Plastid terminal oxidase 2 (PTOX2) is the major oxidase involved in chlororespiration in
            <i>Chlamydomonas</i>

Houille-Vernes, Laura; Rappaport, Fabrice; Wollman, Françis-André; Alric, Jean; Johnson, Xenie

doi:10.1073/pnas.1110518109

Cited by 160 publications

(168 citation statements)

References 37 publications

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“…Proteins were transferred onto nitrocellulose filters (BioTrace NT; Pall Corporation) using a semidry apparatus (BIORAD). Primary antibodies were sourced from Michael Hippler (PSAD, LHCSR3, PGRL1, and ANR1; Naumann et al, 2005Naumann et al, , 2007Petroutsos et al, 2009;Terashima et al, 2012), Gilles Peltier (PGRL1; Tolleter et al, 2011), Pierre Cardol (NDA2; Jans et al, 2008), Agrisera (LSU, COXIIb, Psba D1, CF1, and AOX1), and Francis-Andre Wollman (PTOX2 and cyt f; Vallon et al, 1991;Houille-Vernes et al, 2011) and decorated by incubation in Tris-buffered saline. Secondary antibody was anti-rabbit (Invitrogen).…”

Section: Protein Analysismentioning

confidence: 99%

“…Most of these alternative pathways use molecular oxygen (O 2 ) as a terminal electron acceptor, and their prevalence is even more species dependent than CEF. The plastoquinol terminal oxidase (PTOX) is active in chlororespiration to balance dark chloroplast redox poise and can also work as a valve under specific conditions to oxidize plastoquinols while reducing oxygen when the PQ pool is overreduced (Bailey et al, 2008;Houille-Vernes et al, 2011). The Mehler reaction describes a water-water cycle in which electrons generated by the splitting of water at the donor side of PSII are used to reduce O 2 at the acceptor side of PSI.…”

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confidence: 99%

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Proton Gradient Regulation 5-Mediated Cyclic Electron Flow under ATP- or Redox-Limited Conditions: A Study of ƊATPase pgr5 and ƊrbcL pgr5 Mutants in the Green Alga Chlamydomonas reinhardtii

et al. 2014

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The Chlamydomonas reinhardtii proton gradient regulation5 (Crpgr5) mutant shows phenotypic and functional traits similar to mutants in the Arabidopsis (Arabidopsis thaliana) ortholog, Atpgr5, providing strong evidence for conservation of PGR5-mediated cyclic electron flow (CEF). Comparing the Crpgr5 mutant with the wild type, we discriminate two pathways for CEF and determine their maximum electron flow rates. The PGR5/proton gradient regulation-like1 (PGRL1) ferredoxin (Fd) pathway, involved in recycling excess reductant to increase ATP synthesis, may be controlled by extreme photosystem I acceptor side limitation or ATP depletion. Here, we show that PGR5/PGRL1-Fd CEF functions in accordance with an ATP/redox control model. In the absence of Rubisco and PGR5, a sustained electron flow is maintained with molecular oxygen instead of carbon dioxide serving as the terminal electron acceptor. When photosynthetic control is decreased, compensatory alternative pathways can take the full load of linear electron flow. In the case of the ATP synthase pgr5 double mutant, a decrease in photosensitivity is observed compared with the single ATPase-less mutant that we assign to a decreased proton motive force. Altogether, our results suggest that PGR5/PGRL1-Fd CEF is most required under conditions when Fd becomes overreduced and photosystem I is subjected to photoinhibition. CEF is not a valve; it only recycles electrons, but in doing so, it generates a proton motive force that controls the rate of photosynthesis. The conditions where the PGR5 pathway is most required may vary in photosynthetic organisms like C. reinhardtii from anoxia to high light to limitations imposed at the level of carbon dioxide fixation.Photosynthesis is a highly regulated process that integrates different electron transfer pathways to convert light energy into ATP and NADPH and balance this production of chemical energy with its use in anabolic metabolism. Linear electron flow accounts for the major flux of electrons from the primary electron donor water to PSII and intersystem carriers to reduce NADP + , the terminal acceptor associated with PSI. Electron transfer is coupled to proton transfer through reactions involving plastoquinones/plastoquinols that are dependent on the activity of the cytochrome b 6 f complex (cyt f); the protons are transferred from the stroma into the thylakoid lumen. The proton motive force generated is used for ATP synthesis by the ATP synthase. The NADPH and ATP produced in the light serve as the energy/reductant that drives the fixation of carbon dioxide (CO 2 ) by Rubisco and the Calvin-Benson cycle and also supports other downstream metabolic reactions.The Calvin-Benson cycle has a stoichiometric requirement of 3 ATP and 2 NADPH per CO 2 molecule; this requirement is not fulfilled by linear electron flow, because it is slightly imbalanced in favor of NADPH production. Cyclic electron flow (CEF) pathways allow the cells to fulfill the energetic requirement for sustained CO 2 fixation through recycling or reoxidation of ...

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Section: Protein Analysismentioning

confidence: 99%

mentioning

confidence: 99%

Proton Gradient Regulation 5-Mediated Cyclic Electron Flow under ATP- or Redox-Limited Conditions: A Study of ƊATPase pgr5 and ƊrbcL pgr5 Mutants in the Green Alga Chlamydomonas reinhardtii

et al. 2014

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“…The alternative oxidases, plastid plastoquinol terminal oxidases PTOX1 and PTOX2, are thought to be involved in the chlororespiration in C. reinhardtii (Rumeau et al, 2007;Bailleul et al, 2010;Houille-Vernes et al, 2011), and changes in protein and transcript abundance have been found to be associated with nutrient deprivation in algae, particularly iron deprivation as well as light stress (Houille-Vernes et al, 2011). PTOX1 and PTOX2 transcripts decreased in abundance 1.5-fold within the first half hour but then increased through 24 h to slightly less or greater than N-replete conditions.…”

Section: Changes In the Levels Of Transcripts And Proteins Of Photosymentioning

confidence: 99%

The Regulation of Photosynthetic Structure and Function during Nitrogen Deprivation in Chlamydomonas reinhardtii

Juergens

Deshpande²,

Lucker

et al. 2014

Plant Physiology

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The accumulation of carbon storage compounds by many unicellular algae after nutrient deprivation occurs despite declines in their photosynthetic apparatus. To understand the regulation and roles of photosynthesis during this potentially bioenergetically valuable process, we analyzed photosynthetic structure and function after nitrogen deprivation in the model alga Chlamydomonas reinhardtii. Transcriptomic, proteomic, metabolite, and lipid profiling and microscopic time course data were combined with multiple measures of photosynthetic function. Levels of transcripts and proteins of photosystems I and II and most antenna genes fell with differing trajectories; thylakoid membrane lipid levels decreased, while their proportions remained similar and thylakoid membrane organization appeared to be preserved. Cellular chlorophyll (Chl) content decreased more than 2-fold within 24 h, and we conclude from transcript protein and 13 C labeling rates that Chl synthesis was down-regulated both pre-and posttranslationally and that Chl levels fell because of a rapid cessation in synthesis and dilution by cellular growth rather than because of degradation. Photosynthetically driven oxygen production and the efficiency of photosystem II as well as P700 + reduction and electrochromic shift kinetics all decreased over the time course, without evidence of substantial energy overflow. The results also indicate that linear electron flow fell approximately 15% more than cyclic flow over the first 24 h. Comparing Calvin-Benson cycle transcript and enzyme levels with changes in photosynthetic 13 CO 2 incorporation rates also pointed to a coordinated multilevel down-regulation of photosynthetic fluxes during starch synthesis before the induction of high triacylglycerol accumulation rates.

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“…In several plant species, up-regulation of PTOX has been observed in response to adverse conditions, such as exposure to high-light stress in low or elevated temperature environments (Streb et al, 2005) or under salt stress (Stepien and Johnson, 2009). Deletion of the PTOX2 gene in Chlamydomonas reinhardtii, encoding PTOX, confirmed a role in preventing overreduction of the plastoquinone pool in the light (Houille-Vernes et al, 2011). The mutant demonstrated reduced fitness compared with the wild-type under illumination, although growth was not examined under varying environmental conditions.…”

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confidence: 94%

Thylakoid Terminal Oxidases Are Essential for the CyanobacteriumSynechocystissp. PCC 6803 to Survive Rapidly Changing Light Intensities

et al. 2013

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Cyanobacteria perform photosynthesis and respiration in the thylakoid membrane, suggesting that the two processes are interlinked. However, the role of the respiratory electron transfer chain under natural environmental conditions has not been established. Through targeted gene disruption, mutants of Synechocystis sp. PCC 6803 were generated that lacked combinations of the three terminal oxidases: the thylakoid membrane-localized cytochrome c oxidase (COX) and quinol oxidase (Cyd) and the cytoplasmic membrane-localized alternative respiratory terminal oxidase. All strains demonstrated similar growth under continuous moderate or high light or 12-h moderate-light/dark square-wave cycles. However, under 12-h high-light/dark square-wave cycles, the COX/Cyd mutant displayed impaired growth and was completely photobleached after approximately 2 d. In contrast, use of sinusoidal light/dark cycles to simulate natural diurnal conditions resulted in little photobleaching, although growth was slower. Under high-light/dark square-wave cycles, the COX/Cyd mutant suffered a significant loss of photosynthetic efficiency during dark periods, a greater level of oxidative stress, and reduced glycogen degradation compared with the wild type. The mutant was susceptible to photoinhibition under pulsing but not constant light. These findings confirm a role for thylakoid-localized terminal oxidases in efficient dark respiration, reduction of oxidative stress, and accommodation of sudden light changes, demonstrating the strong selective pressure to maintain linked photosynthetic and respiratory electron chains within the thylakoid membrane. To our knowledge, this study is the first to report a phenotypic difference in growth between terminal oxidase mutants and wild-type cells and highlights the need to examine mutant phenotypes under a range of conditions.

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Plastid terminal oxidase 2 (PTOX2) is the major oxidase involved in chlororespiration in Chlamydomonas

Cited by 160 publications

References 37 publications

Proton Gradient Regulation 5-Mediated Cyclic Electron Flow under ATP- or Redox-Limited Conditions: A Study of ƊATPase pgr5 and ƊrbcL pgr5 Mutants in the Green Alga Chlamydomonas reinhardtii

Proton Gradient Regulation 5-Mediated Cyclic Electron Flow under ATP- or Redox-Limited Conditions: A Study of ƊATPase pgr5 and ƊrbcL pgr5 Mutants in the Green Alga Chlamydomonas reinhardtii

The Regulation of Photosynthetic Structure and Function during Nitrogen Deprivation in Chlamydomonas reinhardtii

Thylakoid Terminal Oxidases Are Essential for the CyanobacteriumSynechocystissp. PCC 6803 to Survive Rapidly Changing Light Intensities

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