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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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Intron positions in the transferred α-amylase gene homologous to Phchr1/7087/ found in Fungi. Pink dots: phase 0 introns; green dots: phase 1 introns; blue dots: phase 2 introns. Shaded regions represent unknown sequences. The black bar is a region of uncertain annotation. Asterisks indicate possible cases of intron sliding. CBM20 indicates the presence of an additional carbohydrate binding module of the CBM20 family. The number of introns is meant without the CBM20 extension.
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Figure 2: Intron positions in the transferred α-amylase gene homologous to Phchr1/7087/ found in Fungi. Pink dots: phase 0 introns; green dots: phase 1 introns; blue dots: phase 2 introns. Shaded regions represent unknown sequences. The black bar is a region of uncertain annotation. Asterisks indicate possible cases of intron sliding. CBM20 indicates the presence of an additional carbohydrate binding module of the CBM20 family. The number of introns is meant without the CBM20 extension.

Mentions: As many as 480 introns that map at 64 intron positions were identified (Figure 2 and Additional file 4: Figure S1). The number of introns per gene ranged from 8 (Ganoderma sp. Gansp1/123688/) to 22 (e.g. Stereum hirsutum Stehi1/95395/), with 13.3 introns/gene on average, not counting the CBM20 extension. This high density considerably exceeds the average values for Basidiomycete genomes, which range from 3.8 to 5.7 introns/gene (data from the JGI). In addition, we found no correlation between the average genomic intron density and the intron density in the HGT Amy genes (not shown), in contrast to a previous study [34]. This may be explained by the fact that all the species in our study fall within a relatively narrow range of genomic intron density, compared to the span of the study cited above, which included Ascomycetes, that are more intron-poor, and by the likely large within-genome variance. We were unable to identify the origin of any inserted introns (donor DNA). Indeed, intron sequences diverged too fast to allow alignment between orthologous introns even between closely related species, such as P. chrysosporium and P. carnosa.


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)

Intron positions in the transferred α-amylase gene homologous to Phchr1/7087/ found in Fungi. Pink dots: phase 0 introns; green dots: phase 1 introns; blue dots: phase 2 introns. Shaded regions represent unknown sequences. The black bar is a region of uncertain annotation. Asterisks indicate possible cases of intron sliding. CBM20 indicates the presence of an additional carbohydrate binding module of the CBM20 family. The number of introns is meant without the CBM20 extension.
© Copyright Policy - open-access
Related In: Results  -  Collection

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

Figure 2: Intron positions in the transferred α-amylase gene homologous to Phchr1/7087/ found in Fungi. Pink dots: phase 0 introns; green dots: phase 1 introns; blue dots: phase 2 introns. Shaded regions represent unknown sequences. The black bar is a region of uncertain annotation. Asterisks indicate possible cases of intron sliding. CBM20 indicates the presence of an additional carbohydrate binding module of the CBM20 family. The number of introns is meant without the CBM20 extension.
Mentions: As many as 480 introns that map at 64 intron positions were identified (Figure 2 and Additional file 4: Figure S1). The number of introns per gene ranged from 8 (Ganoderma sp. Gansp1/123688/) to 22 (e.g. Stereum hirsutum Stehi1/95395/), with 13.3 introns/gene on average, not counting the CBM20 extension. This high density considerably exceeds the average values for Basidiomycete genomes, which range from 3.8 to 5.7 introns/gene (data from the JGI). In addition, we found no correlation between the average genomic intron density and the intron density in the HGT Amy genes (not shown), in contrast to a previous study [34]. This may be explained by the fact that all the species in our study fall within a relatively narrow range of genomic intron density, compared to the span of the study cited above, which included Ascomycetes, that are more intron-poor, and by the likely large within-genome variance. We were unable to identify the origin of any inserted introns (donor DNA). Indeed, intron sequences diverged too fast to allow alignment between orthologous introns even between closely related species, such as P. chrysosporium and P. carnosa.

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