Evolution and Mechanism of Translation in Chloroplasts

Sugiura, Masahiro; Hirose, Tetsuro; Sugita, Mamoru

doi:10.1146/annurev.genet.32.1.437

Cited by 179 publications

(132 citation statements)

References 136 publications

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“…The chloroplast translation machinery resembles that in eubacteria in many respects (reviewed in Sugiura et al, 1998). Chloroplast ribosomes are similar to bacterial ribosomes in size and antibiotic sensitivities, and the sequences of many chloroplast ribosomal proteins are closely related to those of their prokaryotic ancestors.…”

Section: Introductionmentioning

confidence: 99%

A Nuclear Gene in Maize Required for the Translation of the Chloroplast atpB/E mRNA

McCormac¹,

Barkan²

1999

The Plant Cell

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To elucidate mechanisms that regulate chloroplast translation in land plants, we sought nuclear mutations in maize that disrupt the translation of subsets of chloroplast mRNAs. Evidence is presented for a nuclear gene whose function is required for the translation of the chloroplast atpB / E mRNA. A mutation in atp1 results in a failure to accumulate the chloroplast ATP synthase complex due to reduced synthesis of the AtpB subunit. This decrease in AtpB synthesis does not result from a change in atpB mRNA structure or abundance. Instead, the atpB mRNA is associated with abnormally few ribosomes in atp1-1 mutants, indicating that atp1 function is required during translation initiation or early in elongation. Previously, only one nuclear gene that is required for the translation of specific chloroplast mRNAs had been identified in a land plant. Thus, atp1 will be a useful tool for dissecting mechanisms of translational control in chloroplasts. INTRODUCTIONThe chloroplast translation machinery resembles that in eubacteria in many respects (reviewed in Sugiura et al., 1998). Chloroplast ribosomes are similar to bacterial ribosomes in size and antibiotic sensitivities, and the sequences of many chloroplast ribosomal proteins are closely related to those of their prokaryotic ancestors. Despite these similarities, there is increasing evidence that translation mechanisms in chloroplasts differ in several important ways from those in Escherichia coli. For example, chloroplast ribosomes include several proteins that do not have bacterial counterparts (Subramanian, 1993), Shine-Dalgarno sequences play a less prevalent role in chloroplast translation (Sakamoto et al., 1994; Hirose and Sugiura, 1996; Fargo et al., 1998), and the sequence of chloroplast start codons affects translational efficiency but plays only a minor role in positioning the start site (Chen et al., 1995). In addition, there is strong genetic evidence that chloroplast translation is commonly regulated by positively acting regulatory proteins (GoldschmidtClermont, 1998), which is a phenomenon that is rare in E. coli (McCarthy and Gualerzi, 1990).The translation of chloroplast mRNAs is regulated by a variety of factors. For example, light stimulates the translation of both the rbcL and psbA mRNAs (Malnoe et al., 1988;Berry et al., 1990;Staub and Maliga, 1993; Kim et al., 1994) and modulates the rates of both the initiation and elongation steps (Berry et al., 1988(Berry et al., , 1990 Kim et al., 1991; Edhofer et al., 1998). For psbA , this regulation is mediated in part by the 5 Ј untranslated region (UTR) of the mRNA (Staub and Maliga, 1993). Failure to synthesize one component of a photosynthetic complex can influence the translation of other subunits of the same complex: the chloroplast-encoded large subunit of ribulose bisphosphate carboxylase (Rubisco) is translated at reduced rates when synthesis of the nucleusencoded small subunit is disrupted (Khrebtukova and Spreitzer, 1996;Rodermel et al., 1996), and the rate of translation of the petA mRNA is ...

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Section: Introductionmentioning

confidence: 99%

A Nuclear Gene in Maize Required for the Translation of the Chloroplast atpB/E mRNA

McCormac¹,

Barkan²

1999

The Plant Cell

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“…This process can be subdivided into insertion͞deletion of nucleotides and base modification. RNA editing in plant organelles belongs to the latter case; specific sites of some transcripts are subject to C-to-U (and rarely U-to-C) conversions (2)(3)(4)(5)(6)(7). Most editing events occur in protein-coding regions and restore codons to conserved amino acids.…”

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confidence: 99%

A site-specific factor interacts directly with its cognate RNA editing site in chloroplast transcripts

Miyamoto

Obokata

Sugiura

2003

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

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RNA editing involves a variety of genetic systems and occurs by different mechanisms. In higher plant chloroplasts, specific sites of some transcripts are subject to C-to-U conversion. We have previously shown that site-specific trans-acting factors for psbE and petB mRNA editing bind corresponding cis-elements, which are located 5 nucleotides upstream from the editing site. Here we report that, by using mRNAs labeled either at the center of the upstream cis-element or at the editing site, the site-specific factors can be cross-linked with nucleotides at both positions. Mutations of nucleotides in the proximal region of the editing site revealed a correlation between editing activity and cross-linking efficiency of factors with the editing site, even though cross-linking with the upstream cis-element was unaffected. These observations suggest that the site-specific factor binds stably to the upstream ciselement, whereas it interacts weakly with the editing site. This finding raises the intriguing possibility that the site-specific factor is involved in both site-determination and C-to-U conversion in chloroplast RNA editing. R NA editing is one of the posttranscriptional processes involved in transcript maturation in a variety of organisms, including viruses, fungi, plants, and mammals (1). This process can be subdivided into insertion͞deletion of nucleotides and base modification. RNA editing in plant organelles belongs to the latter case; specific sites of some transcripts are subject to C-to-U (and rarely U-to-C) conversions (2-7). Most editing events occur in protein-coding regions and restore codons to conserved amino acids. In chloroplasts, editing of psbF, petB, and accD mRNAs has been reported to be necessary for the function of their products (8-10), indicating that at least some RNA editing events are essential posttranscriptional steps. However, one RNA editing event was observed in the third position of a codon and did not lead to amino acid substitution (11). Hence, at least one case of editing seems to have no biological significance.At present, 34 C-to-U editing sites have been found in tobacco chloroplast transcripts (12). Cis-analysis has been pursued for several sites by transplastomic approaches, and all defined cis-acting elements are located within Ϸ30 nucleotides of editing sites (13-15). Sequences surrounding editing sites exhibit no common characteristics, except most of the 5Ј neighboring residues of editing sites are pyrimidines and the 3Ј neighbors are A residues, both in chloroplast and mitochondrial transcripts (16,17). The importance of 5Ј neighbors for editing efficiency has been reported in psbL and ndhB mRNA (site V) editing (13,14).We have recently studied the mechanism of psbE and petB mRNA editing in tobacco and pea chloroplasts (18). Both chloroplast genes possess single editing sites that depend on plant species. The 72nd codon of psbE is encoded as Ser (UCU) at the DNA level in spinach, pea, and maize, whereas tobacco, Arabidopsis, and black pine restore this codon from Pro...

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“…1A). This would be at least an order of magnitude larger than has been described for any plastid genome (which range from 89 to 292 kb: Sugiura et al 1998). Moreover, a second-order rate plot of the reassociation data showed that the L-DNA of O. neapolitana was almost completely composed of single copy genes (Fig.…”

Section: Resultsmentioning

confidence: 76%

“…However, there is increasing evidence for a monophyletic origin of the rhodophyte and chlorophyte lineages, and possibly also the glaucocystophyte lineage (Burger et al 1999;Moreira et al 2000). The genomes of these plastids are typically 89-292 kb in size and the smaller ones among them usually lack an inverted repeat unit of the ribosomal rRNA genes (Sugiura et al 1998).…”

Section: Introductionmentioning

confidence: 99%

Plastid genome size and heterogeneous base composition of nuclear DNA from Ochrosphaera neapolitana (Prymnesiophyta)

et al. 2001

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Evolution and Mechanism of Translation in Chloroplasts

Cited by 179 publications

References 136 publications

A Nuclear Gene in Maize Required for the Translation of the Chloroplast atpB/E mRNA

A Nuclear Gene in Maize Required for the Translation of the Chloroplast atpB/E mRNA

A site-specific factor interacts directly with its cognate RNA editing site in chloroplast transcripts

Plastid genome size and heterogeneous base composition of nuclear DNA from Ochrosphaera neapolitana (Prymnesiophyta)

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