Proteins are shared among RNA-protein complexes that form in the 5′ untranslated regions of spinach chloroplast mRNAs

Robida, Mark D.; Merhige, Patricia M.; Hollingsworth, Margaret J.

doi:10.1007/s00294-002-0283-1

Cited by 9 publications

(5 citation statements)

References 52 publications

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“…Based on cross-competition, it is likely that one editing factor is responsible for recognition of several sites, though our data do not exclude the possibility that particular editing factors exist that operate only on a single site. Binding of chloroplast proteins to 5Ј untranslated regions also exhibited cross-competition when assayed in gel shift experiments (24). Thus, the action of RNA-binding proteins on multiple sequences may not be unusual in plant organelle gene regulation.…”

Section: Discussionmentioning

confidence: 89%

Cross-Competition in Transgenic Chloroplasts Expressing Single Editing Sites Reveals SharedcisElements

Chateigner‐Boutin

Hanson

2002

Molecular and Cellular Biology

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RNA editing in organelles of angiosperm plants results in alteration of Cs to Us in transcripts. In most editing sites analyzed in vitro or in vivo, sequences within approximately 30 nucleotides (nt) 5 and 10 nt 3 of the edited C have been found to be required for selection of the correct C editing target and for editing efficiency, but no consensus sequences have been identified. The effect of high-level expression of two different minigenes carrying either the rpoB-2 or the ndhF-2 editing site on editing was determined for all 31 known edited Cs in two transgenic tobacco lines. The editing efficiencies of both the corresponding rpoB and ndhF editing sites in the endogenous genes' transcripts and in several other genes' transcripts were reduced in the chloroplast transgenic plants. Conserved nucleotides could be identified in the sequences immediately 5 of each overexpressed editing site and in the sites in the additional genes that experienced a competition effect, though the conserved nucleotides differ 5 of rpoB-2 and 5 of ndhF-2. Inspection of sequences surrounding chloroplast and mitochondrial editing sites reveals that they can be grouped into clusters which carry conserved nucleotides within 30 nt 5 of the C target of editing. The data are consistent with a model in which the same trans factor recognizes several chloroplast or mitochondrial editing sites, depending on the particular sequence 5 of the edited C.Transcripts of vascular plant chloroplast and mitochondrial genomes are modified by C-to-U RNA editing (3,10,17,26,29). Angiosperm chloroplasts typically contain 25 to 31 known editing sites (28), while 441 sites have been detected in mitochondria of Arabidopsis, the only vascular plant with a mitochondrial genome that has been completely sequenced (11). RNA editing in angiosperm chloroplasts usually results in alterations of the second codon position in coding regions, changing predicted amino acids (28). Mitochondria exhibit predominantly coding-region editing, but editing in noncoding regions and silent third codon positions is also observed. In both chloroplasts and mitochondria, there is a preference for a 5Ј pyrimidine and 3Ј purine next to the C target of editing (2).The requirements for chloroplast transcript editing have been probed in chloroplasts by introducing transgenes carrying sequences surrounding editing sites. Such experiments have established that 16 to 40 nucleotides immediately 5Ј and 6 to 20 nucleotides 3Ј are critical for editing. The amount of surrounding sequence required varies somewhat depending on the particular editing site. While 21 nucleotides surrounding the psbL editing site allowed efficient editing, 84 nucleotides surrounding two ndhB editing sites did not result in any transgene transcript editing (4). Though mitochondrial transformation is not yet possible, similar conclusions can be drawn by examining naturally occurring mitochondrial genomes which have undergone chance recombination events that have placed extra, truncated fragments of editing genes into coding...

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Section: Discussionmentioning

confidence: 89%

Cross-Competition in Transgenic Chloroplasts Expressing Single Editing Sites Reveals SharedcisElements

Chateigner‐Boutin

Hanson

2002

Molecular and Cellular Biology

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“…One possibility is that p50 is the homolog of the maize atp1 gene product. Specific chloroplast proteins were reported to bind to the atpE 5′-UTR as well as to the atpB 5′-UTR from spinach chloroplast mRNAs (52). Therefore, it is possible that a trans -acting factor(s) is also necessary for atpE translation.…”

Section: Discussionmentioning

confidence: 99%

The downstream atpE cistron is efficiently translated via its own cis-element in partially overlapping atpB–atpE dicistronic mRNAs in chloroplasts

Suzuki

Kuroda

Yukawa

et al. 2011

Nucleic Acids Research

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The chloroplast atpB and atpE genes encode subunits β and ε of the ATP synthase, respectively. They are co-transcribed as dicistronic mRNAs in flowering plants. An unusual feature is an overlap (AUGA) of the atpB stop codon (UGA) with the atpE start codon (AUG). Hence, atpE translation has been believed to depend on atpB translation (i.e. translational coupling). Using an in vitro translation system from tobacco chloroplasts, we showed that both atpB and atpE cistrons are translated from the tobacco dicistronic mRNA, and that the efficiency of atpB translation is higher than that of atpE translation. When the atpB 5′-UTR was replaced with lower efficiency 5′-UTRs, atpE translation was higher than atpB translation. Removal of the entire atpB 5′-UTR arrested atpB translation but atpE translation still proceeded. Introduction of a premature stop codon in the atpB cistron did not abolish atpE translation. These results indicate that atpE translation is independent of atpB translation. Mutation analysis showed that the atpE cistron possesses its own cis-element(s) for translation, located ~25 nt upstream from the start codon.

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“…These pre-mRNAs are generally processed into complex sets of overlapping transcripts including mono-, di-, and poly-cistronic mRNAs (3). Many nuclear-encoded proteins are involved in the mRNA processing as well as translation and mRNA stability (4)(5)(6). Translational control is the major step of chloroplast gene expression, and it is especially important for the stoichiometric production of individual subunits in photosynthetic complexes (7,8).…”

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confidence: 99%

Termination codon-dependent translation of partially overlapping ndhC-ndhK transcripts in chloroplasts

Yukawa

Sugiura

2008

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

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The chloroplast NAD(P)H dehydrogenase complex, a homologue of mitochondrial complex I, consists of >15 subunits, of which 11 are encoded by the chloroplast genome (ndhA-K). The ndhC and ndhK genes are partially overlapped and cotranscribed in many land plants. The downstream ndhK mRNA possesses 4 possible AUG initiation codons in many dicot plants. By using an efficient in vitro translation system from tobacco chloroplasts, we defined that the major initiation site of tobacco ndhK mRNAs is the third AUG that is located 4 nt upstream from the ndhC stop codon. Mutation of the ndhC stop codon (UAG) arrested translation of the ndhK cistron. Frameshift of the ndhC coding strand inhibited also translation of the distal cistron. The results indicated that ndhK translation depends on termination of the preceding cistron, namely translational coupling. Surprisingly, removal of the ndhC 5-UTR and its AUG still supported substantial translation of the ndhK cistron. This translation was abolished again by removing the ndhC stop codon. Although translation of the downstream cistron of an overlapping mRNA is generally very low, we found that the ndhC/K mRNA produces NdhK and NdhC in similar amounts. Based on subunit compositions of the bacterial complex I, the stoichiometry of NdhK and NdhC is suggested to be 1:1 in chloroplasts. To meet this stoichiometry, the ndhC/K mRNA is translated not only by a translational coupling event but also by a termination codondependent pathway.mRNA ͉ cistron ͉ initiation codon ͉ translational coupling

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Proteins are shared among RNA-protein complexes that form in the 5′ untranslated regions of spinach chloroplast mRNAs

Cited by 9 publications

References 52 publications

Cross-Competition in Transgenic Chloroplasts Expressing Single Editing Sites Reveals SharedcisElements

Cross-Competition in Transgenic Chloroplasts Expressing Single Editing Sites Reveals SharedcisElements

The downstream atpE cistron is efficiently translated via its own cis-element in partially overlapping atpB–atpE dicistronic mRNAs in chloroplasts

Termination codon-dependent translation of partially overlapping ndhC-ndhK transcripts in chloroplasts

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