Translational Regulation in the Chloroplast

Danon, Avihai

doi:10.1104/pp.115.4.1293

Cited by 67 publications

(45 citation statements)

References 29 publications

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“…In the chloroplast itself, rates of photosynthesis are adjusted by posttranslational modification of proteins (Buchanan et al, 1994;Wollman, 2001;Aro and Ohad, 2003), by structural reorganization of the photosynthetic protein complexes (Niyogi, 1999), and by metabolic regulation within and downstream of the Calvin cycle (Paul and Pellny, 2003). Moreover, the expression of plastome-encoded photosynthetic genes is regulated by transcriptional (Pfannschmidt et al, 1999;Pfannschmidt and Liere, 2005), posttranscriptional (Deng and Gruissem, 1987;Rochaix, 2001), and translational (Danon, 1997;Choquet and Wollman, 2002) mechanisms. In addition, plastid-to-nucleus (retrograde) signaling modulates the expression of nuclear genes coding for photosynthetic proteins (Leister, 2005).…”

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confidence: 99%

Nuclear Photosynthetic Gene Expression Is Synergistically Modulated by Rates of Protein Synthesis in Chloroplasts and Mitochondria

et al. 2006

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Arabidopsis thaliana mutants prors1-1 and -2 were identified on the basis of a decrease in effective photosystem II quantum yield. Mutations were localized to the 59-untranslated region of the nuclear gene PROLYL-tRNA SYNTHETASE1 (PRORS1), which acts in both plastids and mitochondria. In prors1-1 and -2, PRORS1 expression is reduced, along with protein synthesis in both organelles. PRORS1 null alleles (prors1-3 and -4) result in embryo sac and embryo development arrest. In mutants with the leaky prors1-1 and -2 alleles, transcription of nuclear genes for proteins involved in photosynthetic light reactions is downregulated, whereas genes for other chloroplast proteins are upregulated. Downregulation of nuclear photosynthetic genes is not associated with a marked increase in the level of reactive oxygen species in leaves and persists in the dark, suggesting that the transcriptional response is light and photooxidative stress independent. The mrpl11 and prpl11 mutants are impaired in the mitochondrial and plastid ribosomal L11 proteins, respectively. The prpl11 mrpl11 double mutant, but neither of the single mutants, resulted in strong downregulation of nuclear photosynthetic genes, like that seen in leaky mutants for PRORS1, implying that, when organellar translation is perturbed, signals derived from both types of organelles cooperate in the regulation of nuclear photosynthetic gene expression.

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Section: Introductionmentioning

confidence: 99%

Nuclear Photosynthetic Gene Expression Is Synergistically Modulated by Rates of Protein Synthesis in Chloroplasts and Mitochondria

et al. 2006

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“…The general consensus is that most native primary transcripts require processing to be functional (Barkan, 1988;Zerges, 2000;Meierhoff et al, 2003) and that posttranscriptional RNA processing of primary transcripts represents an important control of chloroplast gene expression (Hashimoto et al, 2003;Nickelsen, 2003). However, it is believed that more than one pathway may be involved in transcript processing (Danon, 1997;Choquet and Wollman, 2002).For example, several studies have shown that the regulation of gene expression in the chloroplast relies more on RNA stability than on transcriptional regulation (Deng and Gruissem, 1987;Jiao et al, 2004). In chloroplast, such stability is mainly influenced by the presence of 5# untranslated regions, or UTRs (Eibl et al, 1999;Zou et al, 2003), nucleus-encoded factors (Lezhneva and Meurer, 2004), and 3#UTRs (Adams and Stern, 1990;Chen and Stern, 1991), without which rapid degradation or low accumulation of primary transcripts has been observed.…”

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Characterization of Heterologous Multigene Operons in Transgenic Chloroplasts. Transcription, Processing, and Translation

2005

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The first characterization of transcriptional, posttranscriptional, and translational processes of heterologous operons expressed via the tobacco (Nicotiana tabacum) chloroplast genome is reported here. Northern-blot analyses performed on chloroplast transgenic lines harboring seven different heterologous operons revealed that polycistronic mRNA was the predominant transcript produced. Despite the lack of processing of such polycistrons, large amounts of foreign protein accumulation was observed in these transgenic lines, indicating abundant translation of polycistrons. This is supported by polysome fractionation assays, which allowed detection of polycistronic RNA in lower fractions of the sucrose gradients. These results show that the chloroplast posttranscriptional machinery can indeed detect and translate multigenic sequences that are not of chloroplast origin. In contrast to native transcripts, processed and unprocessed heterologous polycistrons were stable, even in the absence of 3# untranslated regions (UTRs). Unlike native 5#UTRs, heterologous secondary structures or 5#UTRs showed efficient translational enhancement independent of cellular control. Abundant read-through transcripts were observed in the presence of chloroplast 3#UTRs but they were efficiently processed at introns present within the native operon. Heterologous genes regulated by the psbA (the photosystem II polypeptide D1) promoter, 5# and 3#UTRs have greater abundance of transcripts than the endogenous psbA gene because transgenes were integrated into the inverted repeat region. Addressing questions about polycistrons, and the sequences required for their processing and transcript stability, are essential in chloroplast metabolic engineering. Knowledge of such factors would enable engineering of foreign pathways independent of the chloroplast complex posttranscriptional regulatory machinery.Plastid genes in higher plants are mainly organized as operons, of which more than 60 have been described in the tobacco (Nicotiana tabacum) chloroplast genome (Sugita and Sugiura, 1996). These may group genes of related or unrelated functions, the former being the most common (Barkan, 1988;Rochaix, 1996). Most of these genes are transcribed into polycistronic precursors that may be later processed and modified to render the transcripts competent for translation (Eibl et al., 1999;Barkan and Goldschmidt-Clermont, 2000;Monde et al., 2000b).The processing mechanisms for translation regulation in chloroplast genes of higher plants are still largely unknown. The general consensus is that most native primary transcripts require processing to be functional (Barkan, 1988;Zerges, 2000;Meierhoff et al., 2003) and that posttranscriptional RNA processing of primary transcripts represents an important control of chloroplast gene expression (Hashimoto et al., 2003;Nickelsen, 2003). However, it is believed that more than one pathway may be involved in transcript processing (Danon, 1997;Choquet and Wollman, 2002).For example, several studies have shown that the regul...

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“…Plastids are plant cellular organelles that have their own genome and a prokaryotic-type transcription and translation machinery (Rochaix, 1996;Sugita and Sugiura, 1996;Danon, 1997;Stern et al, 1997;Bruick and Mayfield, 1999;Hess and Bö rner, 1999). In prokaryotes translation is facilitated by mRNA-rRNA interactions between the Shine-Dalgarno (SD) sequence upstream of the translation initiation codon and the anti-Shine-Dalgarno sequence (ASD) at the 3Ј end of the small (16S) ribosomal RNA.…”

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Sequences Downstream of the Translation Initiation Codon Are Important Determinants of Translation Efficiency in Chloroplasts

2001

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The objective of this study was to determine if mRNA sequences downstream of the translation initiation codon are important for translation of plastid mRNAs. We have employed a transgenic approach, measuring accumulation of the neomycin phosphotransferase (NPTII) reporter enzyme translationally fused with 14 N-terminal amino acids encoded in the rbcL or atpB plastid genes. NPTII accumulation from wild-type and mutant rbcL and atpB segments was compared. We report that silent mutations in the rbcL segment reduced NPTII accumulation 35-fold. In contrast, mutations in the atpB mRNA reduced NPTII accumulation only moderately from approximately 7% (w/w) to approximately 4% (w/w) of the total soluble cellular protein, indicating that the importance of sequences downstream of the translation initiation codon are dependent on the individual mRNA. Information provided here will facilitate transgene design for high-level expression of recombinant proteins in chloroplasts by translational fusion with the N-terminal segment of highly expressed plastid genes or by introduction of silent mutations in the N-terminal part of the coding region.Plastids are plant cellular organelles that have their own genome and a prokaryotic-type transcription and translation machinery

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Translational Regulation in the Chloroplast

Cited by 67 publications

References 29 publications

Nuclear Photosynthetic Gene Expression Is Synergistically Modulated by Rates of Protein Synthesis in Chloroplasts and Mitochondria

Nuclear Photosynthetic Gene Expression Is Synergistically Modulated by Rates of Protein Synthesis in Chloroplasts and Mitochondria

Characterization of Heterologous Multigene Operons in Transgenic Chloroplasts. Transcription, Processing, and Translation

Sequences Downstream of the Translation Initiation Codon Are Important Determinants of Translation Efficiency in Chloroplasts

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