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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

Tree of glycosyl hydrolases of the GH13 family. Full gene and species names and taxonomic positions are given in Additional file 3: Table S3. GH13 subfamilies [58] are colour-labelled and indicated by their numbers next to the species names. The fungal genes studied in this work are indicated by an asterisk. Bootstrap values are shown along the branches.
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Figure 1: Tree of glycosyl hydrolases of the GH13 family. Full gene and species names and taxonomic positions are given in Additional file 3: Table S3. GH13 subfamilies [58] are colour-labelled and indicated by their numbers next to the species names. The fungal genes studied in this work are indicated by an asterisk. Bootstrap values are shown along the branches.

Mentions: We first performed TBLASTN and BLASTP searches against GenBank using the candidate α-amylase gene Phchr1/7087/. The best hits belonged to a few Basidiomycetes (Serpula lacrymans, Schizophyllum commune, Piriformospora indica) and then a lot of Bacteria, mainly Actinomycetales. No other fungus was found within the 100 first hits, except Moniliophthora perniciosa (Agaricales, Marasmiaceae), a truncated sequence which will be no longer considered here (MPER_11606), and a single Ascomycete species, Chaetomium globosum, already reported to harbor a similar α-amylase gene (CHGG_04966), but with a distinct bacterial origin [35]. However, most fungal genome data have not been deposited yet to GenBank. Thus, we searched for genes similar to our P. chrysosporium query in the Mycocosm database at the JGI. Our BLAST searches against all fungal database available to us (fungalgenomes.org) retrieved a total of 42 sequences with high similarity to the P. chrysosporium query (BLASTP expect-value < 10-109 in the Mycocosm database) from 24 species only, all Basidiomycetes. This confirmed the limited phylogenetic distribution of this gene among Fungi, and thus supported its likely bacterial origin. Figure 1 shows a tree of α-amylases of the GH13 family [64] from various prokaryotes and eukaryotes. This important enzyme group was divided in subfamilies [58]. The tree shows that the genes we recovered in Basidiomycetes are grouped among Actinobacteria GH13_32 α-amylases, supporting an actinobacterial origin of the donor species. A very recent study supports this conclusion [65]. The phylogenetic distribution of the recovered genes is limited to Agaricomycotina, suggests that the HGT event took place rather basally in Basidiomycetes, but after the split from Tremellomycetes, probably at the basal node of Agaricomycotina. Interestingly, according to the phylogenetic distribution of the genes, a few species seem to have lost this α-amylase: the clade containing Postia placenta, Wolfiporia cocos and Fomitopsis pinicola, and the clade containing Coprinopsis cinerea and Laccaria bicolor. The Bolete Paxillus involutus also lacks the gene (not shown). The gene was duplicated independently in several lineages, with for instance four copies in Stereum hirsutum. In addition to these 42 sequences, two other Basidiomycete sequences from the remote Pucciniomycetes Melampsora laricis-populina (Melpl1/90587/) and Puccinia graminis (Pucgr1/25736/) were retrieved, with much lower similarity with the P. chrysosporium query (expect value ca. 10-67 and 10-76, respectively), but they probably have an origin distinct from the gene studied here, although bacterial too, given their position in the tree (Figure 1 and Additional file 3: Table S3).


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)

Tree of glycosyl hydrolases of the GH13 family. Full gene and species names and taxonomic positions are given in Additional file 3: Table S3. GH13 subfamilies [58] are colour-labelled and indicated by their numbers next to the species names. The fungal genes studied in this work are indicated by an asterisk. Bootstrap values are shown along the branches.
© Copyright Policy - open-access
Related In: Results  -  Collection

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

Figure 1: Tree of glycosyl hydrolases of the GH13 family. Full gene and species names and taxonomic positions are given in Additional file 3: Table S3. GH13 subfamilies [58] are colour-labelled and indicated by their numbers next to the species names. The fungal genes studied in this work are indicated by an asterisk. Bootstrap values are shown along the branches.
Mentions: We first performed TBLASTN and BLASTP searches against GenBank using the candidate α-amylase gene Phchr1/7087/. The best hits belonged to a few Basidiomycetes (Serpula lacrymans, Schizophyllum commune, Piriformospora indica) and then a lot of Bacteria, mainly Actinomycetales. No other fungus was found within the 100 first hits, except Moniliophthora perniciosa (Agaricales, Marasmiaceae), a truncated sequence which will be no longer considered here (MPER_11606), and a single Ascomycete species, Chaetomium globosum, already reported to harbor a similar α-amylase gene (CHGG_04966), but with a distinct bacterial origin [35]. However, most fungal genome data have not been deposited yet to GenBank. Thus, we searched for genes similar to our P. chrysosporium query in the Mycocosm database at the JGI. Our BLAST searches against all fungal database available to us (fungalgenomes.org) retrieved a total of 42 sequences with high similarity to the P. chrysosporium query (BLASTP expect-value < 10-109 in the Mycocosm database) from 24 species only, all Basidiomycetes. This confirmed the limited phylogenetic distribution of this gene among Fungi, and thus supported its likely bacterial origin. Figure 1 shows a tree of α-amylases of the GH13 family [64] from various prokaryotes and eukaryotes. This important enzyme group was divided in subfamilies [58]. The tree shows that the genes we recovered in Basidiomycetes are grouped among Actinobacteria GH13_32 α-amylases, supporting an actinobacterial origin of the donor species. A very recent study supports this conclusion [65]. The phylogenetic distribution of the recovered genes is limited to Agaricomycotina, suggests that the HGT event took place rather basally in Basidiomycetes, but after the split from Tremellomycetes, probably at the basal node of Agaricomycotina. Interestingly, according to the phylogenetic distribution of the genes, a few species seem to have lost this α-amylase: the clade containing Postia placenta, Wolfiporia cocos and Fomitopsis pinicola, and the clade containing Coprinopsis cinerea and Laccaria bicolor. The Bolete Paxillus involutus also lacks the gene (not shown). The gene was duplicated independently in several lineages, with for instance four copies in Stereum hirsutum. In addition to these 42 sequences, two other Basidiomycete sequences from the remote Pucciniomycetes Melampsora laricis-populina (Melpl1/90587/) and Puccinia graminis (Pucgr1/25736/) were retrieved, with much lower similarity with the P. chrysosporium query (expect value ca. 10-67 and 10-76, respectively), but they probably have an origin distinct from the gene studied here, although bacterial too, given their position in the tree (Figure 1 and Additional file 3: Table S3).

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