Organellar RNA Editing and Plant-Specific Extensions of Pentatricopeptide Repeat Proteins in Jungermanniid but not in Marchantiid Liverworts

Rüdinger, Mareike; Polsakiewicz, Monika; Knoop, Volker

doi:10.1093/molbev/msn084

Cited by 96 publications

(85 citation statements)

References 71 publications

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“…More precisely, the reported organelle editing factors are all members of the plant-specific E and DYW subclasses of the PPR family (Table 1), characterized by distinctive C-terminal domains O'Toole et al, 2008). The E (extended) domain is a degenerate motif with some similarities to PPR motifs, while the DYW domain, named for its typical AspTyr-Trp C-terminal tripeptide, is much more highly conserved, and its presence correlates phylogenetically with plant organelle RNA editing (Salone et al, 2007;Rudinger et al, 2008).…”

Section: Introductionmentioning

confidence: 99%

A Study of New Arabidopsis Chloroplast RNA Editing Mutants Reveals General Features of Editing Factors and Their Target Sites

et al. 2009

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RNA editing in higher plant organelles results in the conversion of specific cytidine residues to uridine residues in RNA. The recognition of a specific target C site by the editing machinery involves trans-acting factors that bind to the RNA upstream of the C to be edited. In the last few years, analysis of mutants affected in chloroplast biogenesis has identified several pentatricopeptide repeat (PPR) proteins from the PLS subfamily that are essential for the editing of particular RNA transcripts. We selected other genes from the same subfamily and used a reverse genetics approach to identify six new chloroplast editing factors in Arabidopsis thaliana (OTP80, OTP81, OTP82, OTP84, OTP85, and OTP86). These six factors account for nine editing sites not previously assigned to an editing factor and, together with the nine PPR editing proteins previously described, explain more than half of the 34 editing events in Arabidopsis chloroplasts. OTP80, OTP81, OTP85, and OTP86 target only one editing site each, OTP82 two sites, and OTP84 three sites in different transcripts. An analysis of the target sites requiring the five editing factors involved in editing of multiple sites (CRR22, CRR28, CLB19, OTP82, and OTP84) suggests that editing factors can generally distinguish pyrimidines from purines and, at some positions, must be able to recognize specific bases.

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Section: Introductionmentioning

confidence: 99%

A Study of New Arabidopsis Chloroplast RNA Editing Mutants Reveals General Features of Editing Factors and Their Target Sites

et al. 2009

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“…An exception may be the P class protein PPR596, which when disabled increases editing at several mitochondrial sites (24). The distinctive plant-specific C-terminal DYW domain of most of these proteins correlates phylogenetically with plant organelle RNA editing (25,26). These PPR proteins are thought to play the role of trans-acting specificity factors in the current model of RNA editing in plant organelles.…”

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The Pentatricopeptide Repeat Protein OTP87 Is Essential for RNA Editing of nad7 and atp1 Transcripts in Arabidopsis Mitochondria

Hammani

Francs‐Small

Takenaka

et al. 2011

Journal of Biological Chemistry

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In plant organelles, RNA editing is a post-transcriptional mechanism that converts specific cytidines to uridines in RNA of both mitochondria and plastids, altering the information encoded by the gene. The cytidine to be edited is determined by a cis-element surrounding the editing site that is specifically recognized and bound by a trans-acting factor. All the trans-acting editing factors identified so far in plant organelles are members of a large protein family, the pentatricopeptide repeat (PPR) proteins. We have identified the Organelle Transcript Processing 87 (OTP87) gene, which is required for RNA editing of the nad7-C24 and atp1-C1178 sites in Arabidopsis mitochondria. OTP87 encodes an E-subclass PPR protein with an unusually short E-domain. The recombinant protein expressed in Escherichia coli specifically binds to RNAs comprising 30 nucleotides upstream and 10 nucleotides downstream of the nad7-C24 and atp1-C1178 editing sites. The loss-of-function of OTP87 results in small plants with growth and developmental delays. In the otp87 mutant, the amount of assembled respiratory complex V (ATP synthase) is highly reduced compared with the wild type suggesting that the amino acid alteration in ATP1 caused by loss of editing at the atp1-C1178 site affects complex V assembly in mitochondria.In flowering plants, RNA editing comprises conversion of specific cytidine residues to uridine in both mitochondrial and plastid transcripts. RNA editing occurs most frequently in coding regions of mRNAs, with only few sites found in structural RNAs and introns. In Arabidopsis thaliana, more than 500 sites are edited in mitochondrial transcripts whereas 34 sites are affected in chloroplasts (1-4). The mechanism of plant RNA editing has been extensively studied since the late 1980s, but the identity of the enzyme catalyzing the editing reaction remains unknown. Genetic studies have identified nuclear encoded factors required for the editing of one or more specific cytidines in mitochondrial or chloroplast transcripts of Arabidopsis plants (5-21). All of these protein factors are pentatricopeptide repeat (PPR) 6 proteins, a large family of over 450 RNA-binding proteins in Arabidopsis, the majority of which are thought to be targeted to mitochondria or chloroplasts (22,23). All of the organelle editing factors reported to be required for editing of specific sites are members of the E and DYW subclasses of the PPR family. An exception may be the P class protein PPR596, which when disabled increases editing at several mitochondrial sites (24). The distinctive plant-specific C-terminal DYW domain of most of these proteins correlates phylogenetically with plant organelle RNA editing (25,26). These PPR proteins are thought to play the role of trans-acting specificity factors in the current model of RNA editing in plant organelles. In this model, a protein trans-factor specifically binds a cis-element in the vicinity of the editing site, facilitating the access of a putative RNA editing enzyme (27,28). The proof that these genetica...

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“…The rate of editing in seed plant chloroplast genomes is over an order of magnitude lower (Tillich et al 2006). Outside seed plants, the moss Physcomitrella patens has only 11 edited sites in the mitochondrial genome, and the liverwort Marchantia polymorpha appears to have lost RNA editing altogether (Rü dinger et al 2008(Rü dinger et al , 2009). In contrast, other bryophytes, lycophytes, and ferns exhibit frequent mitochondrial editing (Malek et al 1996;Grewe et al 2009;Li et al 2009), while the only two nonseed plant chloroplast genomes examined (from one hornwort and one fern) also have high levels of editing (Kugita et al 2003;Wolf et al 2004).…”

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Extensive Loss of RNA Editing Sites in Rapidly Evolving Silene Mitochondrial Genomes: Selectionvs. Retroprocessing as the Driving Force

et al. 2010

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Theoretical arguments suggest that mutation rates influence the proliferation and maintenance of RNA editing. We identified RNA editing sites in five species within the angiosperm genus Silene that exhibit highly divergent mitochondrial mutation rates. We found that mutational acceleration has been associated with rapid loss of mitochondrial editing sites. In contrast, we did not find a significant difference in the frequency of editing in chloroplast genes, which lack the mutation rate variation observed in the mitochondrial genome. As found in other angiosperms, the rate of substitution at RNA editing sites in Silene greatly exceeds the rate at synonymous sites, a pattern that has previously been interpreted as evidence for selection against RNA editing. Alternatively, we suggest that editing sites may experience higher rates of C-to-T mutation than other portions of the genome. Such a pattern could be caused by gene conversion with reverse-transcribed mRNA (i.e., retroprocessing). If so, the genomic distribution of RNA editing site losses in Silene suggests that such conversions must be occurring at a local scale such that only one or two editing sites are affected at a time. Because preferential substitution at editing sites appears to occur in angiosperms regardless of the mutation rate, we conclude that mitochondrial rate accelerations within Silene have ''fast-forwarded'' a preexisting pattern but have not fundamentally changed the evolutionary forces acting on RNA editing sites.

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Organellar RNA Editing and Plant-Specific Extensions of Pentatricopeptide Repeat Proteins in Jungermanniid but not in Marchantiid Liverworts

Cited by 96 publications

References 71 publications

A Study of New Arabidopsis Chloroplast RNA Editing Mutants Reveals General Features of Editing Factors and Their Target Sites

A Study of New Arabidopsis Chloroplast RNA Editing Mutants Reveals General Features of Editing Factors and Their Target Sites

The Pentatricopeptide Repeat Protein OTP87 Is Essential for RNA Editing of nad7 and atp1 Transcripts in Arabidopsis Mitochondria

Extensive Loss of RNA Editing Sites in Rapidly Evolving Silene Mitochondrial Genomes: Selectionvs. Retroprocessing as the Driving Force

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