Photosynthesis, respiration and growth: A carbon and energy balancing act for alternative oxidase

This review summarizes knowledge of alternative oxidase, a mitochondrial electron transport chain component that lowers the ATP yield of plant respiration. Analysis of mutant and transgenic plants has established that alternative oxidase activity supports leaf photosynthesis. The interaction of alternative oxidase respiration with chloroplast metabolism is important under conditions that challenge energy and/or carbon balance in the photosynthetic cell. Under such conditions, alternative oxidase provides an extra-chloroplastic means to optimize the status of chloroplast energy pools (ATP, NADPH) and to manage cellular carbohydrate pools in response to changing rates of carbon fixation and carbon demand for growth and maintenance. Transcriptional and post-translational mechanisms ensure that alternative oxidase can respond effectively when carbon and energy balance are being challenged. This function appears particularly significant under abiotic stress conditions such as water deficit, high salinity, or temperature extremes. Under such conditions, alternative oxidase respiration positively affects growth and stress tolerance, despite it lowering the energy yield and carbon use efficiency of respiration. In part, this beneficial effect relates to the ability of alternative oxidase respiration to prevent excessive reactive oxygen species generation in both mitochondria and chloroplasts. Recent evidence suggests that alternative oxidase respiration is an interesting target for crop improvement.