Transcriptional and Metabolic Insights into the Differential Physiological Responses of Arabidopsis to Optimal and Supraoptimal Atmospheric CO(2)

BACKGROUND: In tightly closed human habitats such as space stations, locations near volcano vents and closed culture vessels, atmospheric CO(2) concentration may be 10 to 20 times greater than Earth’s current ambient levels. It is known that super-elevated (SE) CO(2) (>1,200 µmol mol(−1)) induces physiological responses different from that of moderately elevated CO(2) (up to 1,200 µmol mol(−1)), but little is known about the molecular responses of plants to supra-optimal [CO(2)]. METHODOLOGY/PRINCIPAL FINDINGS: To understand the underlying molecular causes for differential physiological responses, metabolite and transcript profiles were analyzed in aerial tissue of Arabidopsis plants, which were grown under ambient atmospheric CO(2) (400 µmol mol(−1)), elevated CO(2) (1,200 µmol mol(−1)) and SE CO(2) (4,000 µmol mol(−1)), at two developmental stages early and late vegetative stage. Transcript and metabolite profiling revealed very different responses to elevated versus SE [CO(2)]. The transcript profiles of SE CO(2) treated plants were closer to that of the control. Development stage had a clear effect on plant molecular response to elevated and SE [CO(2)]. Photosynthetic acclimation in terms of down-regulation of photosynthetic gene expression was observed in response to elevated [CO(2)], but not that of SE [CO(2)] providing the first molecular evidence that there appears to be a fundamental disparity in the way plants respond to elevated and SE [CO(2)]. Although starch accumulation was induced by both elevated and SE [CO(2)], the increase was less at the late vegetative stage and accompanied by higher soluble sugar content suggesting an increased starch breakdown to meet sink strength resulting from the rapid growth demand. Furthermore, many of the elevated and SE CO(2)-responsive genes found in the present study are also regulated by plant hormone and stress. CONCLUSIONS/SIGNIFICANCE: This study provides new insights into plant acclimation to elevated and SE [CO(2)] during development and how this relates to stress, sugar and hormone signaling.