Sudden elevation of carbon dioxide concentration causes perturbation of the electron transport chain and triggers defense responses in Arabidopsis thaliana

Abstract Main conclusion Arabidopsis wildtype plants suffer symptoms of stress at a sudden increase in CO 2 concentration, resulting from perturbation of photosynthetic electron transport. Defense-related gene induction includes increased methionine cycle and glucosinolates metabolism. Abstract Elevated CO 2 (eCO 2 ) increases photosynthetic performance of plants, but also leads to decreased nitrogen-to-carbon ratio and a long-term decline in photosynthetic activity, known as photosynthetic acclimation. It is unclear whether initially increased CO 2 assimilation or perturbation of the physiological homeostasis triggers acclimation. Here, we used a combination of omics analysis to investigate immediate (1 day) and delayed (7 days) responses of plants to rising atmospheric CO 2 , thus allowing us to discriminate regulatory from metabolic effects. Responses of wildtype Arabidopsis plants, Columbia-0, were compared to those of the hpr1-1 mutant of peroxisomal hydroxy-pyruvate reductase that has reduced photorespiratory turnover at ambient CO 2 . Comparisons enabled separating the impact of eCO 2 (1000 ppm) on increased carbon assimilation from that of reduced photorespiration. While both genotypes had elevated sugar levels at eCO 2 , the wildtype displayed symptoms of stress that were accompanied by perturbation of the photosynthetic electron transport chain. These were consistent with physiological parameters, including non-photochemical quenching and chlorophyll fluorescence. The induction of defense-related mechanisms was tightly associated with increased sulfate assimilation, methionine cycle activity and glucosinolates metabolism, all being early responses of the wildtype to eCO 2. Transcriptome data pointed to hexokinase1 as a central regulatory hub in orchestrating these responses. In contrast, eCO 2 enabled the hpr1-1 mutant to metabolically align with the wildtype. Results offer new interpretations of how the impairment of carbon and nitrogen recycling is compensated in the hpr1-1 mutant.