Multiple recent horizontal transfers of the cox1intron in Solanaceae and extended co-conversion of flanking exons

Abstract

BackgroundThe most frequent case of horizontal transfer in plants involves a group I intron in the mitochondrial gene cox1, which has been acquired via some 80 separate plant-to-plant transfer events among 833 diverse angiosperms examined. This homing intron encodes an endonuclease thought to promote the intron's promiscuous behavior. A promising experimental approach to study endonuclease activity and intron transmission involves somatic cell hybridization, which in plants leads to mitochondrial fusion and genome recombination. However, the cox1 intron has not yet been found in the ideal group for plant somatic genetics - the Solanaceae. We therefore undertook an extensive survey of this family to find members with the intron and to learn more about the evolutionary history of this exceptionally mobile genetic element.ResultsAlthough 409 of the 426 species of Solanaceae examined lack the cox1 intron, it is uniformly present in three phylogenetically disjunct clades. Despite strong overall incongruence of cox1 intron phylogeny with angiosperm phylogeny, two of these clades possess nearly identical intron sequences and are monophyletic in intron phylogeny. These two clades, and possibly the third also, contain a co-conversion tract (CCT) downstream of the intron that is extended relative to all previously recognized CCTs in angiosperm cox1. Re-examination of all published cox1 genes uncovered additional cases of extended co-conversion and identified a rare case of putative intron loss, accompanied by full retention of the CCT.ConclusionsWe infer that the cox1 intron was separately and recently acquired by at least three different lineages of Solanaceae. The striking identity of the intron and CCT from two of these lineages suggests that one of these three intron captures may have occurred by a within-family transfer event. This is consistent with previous evidence that horizontal transfer in plants is biased towards phylogenetically local events. The discovery of extended co-conversion suggests that other cox1 conversions may be longer than realized but obscured by the exceptional conservation of plant mitochondrial sequences. Our findings provide further support for the rampant-transfer model of cox1 intron evolution and recommend the Solanaceae as a model system for the experimental analysis of cox1 intron transfer in plants.

The Chloroplast Genome of Hyoscyamus niger and a Phylogenetic Study of the Tribe Hyoscyameae (Solanaceae)

“…Furthermore, intron-containing solanaceous taxa also had an 18 nt-signature in the flanking region of exon 2 (named the co-conversion tract - CCT), presumably obtained by gene conversion during the process of intron homing [50]. The cox1 intron is highly mobile [51], [52] and has been horizontally transferred between two solanaceous lineages, Mandragora and Hyoscyameae [50].…”

Homologous recombination and retention of a single form of most genes shape the highly chimeric mitochondrial genome of a cybrid plant

“…That the group I intron acquired from Hn was successfully spliced in the cybrid is surprising in the context of the best-studied cognate of this intron, from yeast, whose splicing requires nuclear factors (Dujardin et al, 1982; Herbert et al, 1988). On the other hand, this intron is well-established to have been horizontally transferred hundreds if not thousands of times among angiosperm mitochondrial genomes (Cho et al, 1998; Sanchez-Puerta et al, 2008, 2011), which suggests that such factor(s) were widely present in plants before the evolutionary spread of this intron (presumably because it/they play some other, important role). Other differences in Hn-derived mitochondrial genes and/or newly-formed ORFs could be related to the cytoplasmic male sterility and other phenotypic characteristics observed in the cybrid Nt(+Hn) (Zubko et al, 2001).…”

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.…”