overaccumulation of ROS, oxidative stress and death of cotyledons under these conditions
Summary
Plants cannot escape harsh environmental fluctuations, and so their survival hinges on facing each threat To this end plants have developed intricate stress perception and response mechanisms (Devireddy et al, 2021), where the chloroplast is recognized as both a major signaling hub and a target for acclimation (Kleine et al, 2021). The artificial accumulation of ppGpp itself has been shown to repress the expression of certain chloroplast genes in vivo via the inhibition of chloroplast transcription (Yamburenko et al, 2015; Maekawa et al, 2015; Sugliani et al, 2016; Ono et al, 2020). Our work indicates that ppGpp is a pivotal regulator of chloroplast activity with a photoprotective role and that ppGpp signaling is required for the acclimation of plants to harsh environmental conditions
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