Fungal origin by horizontal transfer of a plant mitochondrial group I intron in the chimeric coxI gene of Peperomia

Abstract

We present phylogenetic evidence that a group I intron in an angiosperm mitochondrial gene arose recently by horizontal transfer from a fungal donor species. A 1,716-bp fragment of the mitochondrial coxI gene from the angiosperm Peperomia polybotrya was amplified via the polymerase chain reaction and sequenced. Comparison to other coxI genes revealed a 966-bp group I intron, which, based on homology with the related yeast coxI intron aI4, potentially encodes a 279-amino-acid site-specific DNA endonuclease. This intron, which is believed to function as a ribozyme during its own splicing, is not present in any of 19 coxI genes examined from other diverse vascular plant species. Phylogenetic analysis of intron origin was carried out using three different tree-generating algorithms, and on a variety of nucleotide and amino acid data sets from the intron and its flanking exon sequences. These analyses show that the Peperomia coxI gene intron and exon sequences are of fundamentally different evolutionary origin. The Peperomia intron is more closely related to several fungal mitochondrial introns, two of which are located at identical positions in coxI, than to identically located coxI introns from the land plant Marchantia and the green alga Prototheca. Conversely, the exon sequence of this gene is, as expected, most closely related to other angiosperm coxI genes. These results, together with evidence suggestive of co-conversion of exonic markers immediately flanking the intron insertion site, lead us to conclude that the Peperomia coxI intron probably arose by horizontal transfer from a fungal donor, using the double-strand-break repair pathway. The donor species may have been one of the symbiotic mycorrhizal fungi that live in close obligate association with most plants.

Explosive invasion of plant mitochondria by a group I intron

“…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).…”

“…18 and references therein). This cox1 intron is thought to have been recently acquired by Peperomia, most likely from a fungal donor, based on (i) its singular presence in Peperomia among 25 genera of vascular plants examined, (ii) its closer phylogenetic relationship to fungal introns than to those of the green ''plants'' Marchantia and Prototheca, and (iii) the presence of exonic signatures of homing-mediated coconversion immediately downstream of the Peperomia intron (16,17).We now show that Peperomia is only the tip of a large iceberg: there has been an explosive and recent wave of horizontal transfers of this intron into cox1 genes of many different lineages of flowering plants. We surveyed over 300 diverse land plants and infer that, based on phylogenetic and molecular criteria, 32 separate transfers account for the intron's presence in 48 disparate genera of angiosperms.…”

“…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)(12)(13)(14)(15)(16)(17). Most of these cases involve the same genome and species belonging to the same phylum, usually fungi (11)(12)(13).…”

Post-transcriptional Regulation in Mitochondria of Rice and Wheat at Low Temperatures

“…Mitochondrial group I intron has been identified in cox1 of several angiosperm species 10 . The origin of the cox1 intron may be fungi, while the ancestral intron is believed to have been horizontally transferred from the donor organism 10,78 . No other group I intron has been identified in the vascular plant mitochondrial genome, however, considering the horizontally transferred origin of the cox1 intron, it is possible that another example will be found.…”

Complete Sequence of the Mitochondrial DNA of the Red Alga Porphyra purpurea: Cyanobacterial Introns and Shared Ancestry of Red and Green Algae

“…Several ORF-containing group I and II introns have been shown to be mobile elements in the sense that in genetic crosses, they invade intronless copies of the genes in which they are inserted (Dujon et al, 1986;Skelly et al, 1991). This has led to the inference in a number of cases that introns are also able to spread laterally between unrelated species, and between genomes from different cellular compartments (e.g., Lang et al, 1985;Lonergan and Gray, 1994;Turmel et al, 1995;Vaughn et al, 1995;Cho et al, 1998). In the case of P. purpurea, cyanobacterial introns might have invaded mitochondria via chloroplasts that inherited their introns directly from a cyanobacterial ancestor.…”