Group I introns in the liverwort mitochondrial genome: the gene coding for subunit 1 of cytochrome oxidase shares five intron positions with its fungal counterparts

Ohta, Eiji; Oda, Kazuhiro; Yamato, Katsuyuki T.; Nakamura, Yasukazu; Takemura, Masashi; Nozato, Naoko; Akashi, Kinya; Ohyama, Kanji; Michel, François

doi:10.1093/nar/21.5.1297

Cited by 42 publications

(28 citation statements)

References 57 publications

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“…Consequently, the tRNA UAA Leu intron was likely present in the common ancestor of cyanobacteria and plastids before the endosymbiosis event. Inheritance of an ancient group I intron has also been proposed in other cases (3,26).…”

Section: Discussionmentioning

confidence: 99%

Origin and evolution of group I introns in cyanobacterial tRNA genes

et al. 1997

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Many tRNA UAALeu genes from plastids contain a group I intron. An intron is also inserted in the same gene at the same position in cyanobacteria, the bacterial progenitors of plastids, suggesting an ancient bacterial origin for this intron. A group I intron has also been found in the tRNA fMet gene of some cyanobacteria but not in plastids, suggesting a more recent origin for this intron. In this study, we investigate the phylogenetic distributions of the two introns among cyanobacteria, from the earliest branching to the more derived species. The phylogenetic distribution of the tRNA UAA Leu intron follows the clustering of rRNA sequences, being either absent or present in clades of closely related species, with only one exception in the Pseudanabaena group. Our data support the notion that the tRNA UAA Leu intron was inherited by cyanobacteria and plastids through a common ancestor. Conversely, the tRNA fMet intron has a sporadic distribution, implying that many gains and losses occurred during cyanobacterial evolution. Interestingly, a phylogenetic tree inferred from intronic sequences clearly separates the different tRNA introns, suggesting that each family has its own evolutionary history.Ever since their discovery, the origin of introns has been a subject of controversy. One view, the introns-late hypothesis, proposes that introns are recent invaders and that split genes arose by late insertion of introns into originally uninterrupted genes (28). In that scenario, horizontal transfer and transposition of introns are frequent events, accounting for the scattered phylogenetic distribution of introns. Although the debate has focused on spliceosomal introns, such a scenario could apply as well to other types of introns, some of which are known to be mobile (22). In contrast, the introns-early view implies that introns are very ancient, being present in the progenote (universal ancestor) (7). The demonstration that some members of group I and group II introns are capable of in vitro autocatalytic activity (19,29,39) lends further support to the presence of these introns at an early stage of evolution, maybe as early as the putative precellular RNA world (13). In such a scenario, the observed phylogenetic distribution of introns could be explained by multiple losses in different lineages during evolution (7) and by their mobility, which is assumed to be a derived feature (2). A major obstacle for the introns-early hypothesis was the apparent absence of introns in eubacteria, although this was tentatively rationalized by pressure to streamline the genome in rapidly dividing bacteria (7). Discovery of group I introns in bacteriophages of gram-positive and gram-negative bacteria did not help to resolve the issue, due to uncertainties concerning the origin of the bacteriophages themselves (see discussion in reference 35). The recent discovery of both group I and group II introns in divergent eubacteria (4,11,12,20,31,44) was acclaimed as a breakthrough by introns-early proponents. In most cases, however, the relatio...

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Section: Discussionmentioning

confidence: 99%

Origin and evolution of group I introns in cyanobacterial tRNA genes

et al. 1997

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“…A self-spficing group I intron displays functional similarities to corresponding introns from Podospora anserina, a filamentous fungus As outlined in a previous report, several group I introns residing in the cox 1 gene from P. wickerhamii show significant similarities to corresponding introns from Podospora anserina and M. polymorpha [84,57]. Under defined in vitro conditions several group I and group II introns can undergo self-splicing, without any trans-acting factors [18,65,81 ].…”

Section: Characterization Of a Putative Promoter Region Reveals A Seqmentioning

confidence: 81%

“…In the coxl gene from P. wiekerhamii there are three group I introns, which share structural features with counterparts from fungal and liverwort mitochondria [84,57].…”

Section: In Vitro Autocatalytic Splicing Of Two Group I Introns Residmentioning

confidence: 99%

Transcript mapping and processing of mitochondrial RNA in the chlorophyte alga Prototheca wickerhamii

Wolff

Kück

1996

Plant Mol Biol

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The detailed transcript map of the circular 55328 bp mitochondrial (mt) genome from the colourless chlorophycean alga Prototheca wickerhamii has been determined. On each half of this genome the genes are encoded only on one DNA strand, forming transcriptional units comprising variable numbers of genes. With the exception of four genes coding for ribosomal proteins, transcripts of the three rRNA genes and all protein-coding genes have been detected by both northern analysis and primer extension experiments. Polycistronic transcripts of protein coding and tRNA genes were verified by northern analyses, primer extension and RNAse mapping experiments. The 5' and 3' ends of different RNA species are often located in close proximity to putative stem-loop structures and some 5' termini of mRNAs coincide with the 3' end of tRNAs located immediately upstream. Transcript mapping in a putative promoter region revealed two different possible transcription initiation sites; no significant sequence homology to putative mt promoters from higher plants could be found. In addition, two out of three group I introns residing in the cox1 gene were found to be self-splicing in vitro under reaction conditions developed for related mt introns from a filamentous fungus. Mitochondrial gene expression of P. wickerhamii and of filamentous fungi has several features in common, such as intron splicing and the processing of longer polycistronic transcripts. The similarities in RNA maturation between higher-plant and P. wickerhamii mitochondria are less pronounced, since plants rarely use tRNAs as processing signals for their relatively short mitochondrial co-transcripts.

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“…Mitochondrial introns belong to the organelle specific group II (and in mosses also to group I) [25]. These have never been observed in nuclear genes and therefore presumably have to be eliminated.…”

Section: Functional Transfer By Rnamentioning

confidence: 99%

The mitochondrial genome on its way to the nucleus: different stages of gene transfer in higher plants

et al. 1993

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The vast majority of mltochondrial proteins are in all eukaryotes encoded in the nuclear genomes by genes which have been transferred from the original endosymbiont. DNA as well as RNA was and is exchanged between organelles. A functionally successful mformation transfer, however, requires complex structural and regulatory alterations of the concerned gene. The recently identified variations of the information content in mitochondrial genomes of different plant species represent different stages of the transfer process. These evolutionary intermediates allow a definition of requirements and chances of successful gene transfers.

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Group I introns in the liverwort mitochondrial genome: the gene coding for subunit 1 of cytochrome oxidase shares five intron positions with its fungal counterparts

Cited by 42 publications

References 57 publications

Origin and evolution of group I introns in cyanobacterial tRNA genes

Origin and evolution of group I introns in cyanobacterial tRNA genes

Transcript mapping and processing of mitochondrial RNA in the chlorophyte alga Prototheca wickerhamii

The mitochondrial genome on its way to the nucleus: different stages of gene transfer in higher plants

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