Biogenesis of PSI involves a cascade of translational autoregulation in the chloroplast of Chlamydomonas

Wostrikoff, Katia; Girard‐Bascou, Jacqueline; Wollman, Françis-André; Choquet, Yves

doi:10.1038/sj.emboj.7600266

Cited by 107 publications

(96 citation statements)

References 37 publications

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“…One obstacle in research into PSI assembly in plant chloroplasts has been the fast rate at which this occurs [50,51]. Nevertheless, it is known from Chlamydomonas that the biogenesis of PSI is controlled by the epistasy of synthesis process (CES), in which the presence of the PsaB protein enables the synthesis of the PsaA protein, which is in turn required for translation of the PsaC protein [52]. The assembly of the PSI iron-sulphur clusters is also well coordinated.…”

Section: Does Photoinhibition and Repair Of Psii Also Protect Psi Agamentioning

confidence: 99%

Regulation of the photosynthetic apparatus under fluctuating growth light

Tikkanen

Grieco

Nurmi

et al. 2012

Phil. Trans. R. Soc. B

144

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Safe and efficient conversion of solar energy to metabolic energy by plants is based on tightly interregulated transfer of excitation energy, electrons and protons in the photosynthetic machinery according to the availability of light energy, as well as the needs and restrictions of metabolism itself. Plants have mechanisms to enhance the capture of energy when light is limited for growth and development. Also, when energy is in excess, the photosynthetic machinery slows down the electron transfer reactions in order to prevent the production of reactive oxygen species and the consequent damage of the photosynthetic machinery. In this opinion paper, we present a partially hypothetical scheme describing how the photosynthetic machinery controls the flow of energy and electrons in order to enable the maintenance of photosynthetic activity in nature under continual fluctuations in white light intensity. We discuss the roles of light-harvesting II protein phosphorylation, thermal dissipation of excess energy and the control of electron transfer by cytochrome b 6 f, and the role of dynamically regulated turnover of photosystem II in the maintenance of the photosynthetic machinery. We present a new hypothesis suggesting that most of the regulation in the thylakoid membrane occurs in order to prevent oxidative damage of photosystem I.

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Section: Does Photoinhibition and Repair Of Psii Also Protect Psi Agamentioning

confidence: 99%

Regulation of the photosynthetic apparatus under fluctuating growth light

Tikkanen

Grieco

Nurmi

et al. 2012

Phil. Trans. R. Soc. B

144

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“…Thus translation of the CES subunits only occurs if the previous step in the assembly pathway has been accomplished. In the case of PSI a CES cascade has been identified that proceeds first by the insertion of the PsaB subunit into the membrane (Wostrikoff et al, 2004). The PsaA subunit that forms the PSI core together with PsaA is translated as long as the partner of its assembly, PsaB is present.…”

Section: Assembly Of Photosynthetic Complexesmentioning

confidence: 99%

Assembly of the Photosynthetic Apparatus

Rochaix

2011

Plant Physiology

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The primary reactions of photosynthesis are mediated by three protein complexes embedded in the thylakoid membranes of chloroplasts. These complexes are PSII, the cytochrome b 6 f complex (Cytb 6 f), and PSI, which are connected in series through the photosynthetic electron transport chain. Light energy captured by the light-harvesting systems of PSII (LHCII) and PSI (LHCI) is transferred to the reaction center chlorophylls to create a charge separation across the membrane. This leads to the formation of a strong oxidant on the donor side of PSII capable of splitting water into molecular oxygen, protons, and electrons. The electrons are transferred stepwise from PSII to the plastoquinone pool, Cytb 6 f, plastocyanin, and PSI where a second charge separation creates a strong reductant capable of reducing ferredoxin that subsequently reduces NADP + to NADPH. Besides this linear electron pathway there is a cyclic pathway in which electrons are cycled around PSI through the Cytb 6 f complex. The electron transfer reactions are coupled to proton pumping into the lumen space of the thylakoids and the resulting pH gradient drives the ATP synthase for ATP production. Ultimately NADPH and ATP are used for CO 2 assimilation by the Calvin-Benson cycle. Thylakoid membranes of land plants are organized in two domains, the grana stacks, comprising 80% of the membrane, and the stromal nonappressed membranes that connect different grana stacks. The photosynthetic complexes with exception of Cytb 6 f, are not distributed evenly through the thylakoid membrane system. Whereas PSII is mostly confined to the grana regions, PSI and ATP synthase are located in the stroma lamellae. Electron transfer between these complexes is mediated by the diffusible electron carriers plastoquinone and plastocyanin.A characteristic feature of the photosynthetic complexes is that they all consist of numerous chloroplast and nucleus-encoded subunits. In the case of PSII, PSI, and Cytb 6 f these complexes contain in addition pigments such as chlorophylls and xanthophylls as well as hemes, quinones, and iron-sulfur (Fe-S) centers that act as redox cofactors. Hence the biogenesis of the photosynthetic apparatus involves a concerted interplay between the chloroplast and nucleocytosolic genetic systems as well as a tight coordination between protein and pigment synthesis and insertion into the thylakoid membranes. Analysis of numerous mutants affected in photosynthetic activity in Chlamydomonas reinhardtii, Arabidopsis (Arabidopsis thaliana), and Zea mays has provided many new insights into the assembly of the photosynthetic complexes (Barkan and Goldschmidt-Clermont, 2000;Eberhard et al., 2008).A remarkable feature of photosynthetic organisms is their ability to adapt to changing light conditions, which is reflected in changes in the organization of the photosynthetic complexes. This Update reviews recent advances in our understanding of the assembly of these complexes and for some of them, their remodeling and/or reversible association into supercomplexes...

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“…Selection was performed under 10 mE m 22 s 21 light at 25°C on TAP solid medium supplemented with 100 mg/mL spectinomycin (Sigma). Clones were then screened as described above for complementation of the NPQ phenotype using a laboratorybuilt chlorophyll fluorescence imaging system (Johnson et al, 2009). containing the psaA promoter and 59 UTR recovered by digesting the 59psaA-aadA-39rbcL plasmid (Wostrikoff et al, 2004) with EcoRV and NcoI to create the pExc-aAKR cassette. To replace the atpI coding sequence by the Exc-aAKR cassette for selection of transformed clones based on spectinomycin resistance, a DNA fragment containing the atpI 59 UTR fused to the 39 UTR but lacking the coding sequence was created by a two-step PCR procedure (Higuchi, 1990): two pairs of primers (atpI-dr_DelF1/atpI-dr_R1 and atpI-dr_F1/atpIdr_DelR1) allowed the amplification from the template plasmid p70 (http:// chlamycollection.org/plasmid/p-70-cpdna-ecori-17-4-9-kb/) of two partially overlapping fragments that were mixed and used as templates in a third PCR with the external primers atpI-dr_F1 and atpI-dr_R1 (primer sequences are in Supplemental Table S1).…”

Section: Complementationmentioning

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 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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Biogenesis of PSI involves a cascade of translational autoregulation in the chloroplast of Chlamydomonas

Cited by 107 publications

References 37 publications

Regulation of the photosynthetic apparatus under fluctuating growth light

Regulation of the photosynthetic apparatus under fluctuating growth light

Assembly of the Photosynthetic Apparatus

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

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