Transcript termini of messenger RNAs in higher plant mitochondria

Schuster, W.; Hiesel, Rudolf; Isaac, Peter G.; Leaver, C. J.; Brennicke, Axel

doi:10.1093/nar/14.15.5943

Cited by 88 publications

(34 citation statements)

References 19 publications

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“…Sequencing of 10 cDNA clones obtained from both amplification reactions revealed poly(A) tracts attached at positions ϩ5, ϩ4, and ϩ3 immediately downstream of the double stem-loop structure. These polyadenylation sites are consistent with previously mapped 3Ј ends (26). Only a single clone indicated a polyadenylation site at position Ϫ3 within the downstream part of the second stem (Fig.…”

Section: Potential Poly(a) Tracts In Oenothera Atp1supporting

confidence: 91%

Transcript Lifetime Is Balanced between Stabilizing Stem-Loop Structures and Degradation-Promoting Polyadenylation in Plant Mitochondria

2001

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To determine the influence of posttranscriptional modifications on 3 end processing and RNA stability in plant mitochondria, pea atp9 and Oenothera atp1 transcripts were investigated for the presence and function of 3 nonencoded nucleotides. A 3 rapid amplification of cDNA ends approach initiated at oligo(dT)-adapter primers finds the expected poly(A) tails predominantly attached within the second stem or downstream of the double stem-loop structures at sites of previously mapped 3 ends. Functional studies in a pea mitochondrial in vitro processing system reveal a rapid removal of the poly(A) tails up to termini at the stem-loop structure but little if any influence on further degradation of the RNA. In contrast 3 poly(A) tracts at RNAs without such stem-loop structures significantly promote total degradation in vitro. To determine the in vivo identity of 3 nonencoded nucleotides more accurately, pea atp9 transcripts were analyzed by a direct anchor primer ligation-reverse transcriptase PCR approach. This analysis identified maximally 3-nucleotide-long nonencoded extensions most frequently of adenosines combined with cytidines. Processing assays with substrates containing homopolymer stretches of different lengths showed that 10 or more adenosines accelerate RNA processivity, while 3 adenosines have no impact on RNA life span. Thus polyadenylation can generally stimulate the decay of RNAs, but processivity of degradation is almost annihilated by the stabilizing effect of the stem-loop structures. These antagonistic actions thus result in the efficient formation of 3 processed and stable transcripts.Control of the amount of translatable mRNA is a common parameter to regulate gene expression in many organisms. The available quantity of an RNA depends largely on the rate of synthesis and/or posttranscriptional processes which control the stability of a transcript by preventing it from degradation. Such posttranscriptional processes have been studied in prokaryotes and different subcellular compartments of eukaryotic cells. In spite of the many variations, some common features behind these processes emerge in all organisms and systems. These include the involvement of mRNA secondary structures and 3Ј polyadenylation of RNA. While organized RNA secondary structures generally support transcript stabilization, polyadenylation has opposing functions in eukaryotes and prokaryotes.In the nucleus of eukaryotic cells, pre-mRNAs are polyadenylated at 3Ј ends that have been generated by endonucleolytic cleavages. These poly(A) tails play important roles in translation initiation and mRNA export from the nucleus and also have a major function in stabilizing mRNAs (27). A completely different function has been attributed to polyadenylation in prokaryotes, where the degradation of mRNA is stimulated by the presence of 3Ј poly(A) tracts (4). The degradation-promoting effect of polyadenylation was even found in transcripts, which were otherwise protected and stabilized by stem-loop structures (3). A similar effect has also been ob...

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Section: Potential Poly(a) Tracts In Oenothera Atp1supporting

confidence: 91%

Transcript Lifetime Is Balanced between Stabilizing Stem-Loop Structures and Degradation-Promoting Polyadenylation in Plant Mitochondria

2001

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“…In plant mitochondria, a number of transcripts terminate in inverted repeat sequences, which can be folded, at least in theory, to form hairpin structures with varying loop sizes (Schuster et al 1986). Usually two unrelated elements are found in tandem, suggesting that this double feature may be important for recognition by the respective trans-factor(s).…”

Section: Rna Stabilitymentioning

confidence: 99%

Gene expression in plant mitochondria: transcriptional and post–transcriptional control

Binder

Brennicke

2003

Phil. Trans. R. Soc. Lond. B

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114

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The informational content of the mitochondrial genome in plants is, although small, essential for each cell. Gene expression in these organelles involves a number of distinct transcriptional and post-transcriptional steps. The complex post-transcriptional processes of plant mitochondria such as 59 and 39 RNA processing, intron splicing, RNA editing and controlled RNA stability extensively modify individual steady-state RNA levels and influence the mRNA quantities available for translation. In this overview of the processes in mitochondrial gene expression, we focus on confirmed and potential sites of regulatory interference and discuss the evolutionary origins of the transcriptional and post-transcriptional processes.

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“…For instance, no proteins involved in these processes have been formally identified, although several candidate genes have now been identified since the completion of the nuclear genome sequence of Arabidopsis thaliana. Stable secondary structures can be predicted at the 3Ј-extremities of some but not all plant mitochondrial mRNAs (12). When present, these structures appear to be involved in stabilizing the transcripts (13)(14)(15) and in the correct processing of 3Ј-extremities rather than being signals for transcription termination (15).…”

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confidence: 98%

Plant Mitochondrial Polyadenylated mRNAs Are Degraded by a 3′- to 5′-Exoribonuclease Activity, Which Proceeds Unimpeded by Stable Secondary Structures

Gagliardi¹,

Perrin²,

Maréchal-Drouard³

et al. 2001

Journal of Biological Chemistry

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Recently, we and others have reported that mRNAs may be polyadenylated in plant mitochondria, and that polyadenylation accelerates the degradation rate of mRNAs. To further characterize the molecular mechanisms involved in plant mitochondrial mRNA degradation, we have analyzed the polyadenylation and degradation processes of potato atp9 mRNAs. The overall majority of polyadenylation sites of potato atp9 mRNAs is located at or in the vicinity of their mature 3-extremities. We show that a 3-to 5-exoribonuclease activity is responsible for the preferential degradation of polyadenylated mRNAs as compared with non-polyadenylated mRNAs, and that 20 -30 adenosine residues constitute the optimal poly(A) tail size for inducing degradation of RNA substrates in vitro. The addition of as few as seven non-adenosine nucleotides 3 to the poly(A) tail is sufficient to almost completely inhibit the in vitro degradation of the RNA substrate. Interestingly, the exoribonuclease activity proceeds unimpeded by stable secondary structures present in RNA substrates. From these results, we propose that in plant mitochondria, poly(A) tails added at the 3 ends of mRNAs promote an efficient 3-to 5-degradation process.The control of mRNA stability constitutes an important aspect of the regulation of gene expression in all organisms. Polyadenylation of mRNAs is involved in the control of mRNA stability, however, with two significantly different roles depending on the organism or subcellular compartment concerned. Polyadenylation is required for stabilizing virtually all nuclear-encoded mRNAs in all eukaryotes. In contrast, polyadenylation targets mRNAs for degradation in eubacteria (1, 2), chloroplasts (3-6), plant mitochondria (7-9), and trypanosome mitochondria (10). In eubacteria and chloroplasts, degradation of mRNAs is initiated by endonucleolytic cleavages. The resulting fragments are then degraded by 3Ј-to 5Ј-exonuclease activities (1, 5). In both systems, polyadenylation targets endonucleolytic cleavage products for rapid degradation. In chloroplasts, structured mature 3Ј ends are poor substrates for polyadenylation as compared with the internal RNA fragments generated by endonuclease(s) (5, 6).In plant mitochondria, molecular mechanisms involved in mRNA stability or degradation are still poorly understood (11). For instance, no proteins involved in these processes have been formally identified, although several candidate genes have now been identified since the completion of the nuclear genome sequence of Arabidopsis thaliana. Stable secondary structures can be predicted at the 3Ј-extremities of some but not all plant mitochondrial mRNAs (12). When present, these structures appear to be involved in stabilizing the transcripts (13-15) and in the correct processing of 3Ј-extremities rather than being signals for transcription termination (15). Mature 3Ј termini of plant mitochondria mRNAs are generated by 3Ј-processing of longer pre-mRNA molecules (15), and stable mature mRNAs are not constitutively polyadenylated at their 3Ј-extremit...

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Transcript termini of messenger RNAs in higher plant mitochondria

Cited by 88 publications

References 19 publications

Transcript Lifetime Is Balanced between Stabilizing Stem-Loop Structures and Degradation-Promoting Polyadenylation in Plant Mitochondria

Transcript Lifetime Is Balanced between Stabilizing Stem-Loop Structures and Degradation-Promoting Polyadenylation in Plant Mitochondria

Gene expression in plant mitochondria: transcriptional and post–transcriptional control

Plant Mitochondrial Polyadenylated mRNAs Are Degraded by a 3′- to 5′-Exoribonuclease Activity, Which Proceeds Unimpeded by Stable Secondary Structures

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