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

Arabidopsis wildtype plants suffer symptoms of stress at a sudden increase in CO₂ concentration, resulting from perturbation of photosynthetic electron transport. Defense-related gene induction includes increased methionine cycle and glucosinolates metabolism. Elevated CO₂ (eCO₂) 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 CO₂ 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 CO₂, 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 CO₂. Comparisons enabled separating the impact of eCO₂ (1000 ppm) on increased carbon assimilation from that of reduced photorespiration. While both genotypes had elevated sugar levels at eCO₂, 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, eCO₂ 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.