The Plastid Terminal Oxidase: Its Elusive Function Points to Multiple Contributions to Plastid Physiology

Abstract

Plastids have retained from their cyanobacterial ancestor a fragment of the respiratory electron chain comprising an NADPH dehydrogenase and a diiron oxidase, which sustain the so-called chlororespiration pathway. Despite its very low turnover rates compared with photosynthetic electron flow, knocking out the plastid terminal oxidase (PTOX) in plants or microalgae leads to severe phenotypes that encompass developmental and growth defects together with increased photosensitivity. On the basis of a phylogenetic and structural analysis of the enzyme, we discuss its physiological contribution to chloroplast metabolism, with an emphasis on its critical function in setting the redox poise of the chloroplast stroma in darkness. The emerging picture of PTOX is that of an enzyme at the crossroads of a variety of metabolic processes, such as, among others, the regulation of cyclic electron transfer and carotenoid biosynthesis, which have in common their dependence on the redox state of the plastoquinone pool, set largely by the activity of PTOX in darkness.

Impaired Mitochondrial Transcription Termination Disrupts the Stromal Redox Poise in Chlamydomonas

“…In addition to respiratory pathways located in mitochondria, chlororespiration (Bennoun, 1982) can contribute to dark respiration. Within this pathway, electrons from NADPH can be transferred to oxygen via the concerted action of the plastid-localized NADPH:plastoquinone oxidoreductase NDA2 (Jans et al, 2008) and a plastid terminal oxidase (PTOX), which transfers electrons from plastoquinol to oxygen (Nawrocki et al, 2015). To determine the relative contribution of cyanide-sensitive complex IV (cytochrome c oxidase) and cyanide-insensitive alternative respiration (AOX and PTOX activity) to mitochondrial respiration (Fig.…”

“…4). Although chlororespiration should be a means to prevent PQ pool overreduction and could dissipate excess reducing equivalents in the chloroplast, the restricted electron flow capacity of this pathway challenges its prominent role for PSII protection under high light conditions (Nawrocki et al, 2015).…”

The Low Molecular Weight Protein PsaI Stabilizes the Light-Harvesting Complex II Docking Site of Photosystem I

“…In the dark, the redox state of the PQ is poised by reducing agents such as ascorbate (Hou et al, 2003) and the chlororespiratory pathway involving electron transfer from reducing equivalents to PQ and the NDH complex and reoxidation of PQ by the plastid terminal oxidase (PTOX), which transfers the electrons to oxygen (for review, see Nawrocki et al, 2015). Consequently, these light-independent processes probably help to keep up a proton gradient across the thylakoid membrane, which in turn might be necessary for various processes that depend on a proton motive force (for review, see Nawrocki et al, 2015).…”

“…Consequently, these light-independent processes probably help to keep up a proton gradient across the thylakoid membrane, which in turn might be necessary for various processes that depend on a proton motive force (for review, see Nawrocki et al, 2015). Changes in nonphotochemical dark reduction/oxidation of PQ were previously shown to occur under certain stress conditions, such as high light, heat, cold, and CO 2 deprivation, but the exact mechanism and original electron sources remained rather elusive (Rumeau et al, 2007;Trouillard et al, 2012).…”

“…The increased amount of PSI-LHCII complexes of DpsaI and PSI mutants in the dark possibly reflects a nonphotochemical mechanism to balance excitation of both photosystems and/or to protect the photosystems from photoinhibition upon the onset of light or under fluctuating light conditions Horton 2012). Further analysis of the different PSI mutants will be necessary to address the nature of the redox carriers (Fisher and Cramer 2014), the regulation of nonphotochemical dark reduction/oxidation of PQ, and its contribution to multiple physiological processes, such as redox sensing, retrograde signaling, lumenal import of proteins, metabolic processes, and DpH-dependent nonphotochemical quenching upon dark-light switches (Pfalz et al, 2012;Puthiyaveetil et al, 2012;Nawrocki et al, 2015).…”