The fragmented mitochondrial ribosomal RNAs of Plasmodium falciparum have short A tails

Gillespie, Doreen E.; Salazar, Nelson A.; Rehkopf, David H.; Feagin, Jean E.

doi:10.1093/nar/27.11.2416

Cited by 46 publications

(36 citation statements)

References 36 publications

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“…For the coxI-III data set this concerns Scenedesums obliquus, since a parts of its coxIII gene had moved to the nucleus; Pylaiella littoralis and Laminaria digitata, since their coxII gene contains a large in frame insertion of unknown function (Secq et al 2001); and Acanthamoeba castellanii and Dictyostelium discoideum, because their coxI-II genes are represented by a single open reading frame only. For the ssu/lsu rRNA data all apicomplexans were excluded since their mitochondrial rRNAs genes are fragmented and encoded by a large number of incompletely characterized transcripts (Gillespie et al 1999).…”

Section: Methodsmentioning

confidence: 99%

Covariation of Mitochondrial Genome Size with Gene Lengths: Evidence for Gene Length Reduction During Mitochondrial Evolution

Schneider

Ebert

2004

J Mol Evol

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Abstract. Reduction of genome size and gene shortening have been observed in a number of parasitic and mutualistic intracellular symbionts. Reduction of coding capacity is also a unifying principle in the evolutionary history of mitochondria, but little is known about the evolution of gene length in mitochondria. The genes for cytochrome c oxidase subunits I-III, cytochrome b, and the large and small subunit rRNAs are, with very few exceptions, always found on the mitochondrial genome. These resident mitochondrial genes can therefore be used to test whether the reduction in gene lengths observed in a number of intracellular symbionts is also seen in mitochondria. Here we show that resident mitochondrial gene products are shorter than their corresponding counterparts in a-proteobacteria and, furthermore, that the reduction of mitochondrial genome size is correlated with a reduction in the length of the corresponding resident gene products. We show that relative genomic AT content, which has been identified as a factor influencing gene lengths in other systems, cannot explain gene length/ genome size covariance observed in mitochondria. Our data are therefore in agreement with the idea that gene length evolves as a consequence of selection for smaller genomes, either to avoid accumulation of deleterious mutations or triggered by selection for a replication advantage.

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Section: Methodsmentioning

confidence: 99%

Covariation of Mitochondrial Genome Size with Gene Lengths: Evidence for Gene Length Reduction During Mitochondrial Evolution

Schneider

Ebert

2004

J Mol Evol

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“…These are about 8 nucleotides (nt) long and predominantly found at the large rRNAs (29). Similarly, oligo(A) tracts were found at some RNA species of the fragmented rRNA in Plasmodium falciparum (12). While the function of the oligo(A) tails in yeast is still unclear, those in Plasmodium were suggested to protect these RNA fragments from exonucleolytic digestion.…”

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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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“…Fragmented genes exist in a variety of taxa, including other Alveolates [e.g., split ribosomal RNAs in Plasmodium and Theileria (9,10)]. However, rarely are they actually ''sewn'' back together at the level of DNA, to create a contiguous gene from all pieces.…”

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Evolution and assembly of an extremely scrambled gene

Landweber¹

2000

Proceedings of the National Academy of Sciences

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The process of gene unscrambling in hypotrichous ciliates represents one of nature's ingenious solutions to the problem of gene assembly. With some essential genes scrambled in as many as 51 pieces, these ciliates rely on sequence and structural cues to rebuild their fragmented genes and genomes. Here we report the complex pattern of scrambling in the DNA polymerase ␣ gene of Stylonychia lemnae. The germline (micronuclear) copy of this gene is broken into 48 pieces with 47 dispersed over two loci, with no asymmetry in the placement of coding segments on either strand. Direct repeats present at the boundaries between coding and noncoding sequences provide pointers to help guide assembly of the functional (macronuclear) gene. We investigate the evolution of this complex gene in three hypotrichous species.A ll ciliates possess two types of nuclei: an active somatic macronucleus and a germline micronucleus that contributes to sexual reproduction. The macronucleus forms from the micronucleus after cell mating, during the course of development. Prescott and colleagues discovered that the genomic copies of some protein-coding genes in the micronucleus of hypotrichous ciliates are encrypted in three ways (reviewed in ref. 1): (i) intervening non-protein-coding DNA segments [internal eliminated segments (IESs)] interrupt protein-coding DNA segments [macronuclear destined segments (MDSs)] and must be removed from the DNA during macronuclear development (2), (ii) the MDS order in 3 of 10 micronuclear genes is permuted relative to the chronological order in the macronuclear copy (1, 3), and (iii) these scrambled MDSs may be encoded in either orientation on the micronuclear DNA (Fig. 1). Some IESs may be remnants of transposons that lost their transposase and are now excised by a ciliate-specific mechanism for DNA rearrangements (2, 4). The total amount of DNA eliminated from the micronucleus is as great as 98% in Stylonychia (1), a dramatic reduction of noncoding DNA. These acrobatic genome rearrangements therefore present a potentially complicated cellular computational paradigm (5).Homologous recombination between short repeats at MDS-IES boundaries has been implicated as the likely mechanism of gene unscrambling, as it could simultaneously remove the IESs and reorder the MDSs (1). Typically, a short DNA sequence present at the boundary between MDS n and the downstream IES is repeated between MDS n ϩ 1 and its upstream IES, such that this sequence provides a pointer between MDS n and MDS n ϩ 1 at a distance (refs. 1, 6, and 7; Table 1), with one copy of the repeat retained in the macronucleus. However, the presence of such short direct repeats [average length of 4 bp between nonscrambled MDSs and 9 bp between scrambled MDSs (ref. 8; Table 1)] suggested that, although these pointers are necessary, they cannot be sufficient to direct accurate splicing and may play more of a role in structure than recognition. Otherwise, incorrectly spliced sequences (the results of promiscuous recombination) would dominate. This incorrect h...

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The fragmented mitochondrial ribosomal RNAs of Plasmodium falciparum have short A tails

Cited by 46 publications

References 36 publications

Covariation of Mitochondrial Genome Size with Gene Lengths: Evidence for Gene Length Reduction During Mitochondrial Evolution

Covariation of Mitochondrial Genome Size with Gene Lengths: Evidence for Gene Length Reduction During Mitochondrial Evolution

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

Evolution and assembly of an extremely scrambled gene

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