Kinetic properties and physiological role of the plastoquinone terminal oxidase (PTOX) in a vascular plant

Trouillard, Martin; Shahbazi, Maryam; Moyet, Lucas; Rappaport, Fabrice; Joliot, Pierre; Kuntz, Marcel; Finazzi, Guido

doi:10.1016/j.bbabio.2012.08.006

Cited by 77 publications

(55 citation statements)

References 51 publications

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“…This response is called RISE , and it might be the main driver of P700 oxidation under CO 2 limitation in cyanobacteria. Respiratory terminal oxidases like Cyt c oxidase and cytochrome bd-type quinol oxidase also may contribute to the oxidation of the donor side of PSI under CO 2 limitation (Beardall et al, 2003;Trouillard et al, 2012;Lea-Smith et al, 2013). It is difficult, however, to explain why Y(II) decreased during CO 2 limitation in the cyanobacteria we studied ( Fig.…”

Section: Discussionmentioning

confidence: 69%

“…Second, plastidial terminal oxidase and cyanobacterial respiratory terminal oxidases on the thylakoid membranes suppress PSI electron influx by accepting upstream PSI electrons in the PET system. Oxygen is the final electron acceptor (Beardall et al, 2003;Trouillard et al, 2012;Lea-Smith et al, 2013). Finally, plastoquinol accumulation inhibits the Q-cycle turnover in the Cyt b 6 /f complex, which suppresses electron flow from the Cyt b 6 /f complex to P700.…”

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confidence: 99%

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Oxidation of P700 in Photosystem I Is Essential for the Growth of Cyanobacteria

2016

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The photoinhibition of photosystem I (PSI) is lethal to oxygenic phototrophs. Nevertheless, it is unclear how photodamage occurs or how oxygenic phototrophs prevent it. Here, we provide evidence that keeping P700 (the reaction center chlorophyll in PSI) oxidized protects PSI. Previous studies have suggested that PSI photoinhibition does not occur in the two model cyanobacteria, Synechocystis sp. PCC 6803 and Synechococcus elongatus PCC 7942, when photosynthetic CO 2 fixation was suppressed under low CO 2 partial pressure even in mutants deficient in flavodiiron protein (FLV), which mediates alternative electron flow. The lack of FLV in Synechococcus sp. PCC 7002 (S. 7002), however, is linked directly to reduced growth and PSI photodamage under CO 2 -limiting conditions. Unlike Synechocystis sp. PCC 6803 and S. elongatus PCC 7942, S. 7002 reduced P700 during CO 2 -limited illumination in the absence of FLV, resulting in decreases in both PSI and photosynthetic activities. Even at normal air CO 2 concentration, the growth of S. 7002 mutant was retarded relative to that of the wild type. Therefore, P700 oxidation is essential for protecting PSI against photoinhibition. Here, we present various strategies to alleviate PSI photoinhibition in cyanobacteria.Low CO 2 fixation efficiency in the Calvin-Benson cycle prevents the utilization of NADPH and ATP in photosynthesis and causes these molecules to accumulate, resulting in oxidative photosynthetic cell damage. High light, low temperature, and CO 2 limitation increase NADPH and ATP levels beyond the Calvin-Benson cycle requirements. Electrons and H +

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Section: Discussionmentioning

confidence: 69%

mentioning

confidence: 99%

Oxidation of P700 in Photosystem I Is Essential for the Growth of Cyanobacteria

2016

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“…8). The electron flow capacity of PTOX in chloroplasts from tomato leaves is consistently described as being two orders of magnitude lower than the photosynthetic linear flow (Trouillard et al, 2012); therefore, the oxygen uptake activity attributable to PTOX in photosynthetic tissues is probably undetectable by the oxygen electrode.…”

Section: Chromorespiration Involves the Cytochrome B 6 F Complex And mentioning

confidence: 99%

Tomato Fruit Chromoplasts Behave as Respiratory Bioenergetic Organelles during Ripening

et al. 2014

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During tomato (Solanum lycopersicum) fruit ripening, chloroplasts differentiate into photosynthetically inactive chromoplasts. It was recently reported that tomato chromoplasts can synthesize ATP through a respiratory process called chromorespiration. Here we show that chromoplast oxygen consumption is stimulated by the electron donors NADH and NADPH and is sensitive to octyl gallate (Ogal), a plastidial terminal oxidase inhibitor. The ATP synthesis rate of isolated chromoplasts was dependent on the supply of NAD(P)H and was fully inhibited by Ogal. It was also inhibited by the proton uncoupler carbonylcyanide m-chlorophenylhydrazone, suggesting the involvement of a chemiosmotic gradient. In addition, ATP synthesis was sensitive to 2,5-dibromo-3-methyl-6-isopropyl-p-benzoquinone, a cytochrome b 6 f complex inhibitor. The possible participation of this complex in chromorespiration was supported by the detection of one of its components (cytochrome f) in chromoplasts using immunoblot and immunocytochemical techniques. The observed increased expression of cytochrome c 6 during ripening suggests that it could act as electron acceptor of the cytochrome b 6 f complex in chromorespiration. The effects of Ogal on respiration and ATP levels were also studied in tissue samples. Oxygen uptake of mature green fruit and leaf tissues was not affected by Ogal, but was inhibited increasingly in fruit pericarp throughout ripening (up to 26% in red fruit). Similarly, Ogal caused a significant decrease in ATP content of red fruit pericarp. The number of energized mitochondria, as determined by confocal microscopy, strongly decreased in fruit tissue during ripening. Therefore, the contribution of chromoplasts to total fruit respiration appears to increase in late ripening stages.

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“…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). Thus, the nonphotochemical dark reduction of PQ in DpsaI could arise from an increased reduction and/or a decreased oxidation rate and relies on the availability of oxygen and reducing equivalents.…”

Section: Nonphotochemical Dark-reduction Of Pq As a Compensatory Mechmentioning

confidence: 99%

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

et al. 2016

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PsaI represents one of three low molecular weight peptides of PSI. Targeted inactivation of the plastid PsaI gene in Nicotiana tabacum has no measurable effect on photosynthetic electron transport around PSI or on accumulation of proteins involved in photosynthesis. Instead, the lack of PsaI destabilizes the association of PsaL and PsaH to PSI, both forming the light-harvesting complex (LHC)II docking site of PSI. These alterations at the LHCII binding site surprisingly did not prevent state transition but led to an increased incidence of PSI-LHCII complexes, coinciding with an elevated phosphorylation level of the LHCII under normal growth light conditions. Remarkably, LHCII was rapidly phosphorylated in DpsaI in darkness even after illumination with far-red light. We found that this dark phosphorylation also occurs in previously described mutants impaired in PSI function or state transition. A prompt shift of the plastoquinone (PQ) pool into a more reduced redox state in the dark caused an enhanced LHCII phosphorylation in DpsaI. Since the redox status of the PQ pool is functionally connected to a series of physiological, biochemical, and gene expression reactions, we propose that the shift of mutant plants into state 2 in darkness represents a compensatory and/or protective metabolic mechanism. This involves an increased reduction and/or reduced oxidation of the PQ pool, presumably to sustain a balanced excitation of both photosystems upon the onset of light.PSI is indisputably the most efficient solar energy converter with a potential quantum efficiency close to 100% (Nelson and Yocum, 2006;Nelson, 2009). It mediates the oxidation of plastocyanin and, subsequently, the reduction of ferredoxin resulting in the production of NADPH. The connection between PSII and PSI in the linear electron transport is provided by the cytochrome b 6 f complex. The electrochemical proton gradient build-up during the light-driven electron transport across the thylakoid membrane provides the proton motive force used for the conversion of ADP to ATP. Besides the linear electron transport, which leads to the production of both ATP and NADPH, PSI is also able to perform cyclic electron transport without the involvement of PSII and resulting solely in the generation of ATP (Yamori and Shikanai, 2016). Two routes of cyclic electron transport exist, the PROTON GRADIENT REGULATION (PGR)5/PGRL1-and the NAD(P)H dehydrogenase (NDH)-dependent pathway providing the possibility to adjust the ATP/NADPH ratio to handle changing metabolic demands and to prevent especially PSI from photoinhibition under challenging light regimes (Munekage et al., 2002;Kramer et al., 2004;Joliot and Johnson, 2011;Suorsa et al., 2012).Although the catalytic core and the function of PSI in cyanobacteria and plants remained very similar since the endosymbiotic event, its structural organization strikingly changed during plant evolution Nelson, 2008, 2009). The size of the entire plant PSI complex increased compared to the cyanobacterial PSI (Jordan et al., 2001;Amun...

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Kinetic properties and physiological role of the plastoquinone terminal oxidase (PTOX) in a vascular plant

Cited by 77 publications

References 51 publications

Oxidation of P700 in Photosystem I Is Essential for the Growth of Cyanobacteria

Oxidation of P700 in Photosystem I Is Essential for the Growth of Cyanobacteria

Tomato Fruit Chromoplasts Behave as Respiratory Bioenergetic Organelles during Ripening

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

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