Explosive invasion of plant mitochondria by a group I intron

Abstract

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...

Horizontal transfer of an adaptive chimeric photoreceptor from bryophytes to ferns

“…In angiosperms, rampant HGTs have been documented for the mitochondrial cox1 homing intron. This intron is believed to have experienced one initial "seed transfer" from fungi that was followed by at least 80 incidents of plant-to-plant HGT among 833 diverse angiosperm species (23)(24)(25). Perhaps neochrome is similarly associated with mobile elements that may have facilitated its movement across species boundaries.…”

Linkage disequilibrium and phylogenetic congruence between chloroplast and mitochondrial haplotypes inSilene vulgaris

“…Digested DNA was electrophoresed on a 0.7% agarose gel and transferred to a Hybond N + membrane (Amersham Pharmacia, Buckinghamshire, UK) via a capillary blot. Approximately 1.5 kb of the coxI gene was PCR-ampli¢ed from S. vulgaris using primers coxIf82 (Bowe et al 2000) and coxIr1.6k (Cho et al 1998). This PCR product was radioactively labelled and hybridized to the total genomic blots overnight.…”

Site-specific selfish genes as tools for the control and genetic engineering of natural populations

“…Horizontal transmission between species has been demonstrated for HEGs in plant mitochondria and in yeast mitochondria and nuclei, and probably occurs in all taxa in which HEGs exist (Cho et al 1998; Proc. R. Soc.…”