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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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Related in: MedlinePlus

Apparent intron gain and loss rates per million year and per lineage. Gain rates are in blue, loss rates are in red. The X axis is graduated in million years from the present.
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Figure 4: Apparent intron gain and loss rates per million year and per lineage. Gain rates are in blue, loss rates are in red. The X axis is graduated in million years from the present.

Mentions: We attempted to date divergence times of various fungal clades in order to date intron gains or losses (Additional file 7: Figure S4). These values were flawed by a large variance, due in part to the scarcity of fossils to be used for calibration and their datation. We estimated that the gene transfer occurred 448–363 million years ago (Ma). This means that at least 17 gains occurred within a ca. 85 Ma period, which is a high rate for a single gene. The average apparent rates of gains and losses per million year and per lineage are shown on Figure 4. This graph shows that after the initial burst of gains, few gains took place whereas losses accumulated. There were exceptions in two terminal branches, Stereum hirsutum and Punctularia strigosozonata, which both experienced numerous specific gains and losses. These two species are the main contributors to the second rise of gains in recent times in Figure 4.


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)

Apparent intron gain and loss rates per million year and per lineage. Gain rates are in blue, loss rates are in red. The X axis is graduated in million years from the present.
© Copyright Policy - open-access
Related In: Results  -  Collection

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

Figure 4: Apparent intron gain and loss rates per million year and per lineage. Gain rates are in blue, loss rates are in red. The X axis is graduated in million years from the present.
Mentions: We attempted to date divergence times of various fungal clades in order to date intron gains or losses (Additional file 7: Figure S4). These values were flawed by a large variance, due in part to the scarcity of fossils to be used for calibration and their datation. We estimated that the gene transfer occurred 448–363 million years ago (Ma). This means that at least 17 gains occurred within a ca. 85 Ma period, which is a high rate for a single gene. The average apparent rates of gains and losses per million year and per lineage are shown on Figure 4. This graph shows that after the initial burst of gains, few gains took place whereas losses accumulated. There were exceptions in two terminal branches, Stereum hirsutum and Punctularia strigosozonata, which both experienced numerous specific gains and losses. These two species are the main contributors to the second rise of gains in recent times in Figure 4.

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