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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.

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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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Consensus sequences at positions −2 and −1, and +1 and +2 around intron positions, drawn with Weblogo 3.2[72](http://weblogo.threeplusone.com/create.cgi). A: all positions, intron present. B: all positions, intron absent. C: sequence at the 17 oldest positions when an intron is present; D: sequence at the 17 oldest positions in the absence of intron, i. e. after intron loss; E: sequence at the recent positions 2, 3, 4, 11, 12, 13, 14, 15, 16, 21, 25, 31, 37, 39a, 47, 48, 51, 52, 55, 57 in the presence of intron; F: same positions as E, in the absence of intron. Introns of Stehi_78757, of Jaapia argillacea and of Bjerkandera adusta were not included. n is the number of sequences. Y-axis is graduated in bits of information. Error bars are Bayesian 95% confidence intervals.
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Figure 6: Consensus sequences at positions −2 and −1, and +1 and +2 around intron positions, drawn with Weblogo 3.2[72](http://weblogo.threeplusone.com/create.cgi). A: all positions, intron present. B: all positions, intron absent. C: sequence at the 17 oldest positions when an intron is present; D: sequence at the 17 oldest positions in the absence of intron, i. e. after intron loss; E: sequence at the recent positions 2, 3, 4, 11, 12, 13, 14, 15, 16, 21, 25, 31, 37, 39a, 47, 48, 51, 52, 55, 57 in the presence of intron; F: same positions as E, in the absence of intron. Introns of Stehi_78757, of Jaapia argillacea and of Bjerkandera adusta were not included. n is the number of sequences. Y-axis is graduated in bits of information. Error bars are Bayesian 95% confidence intervals.

Mentions: We studied whether introns were inserted into preferential sequences, according to the protosplice model [69], and whether local sequence information changed in the presence vs. in the absence of introns. The major fact is that overall, considering all intron positions and phases, there was little information at the last two exonic 5' and the first two exonic 3' nucleotide positions (Figure 6A and 6B). A slight preference for G[intron]G was suggested, more visible for phase 1 introns (Additional file 9: Figure S5), as observed earlier (e.g.[70]). When the intron was absent, the level of information was even lower. This lower information level in the absence of intron was observed for each phase considered separately (Additional file 9: Figure S5). We also compared information level according to the age of insertions, i.e. recently inserted introns vs. the 17 oldest positions. Information was slightly stronger around oldest introns than around more recent introns, although not significantly (Figure 6C and 6E). Conserved oldest introns, i.e. still present in most extant genes, had not a higher informational environment (not shown). One might assume that their presence in a majority of genes until now might be related to a strong splicing signal, avoiding missplicing, and thus negative selection. We observed that their conservation until now could not be explained by a more informative environment. In contrast, the level of information increased at oldest positions after intron loss (Figure 6D). Information content inside the introns was investigated at the 5' and 3' splicing sites. Sequences complied to a classical consensus GTrnG…yAG. Thirteen introns over 478 (2.7%) had GC instead of GT as the donor site, consistent with the 1.3% reported by Iwata et al. (2011). There was a strongly conserved G at position 5, as noticed in Fungi [71]. However, the prevalence of this G varied according to the intron position (e.g. 30 vs. 56) or the species (Additional file 10: Figure S6). Recent introns showed a lower information content at positions 3 and 4 of the 5' splicing site; however, this may be not significant given the limited sample size.


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)

Consensus sequences at positions −2 and −1, and +1 and +2 around intron positions, drawn with Weblogo 3.2[72](http://weblogo.threeplusone.com/create.cgi). A: all positions, intron present. B: all positions, intron absent. C: sequence at the 17 oldest positions when an intron is present; D: sequence at the 17 oldest positions in the absence of intron, i. e. after intron loss; E: sequence at the recent positions 2, 3, 4, 11, 12, 13, 14, 15, 16, 21, 25, 31, 37, 39a, 47, 48, 51, 52, 55, 57 in the presence of intron; F: same positions as E, in the absence of intron. Introns of Stehi_78757, of Jaapia argillacea and of Bjerkandera adusta were not included. n is the number of sequences. Y-axis is graduated in bits of information. Error bars are Bayesian 95% confidence intervals.
© Copyright Policy - open-access
Related In: Results  -  Collection

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

Figure 6: Consensus sequences at positions −2 and −1, and +1 and +2 around intron positions, drawn with Weblogo 3.2[72](http://weblogo.threeplusone.com/create.cgi). A: all positions, intron present. B: all positions, intron absent. C: sequence at the 17 oldest positions when an intron is present; D: sequence at the 17 oldest positions in the absence of intron, i. e. after intron loss; E: sequence at the recent positions 2, 3, 4, 11, 12, 13, 14, 15, 16, 21, 25, 31, 37, 39a, 47, 48, 51, 52, 55, 57 in the presence of intron; F: same positions as E, in the absence of intron. Introns of Stehi_78757, of Jaapia argillacea and of Bjerkandera adusta were not included. n is the number of sequences. Y-axis is graduated in bits of information. Error bars are Bayesian 95% confidence intervals.
Mentions: We studied whether introns were inserted into preferential sequences, according to the protosplice model [69], and whether local sequence information changed in the presence vs. in the absence of introns. The major fact is that overall, considering all intron positions and phases, there was little information at the last two exonic 5' and the first two exonic 3' nucleotide positions (Figure 6A and 6B). A slight preference for G[intron]G was suggested, more visible for phase 1 introns (Additional file 9: Figure S5), as observed earlier (e.g.[70]). When the intron was absent, the level of information was even lower. This lower information level in the absence of intron was observed for each phase considered separately (Additional file 9: Figure S5). We also compared information level according to the age of insertions, i.e. recently inserted introns vs. the 17 oldest positions. Information was slightly stronger around oldest introns than around more recent introns, although not significantly (Figure 6C and 6E). Conserved oldest introns, i.e. still present in most extant genes, had not a higher informational environment (not shown). One might assume that their presence in a majority of genes until now might be related to a strong splicing signal, avoiding missplicing, and thus negative selection. We observed that their conservation until now could not be explained by a more informative environment. In contrast, the level of information increased at oldest positions after intron loss (Figure 6D). Information content inside the introns was investigated at the 5' and 3' splicing sites. Sequences complied to a classical consensus GTrnG…yAG. Thirteen introns over 478 (2.7%) had GC instead of GT as the donor site, consistent with the 1.3% reported by Iwata et al. (2011). There was a strongly conserved G at position 5, as noticed in Fungi [71]. However, the prevalence of this G varied according to the intron position (e.g. 30 vs. 56) or the species (Additional file 10: Figure S6). Recent introns showed a lower information content at positions 3 and 4 of the 5' splicing site; however, this may be not significant given the limited sample size.

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