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

Maria V Sanchez-Puerta,Eric J Tepe,Lynn Bohs,Cinthia C Abbona,Richard G Olmstead,Jeffrey D Palmer,Shi Zhuo

doi:10.1186/1471-2148-11-277

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.

Highlights

The 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
Intron presence-absence and phylogeny PCR was used to assess the presence/absence of an intron at the one site, near the middle of the cox1 gene, in which all previously described cases of introns in this gene in angiosperms have been found. This approach was facilitated by the conserved length (953-1,031 bp) of this intron in angiosperms [9,12], as well as by the generally highly conserved nature of plant mitochondrial sequences owing to very low rates of synonymous substitutions [34,35,36]
We will let past studies (by our group ([9,10,12] and by others [8,11]) and, importantly, the results presented in the current study stand in rebuttal of Cusimano et al.’s untenable claim that phylogenetic analyses of the cox1 intron “are largely congruent with known phylogenetic relationships” and that the only phylogenetic “finding suggestive of horizontal cox1 intron transfer” is poorly supported and instead best explained by vertical transmission

Summary

Introduction

The most frequent case of horizontal transfer in plants involves a group I intron in the mitochondrial gene cox, 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 notable case of HGT in plant mitochondria involves a “homing” group I intron present in the mitochondrial cox gene of many disparately related lineages of angiosperms. A region of converted exonic sequence is called a “coconversion tract” (CCT)

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