RNA editing in tobacco chloroplasts leads to the formation of a translatable psbL mRNA by a C to U substitution within the initiation codon.

Kudla, Jörg; Igloi, Gabor L.; Metzlaff, Michael; Hagemann, Rudolf; Kössel, Hans

doi:10.1002/j.1460-2075.1992.tb05149.x

Cited by 121 publications

(80 citation statements)

References 30 publications

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“…The phenylalanine residue restored at editing site I is conserved even in the IRF170-encoded homolog of the more distantly related cyanobacterium Syn- echocystis. Previously, the ACG-to-ATG codon transition has been observed for the restoration of initiating methionine codons (3,4). With editing site II this transition is now also observed for the restoration of an internal methionine codon.…”

Section: Resultsmentioning

confidence: 85%

“…More recently, editing has been detected as an additional step of chloroplast mRNA maturation (3)(4)(5)(6)(7). This process was originally observed in mitochondrial transcripts of trypanosomes (8,9) but was subsequently also found in nuclear-encoded transcripts of mammals (10) and in mitochondrial transcripts of plants (11)(12)(13) and of the acellular slime mold Physarum (14).…”

Section: Introductionmentioning

confidence: 97%

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Complete RNA editing of unspliced and dicistronic transcripts of the intron-containing reading frame IRF170 from maize chloroplasts.

Ruf

Zeltz

Kössel

1994

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

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The maize plastome harbors within the rps4-rpsl4 gene cluster the reading frame IRF170, which is interrupted by two introns. Although the function of the encoded peptide of 170 amino acids is not known, the conservation of IRF170 homologs in other plastomes is a strong indication that IRF170 is a functional gene. Amplification and sequence analyses ofIRF170 specific cDNAs reveals two C-to-U editing events occurring within each of the first two exons. This situation allows an analysis of the temporal order between editing and splicing of a chloroplast transcript. By using intron-specific primer combinations, cDNAs derived from partially or even uuspliced IRF170 transcripts could be amplfied which in all cases showed complete editing. Complete editing was also observed with a cDNA derived from a transcript in which the proximal rps4 and the 5' half of IRF170-encoded sequences were still linked. This demonstrates that editing of the IRF170 transcript is an early processing step preceding both splicing and cleavage to monocistronic mRNA.The primary transcripts encoded by chloroplast protein genes are known to undergo a series of processing steps such as splicing, cleavage to monocistronic mRNAs, and trimming of terminal sequences (1, 2). More recently, editing has been detected as an additional step of chloroplast mRNA maturation (3-7). This process was originally observed in mitochondrial transcripts of trypanosomes (8, 9) but was subsequently also found in nuclear-encoded transcripts of mammals (10) and in mitochondrial transcripts of plants (11-13) and of the acellular slime mold Physarum (14). Depending on the different types of editing processes, the genetic information transmitted to the primary transcripts of the respective genes can be altered by nucleotide insertions and deletions (8,9,14) or by base substitutions (10-13). The editing events observed in chloroplast transcripts so far all result in C-to-U transitions, thereby restoring codons for conserved amino acid residues of the respective peptides (3-7).The reading frame designated IRF170 is subdivided by two introns and is well conserved within the rps4-rpsl4 gene cluster of the plastomes of higher plants (ref. 15; see Fig. 1), whereas a homologous reading frame without introns could be identified in the cyanobacterium Synechocystis (16). Although the function of the encoded peptide, consisting in maize of 170 amino acids, is not known, the absence of an IRF170 homolog in the plastome of the nonphotosynthetic parasitic plant Epifagus (17) as well as differences in the processing of IRF170 transcripts between amyloplasts and chloroplasts from maize (18) appears to suggest a function as a component of the photosynthetic apparatus. This supposition is further supported by the codon usage of IRF170-encoded mRNAs (15) and by the existence of a cyanobacterial IRF170 homolog (16).The existence of a large primary transcript which includes sequences of the flanking genes of the rps4-rpsl4 gene cluster and the presence of two introns in the IRF170-enco...

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Section: Resultsmentioning

confidence: 85%

Section: Introductionmentioning

confidence: 97%

Complete RNA editing of unspliced and dicistronic transcripts of the intron-containing reading frame IRF170 from maize chloroplasts.

Ruf

Zeltz

Kössel

1994

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

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“…When genomic and cDNA sequences of the mitochondrial coxIll coding region from these algae were compared, no 5 difference was observed. Thus RNA editing is not involved in expression of this gene and may be absent entirely from mitochondria of these algae.…”

Section: And Unpublished Results)mentioning

confidence: 96%

“…In both organelles specific cytidines of the primary transcripts are altered to uridines in the mature mRNAs. Only a few instances of editing have been found in chloroplasts (4)(5)(6), whereas numerous editing events have been documented in mitochondria of higher plants for almost all mRNAs investigated (7)(8)(9)(10)(11). In the more thoroughly investigated higher plant species, all of the open reading frames encoding conserved functional polypeptides appear to be edited to some extent and the total number of editing sites documented amounts to 294 in wheat (11) and to >400 in Oenothera (10).…”

mentioning

confidence: 98%

Evidence for RNA editing in mitochondria of all major groups of land plants except the Bryophyta.

Hiesel

Combettes

Brennicke

1994

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

109

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RNA editing has been documented in mitochondria of higher plants, notably dicots and monocots. To determine the distribution of mitochondrial RNA editing in the plant kingdom, we have now undertaken a survey of evolutionarily distant plants. RNA editing occurs in all major groups of land plants except the Bryophyta, suggesting that this process is an ancient trait that was established before the radiation of kormophyte plants. No editing is observed in representatives of the green algae, suggesting that editing arose in early land plants after the split of the Bryophyta or has been lost selectively in both algae and mosses. In ferns several U -* C changes are observed, one of which eliminates a genomically encoded UAA termination codon and creates a functional open reading frame.RNA editing has been observed in mitochondria and chloroplasts of angiosperm plants belonging to the Dicotyledonae and Monocotyledonae (1-3). In both organelles specific cytidines of the primary transcripts are altered to uridines in the mature mRNAs. Only a few instances of editing have been found in chloroplasts (4-6), whereas numerous editing events have been documented in mitochondria of higher plants for almost all mRNAs investigated (7-11). In the more thoroughly investigated higher plant species, all of the open reading frames encoding conserved functional polypeptides appear to be edited to some extent and the total number of editing sites documented amounts to 294 in wheat (11) and to >400 in Oenothera (10). The observed effect ofthis extensive editing on the encoded polypeptide sequences suggests that many of the higher plant mitochondrial genes would not encode functionally competent products without appropriate "correction" by RNA editing.Mitochondrial RNA editing has been reported in a number of angiosperm species, including the monocots wheat and maize and the dicots Oenothera, Sorghum, Petunia, Daucus, and Arabidopsis (7-11). The observation of analogous RNA editing in both monocots and dicots suggests that the origin of this process predates the divergence of the two lineages and is generally present in angiosperms. Recently, RNA editing has also been described in the gymnosperm Thuja (12). However, none of the plant species presumed to be closer to the evolutionary origin of flowering plants has been investigated. The only mitochondrial sequence data available allowing any inference about the need of RNA editing in nonflowering plants are from two bryophytes.Analysis of protein sequences deduced from the complete genomic nucleotide sequence of the liverwort Marchantia polymorpha (13) and comparison of several cDNA and genomic DNA sequences (14) did not show any evidence of RNA editing. Genomic sequence analysis of a mitochondrial gene in the moss Physcomitrella patens (15) allows a similar deduction, suggesting that RNA editing might not occur in mitochondria of the two bryophytes.The publication costs of this article were defrayed in part by page charge payment. This article must therefore be hereby marked "adve...

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“…Post-transcriptional modification of plant organellar mRNAs by RNA editing is required for maintenance of functional protein sequences (1)(2)(3) and also for the introduction of translation initiation codons in particular transcripts (4,5). Typically, chloroplast genomes of higher land plants have on the order of 30 -40 editing sites, whereas mitochondria generally have greater than 400 (6 -12).…”

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confidence: 99%

Cross-competition in Editing of Chloroplast RNA Transcripts in Vitro Implicates Sharing of Trans-factors between Different C Targets

Heller

Hayes

Hanson

2008

Journal of Biological Chemistry

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C 3 U plant organellar RNA editing is required for the translation of evolutionarily conserved and functional proteins. 28 different C targets of RNA editing have been identified in maize chloroplasts, and hundreds of Cs are edited in mitochondria. Mutant analysis in Arabidopsis has indicated that absence of a single site-specific recognition protein can result in loss of editing of a single C target, raising the possibility that each C target requires a recognition protein. Here we show that transcripts encompassing two editing sites, ZMrpoB C467 and ZMrps14 C80, can compete editing activity from each other in vitro despite limited sequence similarity. The signal causing competition overlaps a 5 -cis element required for editing efficiency. A single five-nucleotide mutation spanning the region from ؊20 to ؊16 relative to the edited C of rpoB C467 is sufficient to eliminate its substrate editing as well as its ability to compete editing activity from rps14 C80 substrates. A corresponding mutation in an rps14 C80 competitor likewise eliminated its ability to compete editing activity from rpoB C467 substrates. Taken together, our results indicate that the RNA sequences mediating both editing efficiency and cross-competition are highly similar and that a common protein is involved in their editing. Sharing of trans-factors can facilitate editing of the large number of different C targets in plant organelles so that a different protein factor would not be required for every editing site.Post-transcriptional modification of plant organellar mRNAs by RNA editing is required for maintenance of functional protein sequences (1-3) and also for the introduction of translation initiation codons in particular transcripts (4, 5). Typically, chloroplast genomes of higher land plants have on the order of 30 -40 editing sites, whereas mitochondria generally have greater than 400 (6 -12). To date, 28 cytidine-to-uridine editing sites have been identified in 15 chloroplast transcripts in maize (12, 13), all of which alter the encoded amino acid, except one site in the 5Ј-untranslated region of ndhG.It is currently believed that the plant organellar RNA editing machinery consists of two distinct components: the ciselement, which uniquely identifies a given editing site by its sequence and structure within the transcript itself, and the trans-acting factors, which are likely to be proteins that recognize the cis-element and catalyze the editing reaction (14). The sequences surrounding all editing sites in a given organism do not show obvious similarity to each other either by direct sequence alignment or by secondary structure prediction. However, transplastomic tobacco that overexpress a fragment of maize rpoB or tobacco ndhF transcripts spanning the rpoB C467 or ndhF C290 editing sites, respectively, showed reduced editing at the cognate tobacco sites, as well as at additional sites (15), indicating that at least some ciselements are related. These three editing sites therefore form a "cluster" affected by overexpression of transc...

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RNA editing in tobacco chloroplasts leads to the formation of a translatable psbL mRNA by a C to U substitution within the initiation codon.

Cited by 121 publications

References 30 publications

Complete RNA editing of unspliced and dicistronic transcripts of the intron-containing reading frame IRF170 from maize chloroplasts.

Complete RNA editing of unspliced and dicistronic transcripts of the intron-containing reading frame IRF170 from maize chloroplasts.

Evidence for RNA editing in mitochondria of all major groups of land plants except the Bryophyta.

Cross-competition in Editing of Chloroplast RNA Transcripts in Vitro Implicates Sharing of Trans-factors between Different C Targets

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