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Open Access Research article

Gene make-up: rapid and massive intron gains after horizontal transfer of a bacterial α-amylase gene to Basidiomycetes

Jean-Luc Da Lage1*, Manfred Binder2, Aurélie Hua-Van1, Štefan Janeček3 and Didier Casane14

Author Affiliations

1 Laboratoire Evolution, génomes et spéciation UPR 9034 CNRS, 91198 Gif-sur-Yvette, and Université Paris-Sud, Orsay, 91405, France

2 CBS Fungal Biodiversity Centre, Evolutionary Phytopathology, Institute of the Royal Netherlands Academy of Arts and Sciences (KNAW), Uppsalalaan 8, Utrecht, CT, 3584, The Netherlands

3 Laboratory of Protein Evolution, Institute of Molecular Biology, Slovak Academy of Science, Dubravska cesta 21, Bratislava, SK-84551, Slovakia

4 Université Paris Diderot, Sorbonne Paris Cité, France

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BMC Evolutionary Biology 2013, 13:40  doi:10.1186/1471-2148-13-40

Published: 13 February 2013

Abstract

Background

Increasing genome data show that introns, a hallmark of eukaryotes, already existed at a high density in the last common ancestor of extant eukaryotes. However, intron content is highly variable among species. The tempo of intron gains and losses has been irregular and several factors may explain why some genomes are intron-poor whereas other are intron-rich.

Results

We studied the dynamics of intron gains and losses in an α-amylase gene, whose product breaks down starch and other polysaccharides. It was transferred from an Actinobacterium to an ancestor of Agaricomycotina. This gene underwent further duplications in several species. The results indicate a high rate of intron insertions soon after the gene settled in the fungal genome. A number of these oldest introns, regularly scattered along the gene, remained conserved. Subsequent gains and losses were lineage dependent, with a majority of losses. Moreover, a few species exhibited a high number of both specific intron gains and losses in recent periods. There was little sequence conservation around insertion sites, then probably little information for splicing, whereas splicing sites, inside introns, showed typical and conserved patterns. There was little variation of intron size.

Conclusions

Since most Basidiomycetes have intron-rich genomes and this richness was ancestral in Fungi, long before the transfer event, we suggest that the new gene was shaped to comply with requirements of the splicing machinery, such as short exon and intron sizes, in order to be correctly processed.

Keywords:
Glycosyl hydrolase; Lateral gene transfer; Fungi; Gene duplication; Intron gain; Protosplice