Alternative Oxidase: Integrating Carbon Metabolism and Electron Transport in Plant Respiration

Abstract

The plant mitochondrial electron transport chain (ETC) is branched. Electrons pass along the phosphorylating cytochrome pathway or the non-phosphorylating alternative oxidase (AOX) pathway, which represents the CN-resistant component of respiration. The production of monoclonal antibodies, isolation of cDNA and genomic clones, and generation of transgenic plants have dramatically increased our understanding of AOX. The partitioning ofelectrons to AOX is regulated in a dynamic manner which is dependent upon both the carbon and redox status of the mitochondrion and it is likely that the contribution of AOX to total plant respiration has often been dramatically underestimated. Both matrix pyruvate level and the redox state of matrix NAD(P) alter the kinetic properties of AOX, modulating its ability to compete with the cytochrome pathway for electrons. Sitedirected rnutagenesis studies are revealing the mechanisms of this biochemical regulation. AOX is encoded, in some species at least, by a multi-gene family and, while the genes are differentially expressed, the functional significance of the different gene products is not yet understood. AOX gene expression may be dependent upon signals which reflect the carbon and redox status of the mitochondrion. Both citrate and active oxygen species (AOS) are potentially important in the signal transduction from mitochondrion to nucleus that controls AOX expression. Metabolic conditions that lead to accumulation of reducing equivalents and pyruvate in the mitochondrial matrix will favor partitioning of electrons toward AOX. Such conditions arise when there is an imbalance between upstream carbon metabolism and downstream electron transport, for example during shifts in metabolism, developmental change, nutrient availability, abiotic or biotic stress. Hence, the general function of AOX may be to integrate the coupled processes of carbon metabolism and electron transport, so as to correct for such imbalances. Experiments with transgenic cells lacking AOX have shown that such integration is critical in preventing both excessive mitochondrial AOS generation and redirections in carbon metabolism. This role for AOX may be particularly important under conditions such as phosphorus-limited growth. Recent data also suggest that AOX plays a role in resistance responses to pathogen attack and in cell death processes.