The Nucleus-Encodedtrans-Acting Factor MCA1 Plays a Critical Role in the Regulation of CytochromefSynthesis inChlamydomonasChloroplasts

Boulouis, Alix; Raynaud, Cécile; Bujaldon, Sandrine; Aznar, Aude; Wollman, Françis-André; Choquet, Yves

doi:10.1105/tpc.110.078170

Cited by 72 publications

(73 citation statements)

References 75 publications

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“…It is also possible that the reduced atpH/F transcript levels may be a destabilization effect mediated by translational regulation. Such effects are also observed in the petA gene expression system in Chlamydomonas (Boulouis et al, 2011). Unlike its effects on atpH/F, loss of BFA3 resulted in a drastic increase in atpB transcript levels (Supplemental Fig.…”

Section: Discussionmentioning

confidence: 84%

BIOGENESIS FACTOR REQUIRED FOR ATP SYNTHASE 3 Facilitates Assembly of the Chloroplast ATP Synthase Complex

et al. 2016

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Thylakoid membrane-localized chloroplast ATP synthases use the proton motive force generated by photosynthetic electron transport to produce ATP from ADP. Although it is well known that the chloroplast ATP synthase is composed of more than 20 proteins with a 3 b 3 g 1 « 1 d 1 I 1 II 1 III 14 IV 1 stoichiometry, its biogenesis process is currently unclear. To unravel the molecular mechanisms underlying the biogenesis of chloroplast ATP synthase, we performed extensive screening for isolating ATP synthase mutants in Arabidopsis (Arabidopsis thaliana). In the recently identified bfa3 (biogenesis factors required for ATP synthase 3) mutant, the levels of chloroplast ATP synthase subunits were reduced to approximately 25% of wild-type levels. In vivo labeling analysis showed that assembly of the CF 1 component of chloroplast ATP synthase was less efficient in bfa3 than in the wild type, indicating that BFA3 is required for CF 1 assembly. BFA3 encodes a chloroplast stromal protein that is conserved in higher plants, green algae, and a few species of other eukaryotic algae, and specifically interacts with the CF 1 b subunit. The BFA3 binding site was mapped to a region in the catalytic site of CF 1 b. Several residues highly conserved in eukaryotic CF 1 b are crucial for the BFA3-CF 1 b interaction, suggesting a coevolutionary relationship between BFA3 and CF 1 b. BFA3 appears to function as a molecular chaperone that transiently associates with unassembled CF 1 b at its catalytic site and facilitates subsequent association with CF 1 a during assembly of the CF 1 subcomplex of chloroplast ATP synthase.

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Section: Discussionmentioning

confidence: 84%

BIOGENESIS FACTOR REQUIRED FOR ATP SYNTHASE 3 Facilitates Assembly of the Chloroplast ATP Synthase Complex

et al. 2016

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“…This latter plasmid was digested with SacI and XhoI and ligated with the 2,504-bp fragments obtained by digesting pExc-aAKR by the same enzymes to yield plasmid pDatpI. This construction was then introduced in the chloroplast genome of C. reinhardtii by biolistic transformation as described by Boulouis et al (2011), and transformed clones were recovered on TAP plates supplemented with spectinomycin (100 mg mL 21 ). The transformants were then individually streaked onto 500 mg mL 21 spectinomycin to generate homoplasmic strains.…”

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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“…For example, in Chlamydomonas, nitrogen deprivation leads to rapid decrease in the amount of cytochrome b 6 f complexes. This coordinate response involves the proteolytic degradation of its subunits and also of Mca1 and Tca1, nucleusencoded proteins that determine the stability and translation of petA mRNA, which encodes the Cytf subunit (Raynaud et al, 2007;Boulouis et al, 2011;Wei et al, 2014). The concerted response to nitrogen deprivation also involves other nucleusencoded proteins that take part in the assembly of the complex and its hemes (Wei et al, 2014).…”

Section: Introductionmentioning

confidence: 99%

A Nucleus-Encoded Chloroplast Phosphoprotein Governs Expression of the Photosystem I Subunit PsaC in Chlamydomonas reinhardtii

Douchi

Longoni

et al. 2016

Plant Cell

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The nucleo-cytoplasmic compartment exerts anterograde control on chloroplast gene expression through numerous proteins that intervene at posttranscriptional steps. Here, we show that the maturation of psaC mutant (mac1) of Chlamydomonas reinhardtii is defective in photosystem I and fails to accumulate psaC mRNA. The MAC1 locus encodes a member of the Half-A-Tetratricopeptide (HAT) family of super-helical repeat proteins, some of which are involved in RNA transactions. The Mac1 protein localizes to the chloroplast in the soluble fraction. MAC1 acts through the 59 untranslated region of psaC transcripts and is required for their stability. Small RNAs that map to the 59end of psaC RNA in the wild type but not in the mac1 mutant are inferred to represent footprints of MAC1-dependent protein binding, and Mac1 expressed in bacteria binds RNA in vitro. A coordinate response to iron deficiency, which leads to dismantling of the photosynthetic electron transfer chain and in particular of photosystem I, also causes a decrease of Mac1. Overexpression of Mac1 leads to a parallel increase in psaC mRNA but not in PsaC protein, suggesting that Mac1 may be limiting for psaC mRNA accumulation but that other processes regulate protein accumulation. Furthermore, Mac 1 is differentially phosphorylated in response to iron availability and to conditions that alter the redox balance of the electron transfer chain.

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The Nucleus-Encodedtrans-Acting Factor MCA1 Plays a Critical Role in the Regulation of CytochromefSynthesis inChlamydomonasChloroplasts

Cited by 72 publications

References 75 publications

BIOGENESIS FACTOR REQUIRED FOR ATP SYNTHASE 3 Facilitates Assembly of the Chloroplast ATP Synthase Complex

BIOGENESIS FACTOR REQUIRED FOR ATP SYNTHASE 3 Facilitates Assembly of the Chloroplast ATP Synthase Complex

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

A Nucleus-Encoded Chloroplast Phosphoprotein Governs Expression of the Photosystem I Subunit PsaC in Chlamydomonas reinhardtii

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