Light Regulation of the Arabidopsis Respiratory Chain. Multiple Discrete Photoreceptor Responses Contribute to Induction of Type II NAD(P)H Dehydrogenase Genes

Abstract

Controlled oxidation reactions catalyzed by the large, proton-pumping complexes of the respiratory chain generate an electrochemical gradient across the mitochondrial inner membrane that is harnessed for ATP production. However, several alternative respiratory pathways in plants allow the maintenance of substrate oxidation while minimizing the production of ATP. We have investigated the role of light in the regulation of these energy-dissipating pathways by transcriptional profiling of the alternative oxidase, uncoupling protein, and type II NAD(P)H dehydrogenase gene families in etiolated Arabidopsis seedlings. Expression of the nda1 and ndc1 NAD(P)H dehydrogenase genes was rapidly up-regulated by a broad range of light intensities and qualities. For both genes, light induction appears to be a direct transcriptional effect that is independent of carbon status. Mutant analyses demonstrated the involvement of two separate photoreceptor families in nda1 and ndc1 light regulation: the phytochromes (phyA and phyB) and an undetermined blue light photoreceptor. In the case of the nda1 gene, the different photoreceptor systems generate distinct kinetic induction profiles that are integrated in white light response. Primary transcriptional control of light response was localized to a 99-bp region of the nda1 promoter, which contains an I-box flanked by two GT-1 elements, an arrangement prevalent in the promoters of photosynthesis-associated genes. Light induction was specific to nda1 and ndc1. The only other substantial light effect observed was a decrease in aox2 expression. Overall, these results suggest that light directly influences the respiratory electron transport chain via photoreceptor-mediated transcriptional control, likely for supporting photosynthetic metabolism.The electron transport chain (ETC) and ATP synthase catalyze the final steps of aerobic respiration, whereby reduced organic compounds are converted into chemical energy in the form of ATP. The ETC is located in the inner mitochondrial membrane and is composed of four large, multiprotein complexes common to both plants and animals. Complexes I and II catalyze the oxidation of matrix NADH and succinate, respectively, transferring electrons to lipid-soluble ubiquinone. Reduced ubiquinone is then oxidized via complex III, which donates electrons to the cytochrome c protein. Complex IV then transfers electrons from cytochrome c to the terminal electron acceptor, O 2 , generating water. The oxidation reactions mediated by complexes I, III, and IV are coupled to the pumping of protons across the inner membrane, generating an electrochemical gradient. This membrane gradient is harnessed by the F o F 1 -ATP synthase for the production of ATP (Siedow and Day, 2000).In addition to the basal ETC described above, plants possess several alternative respiratory pathways that bypass energy conservation by circumventing the formation or utilization of the electrochemical proton gradient. These energy-dissipating pathways are formed by several simple proteins: type ...

Remodeled Respiration in ndufs4 with Low Phosphorylation Efficiency Suppresses Arabidopsis Germination and Growth and Alters Control of Metabolism at Night

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Thousands of Cis-Regulatory Sequence Combinations Are Shared by Arabidopsis and Poplar

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Plant MetGenMAP: An Integrative Analysis System for Plant Systems Biology

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