Chlororespiration, Sixteen Years Later

Summary

The model of chlororespiration was proposed by Bennoun (1982) in order to take into account experimental data concerning the state of thylakoid membranes in darkness. This model postulated the presence, in the thylakoid membranes, of an electrogenic respiratory electron transport chain. As observed in cyanobacteria, plastoquinone would be reduced by an NAD(P)H dehydrogenase, and reoxidized at the expense of oxygen by an oxidase. Such a pathway would explain both the formation of a permanent thylakoid electrochemical gradient in the absence of CF₀CF₁ ATP synthase, and the redox properties of plastoquinone observed in the dark. This model which stimulated many experiments must now be revised in the light of recent work. Particularly, the occurrence of mitochondrial-chloroplast interactions has to be taken into account: the mitochondrial electron transport chain controls strictly both the redox state of plastoquinone and the permanent electrochemical gradient. The possibility that a respiratory process generates the permanent electrochemical gradient is no longer consistent with the available data. This gradient rather results from the operation of a new ATP-dependent electrogenic pump. With regard to the existence of a chloroplast NAD(P)H dehydrogenase, clear-cut physiological evidence exists for an electron pathway connecting stromal reductants to plastoquinone in Chlamydomonas reinhardtii, whereas molecular evidence for such a chloroplast enzyme is lacking. However, the presence of a proton pumping enzyme closely related to the bacterial Complex I has been demonstrated in higher plants, which shows a higher specificity for NADH than for NADPH. Finally, there is at present no molecular evidence for the existence of a chloroplast oxidase. Given the existence of chloroplast-mitochondrial interactions, plastoquinol oxidation might alternatively occur through the mitochondrial electron transport chain, via a mobile electron carrier. Studies on the state of thylakoid membranes in darkness will have to evaluate the structure and function of the new ATP-dependent electrogenic pump present in the thylakoid membrane, to analyze thoroughly the bioenergetic interactions between chloroplast and mitochondria, and to elucidate the mode of oxidation of plastoquinone in the dark. Alternative models to that of chlororespiration are discussed in order to stimulate further experiments. Clearly, the state of the thylakoid membranes in darkness offers more than ever a vast field of investigations.