Growth at Elevated CO2 Requires Acclimation of the Respiratory Chain to Support Photosynthesis

Plants will experience an elevated atmospheric concentration of CO2 (ECO2) in the future. Growth of tobacco (Nicotiana tabacum) at ECO2 more than doubled the leaf protein amount of alternative oxidase (AOX), a non-energy-conserving component of mitochondrial respiration. To test the functional significance of this AOX increase, wild-type tobacco was compared with AOX knockdown and overexpression lines, following growth at ambient CO2 or ECO2. The ECO2-grown AOX knockdowns had a reduced capacity for triose phosphate use (TPU) during photosynthesis compared with the other plant lines. This TPU limitation of CO2 assimilation was associated with an increased accumulation of glucose-6-phosphate, sucrose, and starch in the leaves of the knockdowns. Under TPU-limiting conditions, the size of the proton gradient and proton motive force across the thylakoid membrane was enhanced in the knockdowns relative to the other plant lines, suggesting a restriction of chloroplast ATP synthase activity. This restriction was not due to a decline in ATP synthase (AtpB) protein amount. The knockdowns also displayed a photosystem stoichiometry adjustment at ECO2, which was absent in the other plant lines. Additional experiments showed that the way in which AOX supports photosynthesis at ECO2 is distinct from its previously described role in supporting photosynthesis during water deficit. The results are discussed in terms of how AOX contributes to TPU capacity and the maintenance of chloroplast ATP synthase activity at ECO2. Overall, the evidence suggests that AOX respiration is needed to maintain both the carbon and energy balance in photosynthetic tissues during growth at ECO2.