Spinach plastid genes coding for initiation factor IF-1, ribosomal protein S11 and RNA polymerase  -subunit

Sijben-Müller, G; Hallick, Richard B.; Alt, Juliane; Westhoff, Peter; Herrmann, Reinhold G.

doi:10.1093/nar/14.2.1029

Cited by 136 publications

(60 citation statements)

References 41 publications

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“…During evolution, the majority of the cyanobacterial genes were lost or transferred to the nucleus of the host cell, while several genes mainly required for photosynthesis and gene expression were retained in the organellar genome (Kleine et al, 2009). The plastid genome (plastome) contains functional rpo genes coding for homologs of the cyanobacterial RNA polymerase subunits a, b, b', and b'', which form the core of the plastid-encoded plastid RNA polymerase (PEP; Ohyama et al, 1986;Shinozaki et al, 1986;Sijben-Mü ller et al, 1986;Hajdukiewicz et al, 1997;Liere et al, 2011). Nuclear-encoded sigma factors interact with PEP to confer promoter recognition (Liu and Troxler, 1996;Tanaka et al, 1996Tanaka et al, , 1997Schweer et al, 2010;Lerbs-Mache, 2011).…”

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confidence: 99%

The Primary Transcriptome of Barley Chloroplasts: Numerous Noncoding RNAs and the Dominating Role of the Plastid-Encoded RNA Polymerase

et al. 2012

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Gene expression in plastids of higher plants is dependent on two different transcription machineries, a plastid-encoded bacterial-type RNA polymerase (PEP) and a nuclear-encoded phage-type RNA polymerase (NEP), which recognize distinct types of promoters. The division of labor between PEP and NEP during plastid development and in mature chloroplasts is unclear due to a lack of comprehensive information on promoter usage. Here, we present a thorough investigation into the distribution of PEP and NEP promoters within the plastid genome of barley (Hordeum vulgare). Using a novel differential RNA sequencing approach, which discriminates between primary and processed transcripts, we obtained a genome-wide map of transcription start sites in plastids of mature first leaves. PEP-lacking plastids of the albostrians mutant allowed for the unambiguous identification of NEP promoters. We observed that the chloroplast genome contains many more promoters than genes. According to our data, most genes (including genes coding for photosynthesis proteins) have both PEP and NEP promoters. We also detected numerous transcription start sites within operons, indicating transcriptional uncoupling of genes in polycistronic gene clusters. Moreover, we mapped many transcription start sites in intergenic regions and opposite to annotated genes, demonstrating the existence of numerous noncoding RNA candidates.

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Section: Introductionmentioning

confidence: 99%

The Primary Transcriptome of Barley Chloroplasts: Numerous Noncoding RNAs and the Dominating Role of the Plastid-Encoded RNA Polymerase

et al. 2012

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“…The initiation of translation in organelles is thought to be similar to that in E. coli , although much less is known about the organelle systems (Pel and Grivell, 1994;Yu and Spremulli, 1998). The gene for chloroplast IF1 was first reported by Sijben-Müller et al (1986) from spinach cpDNA. Chloroplast IF2 and IF3 proteins, encoded by nuclear genes, have been characterized in Euglena gracilis (Ma and Spremulli, 1992;Lin et al, 1994), and candidate nuclear genes for chloroplast IF2 and IF3 are present in the Arabidopsis nuclear genome sequence.…”

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Many Parallel Losses of infA from Chloroplast DNA during Angiosperm Evolution with Multiple Independent Transfers to the Nucleus

et al. 2001

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We used DNA sequencing and gel blot surveys to assess the integrity of the chloroplast gene infA , which codes for translation initiation factor 1, in Ͼ 300 diverse angiosperms. Whereas most angiosperms appear to contain an intact chloroplast infA gene, the gene has repeatedly become defunct in ‫ف‬ 24 separate lineages of angiosperms, including almost all rosid species. In four species in which chloroplast infA is defunct, transferred and expressed copies of the gene were found in the nucleus, complete with putative chloroplast transit peptide sequences. The transit peptide sequences of the nuclear infA genes from soybean and Arabidopsis were shown to be functional by their ability to target green fluorescent protein to chloroplasts in vivo. Phylogenetic analysis of infA sequences and assessment of transit peptide homology indicate that the four nuclear infA genes are probably derived from four independent gene transfers from chloroplast to nuclear DNA during angiosperm evolution. Considering this and the many separate losses of infA from chloroplast DNA, the gene has probably been transferred many more times, making infA by far the most mobile chloroplast gene known in plants. INTRODUCTIONMany genes have been lost from the chloroplast genome during plant and algal evolution. Most of these losses occurred in the murky interval between the original endosymbiosis of a cyanobacterium (with perhaps 2000 proteincoding genes) and the last common ancestor of all existing chloroplast genomes (with ‫ف‬ 210 protein-coding genes; . Many other genes were lost during the early evolution of photosynthetic eukaryotes, often in parallel in different algal lineages, and some of these losses were the result of gene transfers to the nuclear genome . During the evolution of land plants, relatively few changes occurred to the set of genes found in chloroplast DNA (cpDNA) Palmer and Delwiche, 1998). Nonetheless, the most recent changes are likely to provide the most information about the evolutionary mechanisms involved.Among the six completely sequenced chloroplast genomes from angiosperms (excluding the nonphotosynthetic plant Epifagus virginiana ; Wolfe et al., 1992a), 74 proteincoding genes are held in common and an additional five are present in only some species. These five genes are accD , ycf1 , and ycf2 (pseudogenes in rice and maize; Hiratsuka et al., 1989;Maier et al., 1995), rpl23 (pseudogene in spinach; Thomas et al., 1988), and infA (pseudogene in tobacco, Arabidopsis, and Oenothera elata ; Shinozaki et al., 1986;Wolfe et al., 1992b;Sato et al., 1999; Hupfer et al., 2000). Other chloroplast gene losses in angiosperms that have been confirmed by sequencing include rpl22 , rps16 , and ycf4 (open reading frame 184), all of which have been lost in 1 To whom correspondence should be addressed. E-mail (in Dublin) khwolfe@tcd.ie; fax 353-1-6798558. 646The Plant Cell some or all legumes (Gantt et al., 1991;Nagano et al., 1991; Doyle et al., 1995; K.H. Wolfe, unpublished data), and ycf2 and ndhF , both of which have been lost ...

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“…The infA gene is transcribed by two promoters to yield two sizes of monocistronic mRNAs both ending at the same terminator (8). Recently, homologous genes have been identified in Bacillus subtilis and in the chloroplasts of several plants (4,23,28). The high degree of homology indicates that IF1 is a conserved protein and suggests that it plays an important role in the cell.…”

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Translation initiation factor IF1 is essential for cell viability in Escherichia coli

Cummings

Hershey

1994

J Bacteriol

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Translation initiation factor IF1 is a highbly conserved element of the prokaryotic translational apparatus. It has been demonstrated earlier that the factor stimulates in vitro the initiation phase of protein synthesis. However, no mutation in its gene, infA, has been identified, and a role for IF1 in translation has not been demonstrated in vivo. To elucidate the function of IFi and determine if the protein is essential for cell growth, the chromosomal copy of infA was disrupted. Cell viability is maintained only when infA is expressed in trans from a plasmid, thereby demonstrating that WI1 is essential for cell growth in Escherichia coli. Cells depleted of IF1 exhibit few polsomes, suggesting that IFI functions in the initiation phase of protein synthesis.Initiation of protein synthesis in prokaryotes involves formation of a 30S preinitiation complex in which fMet-tRNA interacts with the initiation codon of an mRNA bound to the surface of the 30S ribosomal subunit. The efficiency and fidelity of formation of the 30S preinitiation complex is promoted by three initiation factors; IF1, IF2, and IF3. The properties and mechanism of action of the initiation factors have been reviewed recently (13). All three initiation factors bind to the 30S ribosomal subunit in the absence of other translational components. IF2 binds GTP and fMet-tRNAf, thereby ensuring that the tRNA bound to the 30S subunit is the initiator tRNA, fMet-tRNAf. 1F3 plays at least two roles: it acts as an antiassociation factor to maintain the ribosomal subunits in a dissociated state, and it promotes the selection of the initiator fMet-tRNA by monitoring the tRNA anticodon stem-loop region and the correctness of the anticodon-initiator codon interaction on the ribosome. The function of IF1 is less clear, since no specific role has yet been assigned to this protein.IF1 is the smallest of the initiation factors (Mr,8,100) and consists of 71 amino acid residues. The gene for IF1, infA, has been cloned, sequenced, and mapped to about 20 min on the Escherichia coli chromosome (25). The infA gene is transcribed by two promoters to yield two sizes of monocistronic mRNAs both ending at the same terminator (8). Recently, homologous genes have been identified in Bacillus subtilis and in the chloroplasts of several plants (4,23,28). The high degree of homology indicates that IF1 is a conserved protein and suggests that it plays an important role in the cell. However, our knowledge of the function of IF1 comes exclusively from a number of in vitro assays for translation. IF1 enhances the rates of 70S ribosome dissociation and subunit association but does not change the equilibrium position (10). It alone binds poorly to 30S ribosomal subunits, but when added with IF2 both factor-binding affinities are increased (32). IF1 stimulates IF2-dependent fMet-tRNAf binding to 30S or 70S ribosomes in the presence of mRNA. However, the best demonstration that IF1 truly functions in protein synthesis comes from the observation that ,-galactosidase synthesis in a DNA-l...

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Spinach plastid genes coding for initiation factor IF-1, ribosomal protein S11 and RNA polymerase -subunit

Cited by 136 publications

References 41 publications

The Primary Transcriptome of Barley Chloroplasts: Numerous Noncoding RNAs and the Dominating Role of the Plastid-Encoded RNA Polymerase

The Primary Transcriptome of Barley Chloroplasts: Numerous Noncoding RNAs and the Dominating Role of the Plastid-Encoded RNA Polymerase

Many Parallel Losses of infA from Chloroplast DNA during Angiosperm Evolution with Multiple Independent Transfers to the Nucleus

Translation initiation factor IF1 is essential for cell viability in Escherichia coli

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