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Open Access Research article

Multiple recent horizontal transfers of the cox1 intron in Solanaceae and extended co-conversion of flanking exons

Maria V Sanchez-Puerta1*, Cinthia C Abbona2, Shi Zhuo3, Eric J Tepe45, Lynn Bohs4, Richard G Olmstead6 and Jeffrey D Palmer3

Author Affiliations

1 Instituto de Ciencias Básicas, IBAM-CONICET and Facultad de Ciencias Agrarias, Universidad Nacional de Cuyo, Alte. Brown 500, Mendoza (5500), Argentina

2 IBAM-CONICET and Facultad de Ciencias Agrarias, Universidad Nacional de Cuyo, Alte. Brown 500, Mendoza (5500), Argentina

3 Department of Biology, Indiana University, 1001 E Third St., Bloomington (47405), USA

4 Department of Biology, University of Utah, 257 South 1400 East, Salt Lake City (84112), USA

5 Department of Biological Sciences, University of Cincinnati, Cincinnati (45221), USA

6 Department of Biology, University of Washington, Hitchcock Hall 423, Seattle (98195), USA

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BMC Evolutionary Biology 2011, 11:277  doi:10.1186/1471-2148-11-277

Published: 27 September 2011

Abstract

Background

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. 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.

Results

Although 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.

Conclusions

We 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.

Keywords:
horizontal gene transfer; cox1 intron; Solanaceae; mitochondrial DNA; homing endonuclease