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

Da Lage JL, Binder M, Hua-Van A, Janeček S, Casane D - BMC Evol. Biol. (2013)

Bottom Line: The results indicate a high rate of intron insertions soon after the gene settled in the fungal genome.There was little variation of intron size.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.

View Article: PubMed Central - HTML - PubMed

Affiliation: Laboratoire Evolution, génomes et spéciation UPR 9034 CNRS, 91198 Gif-sur-Yvette, and Université Paris-Sud, Orsay, 91405, France. jldl@legs.cnrs-gif.fr

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.

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Average intron sizes at positions where more than ten values were available. Error bars indicate standard deviations. The long bar at position 6 is due to a single long intron in Stehi1/83072/. Red line : average intron size for the whole genomes of all the species studied. Dashed lines show standard deviation.
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Figure 5: Average intron sizes at positions where more than ten values were available. Error bars indicate standard deviations. The long bar at position 6 is due to a single long intron in Stehi1/83072/. Red line : average intron size for the whole genomes of all the species studied. Dashed lines show standard deviation.

Mentions: Overall, the average intron size was 61.6 bp, with a low dispersion, since the median was 56 bp and the third quartile was 62 bp. Figure 5 shows the average intron sizes at positions with more than ten values available. The sizes fall well within the range of average intron sizes at the genome level for the species included in the study. The conspicuous size homogeneity across intron positions and the generally low standard deviations suggest that intron size, at least in this "young" gene, may be constrained, e.g. to fit the abilities of the spliceosome.


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

Da Lage JL, Binder M, Hua-Van A, Janeček S, Casane D - BMC Evol. Biol. (2013)

Average intron sizes at positions where more than ten values were available. Error bars indicate standard deviations. The long bar at position 6 is due to a single long intron in Stehi1/83072/. Red line : average intron size for the whole genomes of all the species studied. Dashed lines show standard deviation.
© Copyright Policy - open-access
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC3584928&req=5

Figure 5: Average intron sizes at positions where more than ten values were available. Error bars indicate standard deviations. The long bar at position 6 is due to a single long intron in Stehi1/83072/. Red line : average intron size for the whole genomes of all the species studied. Dashed lines show standard deviation.
Mentions: Overall, the average intron size was 61.6 bp, with a low dispersion, since the median was 56 bp and the third quartile was 62 bp. Figure 5 shows the average intron sizes at positions with more than ten values available. The sizes fall well within the range of average intron sizes at the genome level for the species included in the study. The conspicuous size homogeneity across intron positions and the generally low standard deviations suggest that intron size, at least in this "young" gene, may be constrained, e.g. to fit the abilities of the spliceosome.

Bottom Line: The results indicate a high rate of intron insertions soon after the gene settled in the fungal genome.There was little variation of intron size.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.

View Article: PubMed Central - HTML - PubMed

Affiliation: Laboratoire Evolution, génomes et spéciation UPR 9034 CNRS, 91198 Gif-sur-Yvette, and Université Paris-Sud, Orsay, 91405, France. jldl@legs.cnrs-gif.fr

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.

Show MeSH
Related in: MedlinePlus