Site-specific DNA endonuclease and RNA maturase activities of two homologous intron-encoded proteins from yeast mitochondria

Delahodde, Agnès; Goguel, Valérie; Bécam, A.‐M.; Creusot, Francine; Perea, Javier; Banroques, Josette; Jacq, Claude

doi:10.1016/0092-8674(89)90246-8

Cited by 179 publications

(126 citation statements)

References 42 publications

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“…The finding that the C terminus of I-AniI is necessary and sufficient for maturase activity is consistent with "domain" swapping experiments with the S. cerevisiae bI4 maturase and wild-type aI4␣ endonuclease that share extensive amino acid conservation (Delahodde et al 1989). The analysis of hybrid proteins in vivo showed that while an N-terminal aI4␣/C-terminal bI4 protein has robust RNA maturase activity, an N-terminal bI4/C-terminal aI4␣ protein has only weak maturase activity (Goguel et al 1992).…”

Section: Structural Requirements For Other Maturasessupporting

confidence: 65%

A C-terminal fragment of an intron-encoded maturase is sufficient for promoting group I intron splicing

Downing

Brady²,

Caprara³

2005

RNA

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Group I introns often encode proteins that catalyze site-specific DNA hydrolysis. Some of these proteins have acquired the ability to promote splicing of their cognate intron, but whether these two activities reside in different regions of the protein remains obscure. A crystal structure of I-AniI, a dual function intron-encoded protein, has shown that the protein has two pseudo-symmetric domains of equal size. Each domain contacts its DNA substrate on either side of two cleavage sites. As a first step to identify the RNA binding surface, the N-and C-terminal domains of I-AniI were separately expressed and tested for promoting the splicing of the mitochondrial (mt) COB pre-RNA. The N-terminal protein showed no splicing activation or RNA binding, suggesting that this domain plays a minimal role in activity or is improperly folded. Remarkably, the 16-kDa C-terminal half facilitates intron splicing with a rate similar to that of the full-length protein. Both the C-terminal fragment and full-length proteins bind tightly to the COB intron. RNase footprinting shows that the C-terminal and full-length proteins bind to the same regions and induce the same conformational changes in the COB intron. Together, these results show that the C-terminal fragment of I-AniI is necessary and sufficient for maturase activity and suggests that I-AniI acquired splicing function by utilizing a relatively small protein surface that likely represents a novel RNA binding motif. This fragment of I-AniI represents the smallest group I intron splicing cofactor described to date.

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Section: Structural Requirements For Other Maturasessupporting

confidence: 65%

A C-terminal fragment of an intron-encoded maturase is sufficient for promoting group I intron splicing

Downing

Brady²,

Caprara³

2005

RNA

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“…All 30 introns contain a Ϸ270-bp core region typical of group I introns (1-3) interrupted by and partially overlapping with a Ϸ834-bp ORF. The inferred protein from this ORF is about 52% identical over 229 residues with the yeast cox1 aI4 intronic protein, which encodes site-specific DNA endonuclease and RNA maturase activities (4,5,24).…”

Section: Resultsmentioning

confidence: 99%

Explosive invasion of plant mitochondria by a group I intron

Cho

Qiu

Kuhlman

et al. 1998

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

258

204

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Group I introns are mobile, self-splicing genetic elements found principally in organellar genomes and nuclear rRNA genes. The only group I intron known from mitochondrial genomes of vascular plants is located in the cox1 gene of Peperomia, where it is thought to have been recently acquired by lateral transfer from a fungal donor. Southern-blot surveys of 335 diverse genera of land plants now show that this intron is in fact widespread among angiosperm cox1 genes, but with an exceptionally patchy phylogenetic distribution. Four lines of evidence-the intron's highly disjunct distribution, many incongruencies between intron and organismal phylogenies, and two sources of evidence from exonic coconversion tracts-lead us to conclude that the 48 angiosperm genera found to contain this cox1 intron acquired it by 32 separate horizontal transfer events. Extrapolating to the over 13,500 genera of angiosperms, we estimate that this intron has invaded cox1 genes by cross-species horizontal transfer over 1,000 times during angiosperm evolution. This massive wave of lateral transfers is of entirely recent occurrence, perhaps triggered by some key shift in the intron's invasiveness within angiosperms.Many group I introns encode site-specific endonucleases that catalyze their efficient spread from intron-containing to intronless alleles of the same gene in genetic crosses (1-3). This process, termed intron ''homing,'' has been observed for introns located in a variety of mitochondrial (mt) and chloroplast genes (4-7), in nuclear rRNA genes of the slime mold Physarum (8), and in protein genes of T-even phage (9). Homing is initiated by the intron-encoded endonuclease, which makes a staggered double-strand break at its target site within a recipient intronless allele, and is thought to then proceed by the double-strand-break repair pathway (10).The evolutionary importance of intron homing to the spread of group I introns across species barriers has been unclear, as relatively few cases of the horizontal transfer of group I introns between identical genomic sites of nonmating organisms are documented (11-17). Most of these cases involve the same genome and species belonging to the same phylum, usually fungi (11-13). Two notable exceptions are the transfer of two group I introns between identical sites of rRNA genes located in the chloroplast of a Chlamydomonas-type green alga and the mitochondrion of an Acanthamoeba-like ameboid (15).The only group I intron known from vascular plant mt genomes (which contain many group II introns) is also thought to have been acquired by homing-mediated horizontal transfer from a distantly related organism. This intron is present in the cox1 (cytochrome oxidase subunit 1) gene of the angiosperm Peperomia (16, 17) at the same location as related introns in the nonvascular plant Marchantia, the green alga Prototheca, the slime mold Dictyostelium, and several diverse fungi (see ref. 18 and references therein). This cox1 intron is thought to have been recently acquired by Peperomia, most likel...

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“…The putative Var1 protein, involved in the protein translation machinery, is less conserved than the putative Cox3 and Cob proteins of the energy transfer complexes. Despite the small mitochondrial genome size, we also identi¢ed a new putative mitochondrial group I intron open reading frame (ORF) whose closest homologue is I-SceII [16]. Until now, only one putative intronic meganuclease from K. thermotolerans had been identi¢ed by sequence similarity with I-SceI [8,9].…”

Section: Mitochondrial Dnamentioning

confidence: 99%

Genomic Exploration of the Hemiascomycetous Yeasts: 10.Kluyveromyces thermotolerans

et al. 2000

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A genomic exploration of Kluyveromyces thermotolerans was performed by random sequence tag (RST) analysis. We sequenced 2653 RSTs corresponding to inserts sequenced from both ends. We performed a systematic comparison with a complete set of proteins from Saccharomyces cerevisiae, other completely sequenced genomes and SwissProt. We identified six mitochondrial genes and 1358^1496 nuclear genes by comparison with S. cerevisiae. In addition, 25 genes were identified by comparison with other organisms. This corresponds to about 24% of the estimated gene content of this organism. A lower level of conservation is observed with orthologues to genes of S. cerevisiae previously classified as orphans. Gene order was found to be conserved between S. cerevisiae and K. thermotolerans in 56.5% of studied cases. ß

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Site-specific DNA endonuclease and RNA maturase activities of two homologous intron-encoded proteins from yeast mitochondria

Cited by 179 publications

References 42 publications

A C-terminal fragment of an intron-encoded maturase is sufficient for promoting group I intron splicing

A C-terminal fragment of an intron-encoded maturase is sufficient for promoting group I intron splicing

Explosive invasion of plant mitochondria by a group I intron

Genomic Exploration of the Hemiascomycetous Yeasts: 10.Kluyveromyces thermotolerans

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