Cytochrome<i>f</i>Translation in Chlamydomonas Chloroplast Is Autoregulated by its Carboxyl-Terminal Domain[W]

Choquet, Yves; Zito, Francesca; Wostrikoff, Katia; Wollman, Françis-André

doi:10.1105/tpc.011692

Cited by 75 publications

(73 citation statements)

References 37 publications

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“…The basis for this control system is that elimination of one subunit reduces the expression of other subunits in the complex by their translational arrest, or by degradation of unassembled subunits. It was shown, for example, for the cytochrome b6f complex, that translation of cytochrome f, encoded by the petA gene, is autoregulated by its own C terminus, via an element in the 5# UTR of the petA mRNA (Choquet et al, 2003). A model was proposed in which this C-terminal domain is shielded in the assembled complex.…”

Section: Discussionmentioning

confidence: 99%

“…The coordinated expression of subunits that comprise large photosynthetic complexes takes place in the chloroplast, in a process that is designated controlled by epistasy of synthesis (CES; Choquet et al, 2003;Wostrikoff et al, 2004). Thus, in the absence of one subunit in the complex, synthesis of another subunit of the complex decreases (Choquet et al, 2003;Wostrikoff et al, 2004;Minai et al, 2006).…”

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confidence: 99%

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A Conserved Mechanism Controls Translation of Rubisco Large Subunit in Different Photosynthetic Organisms

2006

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We previously proposed a mechanism for control of Rubisco expression and assembly during oxidative stress in Chlamydomonas reinhardtii. The N terminus of the large subunit (LSU) comprises an RNA recognition motif (RRM) that is normally buried in the protein, but becomes exposed under oxidizing conditions when the glutathione pool shifts toward its oxidized form. Thus, de novo translation and assembly of Rubisco LSU stop with similar kinetics and the unpaired small subunit (SSU) is rapidly degraded. Here we show that the structure of the N-terminal domain is highly conserved throughout evolution, despite its relatively low sequence similarity. Furthermore, Rubisco from a broad evolutionary range of photosynthetic organisms binds RNA under oxidizing conditions, with dissociation constant values in the nanomolar range. In line with these observations, oxidative stress indeed causes a translational arrest in land plants as well as in Rhodospirillum rubrum, a purple bacterium that lacks the SSU. We highlight an evolutionary conserved element located within a-helix B, which is located in the center of the RRM and is also involved in the intramolecular interactions between two LSU chains. Thus, assembly masks the N terminus of the LSU hiding the RRM. When assembly is interrupted due to structural changes that occur under oxidizing conditions or in the absence of a dedicated chaperone, the N-terminal domain can become exposed, leading to the translational arrest of Rubisco LSU. Taken together, these results support a model by which LSU translation is governed by its dimerization. In the case that regulation of type I and type II Rubisco is conserved, the SSU does not appear to be directly involved in LSU translation.

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Section: Discussionmentioning

confidence: 99%

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confidence: 99%

A Conserved Mechanism Controls Translation of Rubisco Large Subunit in Different Photosynthetic Organisms

2006

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“…Unassembled cyt. f down-regulates its translation (18,27), most probably by trapping TCA1 by way of its C-terminal regulatory region (34). In tca1 transformants displaying high expression of cyt.…”

Section: Major Traits For the Nuclear Regulation Of Cytochrome F Exprmentioning

confidence: 99%

“…f accumulation (after normalization to that of the OEE2 protein from PSII) was quantified according to ref. 34. TCA1-fl and MCA1-HA were detected by ECL using monoclonal antibodies [anti-flag M2 (Sigma, St. Louis, MO) and anti HA.11 (Covance, Princeton, NJ)] and HRP-conjugated antibody against mouse IgG (Promega, Madison, WI).…”

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confidence: 99%

Evidence for regulatory function of nucleus-encoded factors on mRNA stabilization and translation in the chloroplast

Raynaud

Loiselay

Wostrikoff

et al. 2007

Proc. Natl. Acad. Sci. U.S.A.

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104

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A salient feature of organelle gene expression is the requirement for nucleus-encoded factors that act posttranscriptionally in a gene-specific manner. A central issue is to understand whether these factors are merely constitutive or have a regulatory function. In the unicellular alga Chlamydomonas reinhardtii, expression of the chloroplast petA gene-encoding cytochrome f, a major subunit of the cytochrome b 6f complex, depends on two specific nucleusencoded factors: MCA1, required for stable accumulation of the petA transcript, and TCA1, required for its translation. We cloned the TCA1 gene, encoding a pioneer protein, and transformed appropriate mutant strains with tagged versions of MCA1 and TCA1. In transformed strains expressing decreasing amounts of MCA1 or TCA1, the concentration of these factors proved limiting for petA mRNA accumulation and cytochrome f translation, respectively. This observation suggests that in exponentially growing cells, the abundance of MCA1 sets the pool of petA transcripts, some of which are TCA1-selected for an assembly-dependent translation of cytochrome f. We show that MCA1 is a short-lived protein. Its abundance varies rapidly with physiological conditions that deeply affect expression of the petA gene in vivo, for instance in aging cultures or upon changes in nitrogen availability. We observed similar but more limited changes in the abundance of TCA1. We conclude that in conditions where de novo biogenesis of cytochrome b 6f complexes is not required, a rapid drop in MCA1 exhausts the pool of petA transcripts, and the progressive loss of TCA1 further prevents translation of cytochrome f.

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“…Unassembled cytf could be shown to repress petA translation initiation, acting through the 5Ј untranslated region (9) and the cytf C-terminal domain (10). Analogous regulatory features were subsequently uncovered for the PS I subunits PsaA and PsaC (11) and the PS II subunits D1 and CP47 (12).…”

mentioning

confidence: 99%

Rubisco large-subunit translation is autoregulated in response to its assembly state in tobacco chloroplasts

Wostrikoff

Stern

2007

Proc. Natl. Acad. Sci. U.S.A.

Self Cite

112

102

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Plants rely on ribulose bisphosphate carboxylase/oxygenase (Rubisco) for carbon fixation. Higher plant Rubisco possesses an L8S8 structure, with the large subunit (LS) encoded in the chloroplast by rbcL and the small subunit encoded by the nuclear RBCS gene family. Because its components accumulate stoichiometrically but are encoded in two genetic compartments, rbcL and RBCS expression must be tightly coordinated. Although this coordination has been observed, the underlying mechanisms have not been defined. Here, we use tobacco to understand how LS translation is related to its assembly status. To do so, two transgenic lines deficient in LS biogenesis were created: a chloroplast transformant expressing a truncated and unstable LS polypeptide, and a line where a homolog of the maize Rubisco-specific chaperone, BSD2, was repressed by RNAi. We found that in both lines, LS translation is no longer regulated by the availability of small subunit (SS), indicating that LS translation is not activated by the presence of its assembly partner but, rather, undergoes an autoregulation of translation. Pulse labeling experiments indicate that LS is synthesized but not accumulated in the transgenic lines, suggesting that accumulation of a repressor motif is required for LS assemblydependent translational regulation.autoregulation ͉ gene expression ͉ synthesis ͉ plant M acromolecular organellar energetic complexes are essential and require assembly in defined stoichiometric ratios. Their biogenesis is complicated by their dual genetic origins, with subunits encoded both in the organelle and the nucleus. Prior studies led to the notion of concerted accumulation: the absence of one core subunit is accompanied by the loss of its assembly partners, as exemplified by mitochondrial mutants in yeast (1) or chloroplast mutants in Chlamydomonas (2). Two main mechanisms responsible for unassembled subunits' fate have been identified. The most common is rapid proteolytic degradation, and, in certain cases, substrates for specific chloroplast proteases have been identified (3-7). Alternatively, some chloroplastencoded proteins are subject to assembly-dependent translational regulation or control by epistasy of synthesis (CES) (8). The chloroplast uses CES in a hierarchical manner, whereas proteolysis is a relatively nonspecific mechanism for disposing of excess or incorrectly folded subunits.Insights into CES were first described for Chlamydomonas cytf, which is encoded by petA. Unassembled cytf could be shown to repress petA translation initiation, acting through the 5Ј untranslated region (9) and the cytf C-terminal domain (10). Analogous regulatory features were subsequently uncovered for the PS I subunits PsaA and PsaC (11) and the PS II subunits D1 and CP47 (12). Together, these results suggest that assemblydependent CES is a general feature of chloroplast gene expression in Chlamydomonas. However, its prevalence in higher plants is unclear.Here, we have used Rubisco assembly as a model to investigate whether CES occurs in higher plant...

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CytochromefTranslation in Chlamydomonas Chloroplast Is Autoregulated by its Carboxyl-Terminal Domain[W]

Cited by 75 publications

References 37 publications

A Conserved Mechanism Controls Translation of Rubisco Large Subunit in Different Photosynthetic Organisms

A Conserved Mechanism Controls Translation of Rubisco Large Subunit in Different Photosynthetic Organisms

Evidence for regulatory function of nucleus-encoded factors on mRNA stabilization and translation in the chloroplast

Rubisco large-subunit translation is autoregulated in response to its assembly state in tobacco chloroplasts

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