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Structural and functional characterization of ribosomal protein gene introns in sponges.

Perina D, Korolija M, Mikoč A, Roller M, Pleše B, Imešek M, Morrow C, Batel R, Ćetković H - PLoS ONE (2012)

Bottom Line: Sponges from the Suberites genus show consistency in RPG intron position conservation.However, significant differences in some of the orthologous RPG introns of closely related sponges were observed.This indicates that RPG introns are dynamic even on these shorter evolutionary time scales.

View Article: PubMed Central - PubMed

Affiliation: Department of Molecular Biology, Rudjer Boskovic Institute, Zagreb, Croatia.

ABSTRACT
Ribosomal protein genes (RPGs) are a powerful tool for studying intron evolution. They exist in all three domains of life and are much conserved. Accumulating genomic data suggest that RPG introns in many organisms abound with non-protein-coding-RNAs (ncRNAs). These ancient ncRNAs are small nucleolar RNAs (snoRNAs) essential for ribosome assembly. They are also mobile genetic elements and therefore probably important in diversification and enrichment of transcriptomes through various mechanisms such as intron/exon gain/loss. snoRNAs in basal metazoans are poorly characterized. We examined 449 RPG introns, in total, from four demosponges: Amphimedon queenslandica, Suberites domuncula, Suberites ficus and Suberites pagurorum and showed that RPG introns from A. queenslandica share position conservancy and some structural similarity with "higher" metazoans. Moreover, our study indicates that mobile element insertions play an important role in the evolution of their size. In four sponges 51 snoRNAs were identified. The analysis showed discrepancies between the snoRNA pools of orthologous RPG introns between S. domuncula and A. queenslandica. Furthermore, these two sponges show as much conservancy of RPG intron positions between each other as between themselves and human. Sponges from the Suberites genus show consistency in RPG intron position conservation. However, significant differences in some of the orthologous RPG introns of closely related sponges were observed. This indicates that RPG introns are dynamic even on these shorter evolutionary time scales.

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Multiple alignment of selected introns from three species of the genus Suberites: S. domuncula (SD), S. ficus (SF) and S. pagurorum (SP).A large insertion is shown in the fourth intron of the SF RPL5 gene (A), changes in first introns of RPS15A gene (B), smaller changes between fifth introns of the RPS18 gene (C) and relatively high conservation in the sixth intron of RPP0 gene (D).
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pone-0042523-g007: Multiple alignment of selected introns from three species of the genus Suberites: S. domuncula (SD), S. ficus (SF) and S. pagurorum (SP).A large insertion is shown in the fourth intron of the SF RPL5 gene (A), changes in first introns of RPS15A gene (B), smaller changes between fifth introns of the RPS18 gene (C) and relatively high conservation in the sixth intron of RPP0 gene (D).

Mentions: Both trans-duplication, duplication of snoRNA from introns to distant genomic locations, and previously mentioned cis-duplication, duplication of snoRNA to a neighboring intron of the same gene, were already observed in, most notably, nematodes [47] and platypus [48]. This is in accordance with a model for the evolutionary origin of guide snoRNAs which states that the major source of novel snoRNAs are duplications of the ancestral snoRNA gene [49]. It is interesting to note that all of the 18 identified snoRNAs in the sponge AQ were present in single copies in RPGs while in SD, SF and SP three were present in a single copy and four were found duplicated in neighboring introns. The diverse patterns of snoRNA loci in different sponges' RPGs are possibly a consequence of the mobility of snoRNAs [50]. One of the mechanisms has been shown to be retroposition [47], [48]. It is known that snoRNAs can change their genomic location even within relatively short (vertebrate) evolutionary time scales [51]. Mobile genetic sequences play an important role in the diversification of mammalian genomes, for example, through mechanisms such as exonization and intronization [40]. These mechanisms are probably also present in sponges. Differences in snoRNA pools in the orthologous RPGs of the SD and AQ sponges is also accompanied with differences in conservation of intron position. 87.5% of SD RPG introns analyzed were present in AQ, while 86.7% of SD RPG introns were present in human. These two Demospongiae belong to different clades, AQ to marine Haplosclerida (G3) and SD to the G4 clade [38]. Although it is difficult to resolve the exact time of the split of these clades, it has been estimated to have occurred 600 million years ago [52]. To examine dynamics of sponges' RPG introns on a smaller time scale, we sequenced the introns of two additional species from the Suberites genus: S. ficus (SF) and S. pagurorum (SP). The total of 126 RPG introns examined (available as Text S1) in these three more closely related species are 79.7%, 80.3% and 64.7% (for SD, SF an SP, respectively) conserved in relation to the consensus sequence from all three species (see Fig. S1). All examined RPG intron positions were conserved in Suberites species, which indicates that on this shorter evolutionary time scale mobility of snoRNAs is not a significant factor that determines intron dynamics. However, some introns possess significant variations from the characterized consensus, for example an insertion so large (see Fig. S1 and Fig. 7) that the fourth intron of the SF RPL5 gene is only 17% conserved in relation to the consensus sequence of all three Suberites species. Many mechanisms and factors influence intron characteristics (e.g. see introduction in [53]). Up to date no genome of the Suberites genus has been sequenced, nor a ncRNAs library made, therefore it is very speculative to hypothesize on the origin of these insertions, i.e. if for example these insertions originating from mobile genetic elements and/or parts of the genome inserted during crossover.


Structural and functional characterization of ribosomal protein gene introns in sponges.

Perina D, Korolija M, Mikoč A, Roller M, Pleše B, Imešek M, Morrow C, Batel R, Ćetković H - PLoS ONE (2012)

Multiple alignment of selected introns from three species of the genus Suberites: S. domuncula (SD), S. ficus (SF) and S. pagurorum (SP).A large insertion is shown in the fourth intron of the SF RPL5 gene (A), changes in first introns of RPS15A gene (B), smaller changes between fifth introns of the RPS18 gene (C) and relatively high conservation in the sixth intron of RPP0 gene (D).
© Copyright Policy
Related In: Results  -  Collection

Show All Figures
getmorefigures.php?uid=PMC3412847&req=5

pone-0042523-g007: Multiple alignment of selected introns from three species of the genus Suberites: S. domuncula (SD), S. ficus (SF) and S. pagurorum (SP).A large insertion is shown in the fourth intron of the SF RPL5 gene (A), changes in first introns of RPS15A gene (B), smaller changes between fifth introns of the RPS18 gene (C) and relatively high conservation in the sixth intron of RPP0 gene (D).
Mentions: Both trans-duplication, duplication of snoRNA from introns to distant genomic locations, and previously mentioned cis-duplication, duplication of snoRNA to a neighboring intron of the same gene, were already observed in, most notably, nematodes [47] and platypus [48]. This is in accordance with a model for the evolutionary origin of guide snoRNAs which states that the major source of novel snoRNAs are duplications of the ancestral snoRNA gene [49]. It is interesting to note that all of the 18 identified snoRNAs in the sponge AQ were present in single copies in RPGs while in SD, SF and SP three were present in a single copy and four were found duplicated in neighboring introns. The diverse patterns of snoRNA loci in different sponges' RPGs are possibly a consequence of the mobility of snoRNAs [50]. One of the mechanisms has been shown to be retroposition [47], [48]. It is known that snoRNAs can change their genomic location even within relatively short (vertebrate) evolutionary time scales [51]. Mobile genetic sequences play an important role in the diversification of mammalian genomes, for example, through mechanisms such as exonization and intronization [40]. These mechanisms are probably also present in sponges. Differences in snoRNA pools in the orthologous RPGs of the SD and AQ sponges is also accompanied with differences in conservation of intron position. 87.5% of SD RPG introns analyzed were present in AQ, while 86.7% of SD RPG introns were present in human. These two Demospongiae belong to different clades, AQ to marine Haplosclerida (G3) and SD to the G4 clade [38]. Although it is difficult to resolve the exact time of the split of these clades, it has been estimated to have occurred 600 million years ago [52]. To examine dynamics of sponges' RPG introns on a smaller time scale, we sequenced the introns of two additional species from the Suberites genus: S. ficus (SF) and S. pagurorum (SP). The total of 126 RPG introns examined (available as Text S1) in these three more closely related species are 79.7%, 80.3% and 64.7% (for SD, SF an SP, respectively) conserved in relation to the consensus sequence from all three species (see Fig. S1). All examined RPG intron positions were conserved in Suberites species, which indicates that on this shorter evolutionary time scale mobility of snoRNAs is not a significant factor that determines intron dynamics. However, some introns possess significant variations from the characterized consensus, for example an insertion so large (see Fig. S1 and Fig. 7) that the fourth intron of the SF RPL5 gene is only 17% conserved in relation to the consensus sequence of all three Suberites species. Many mechanisms and factors influence intron characteristics (e.g. see introduction in [53]). Up to date no genome of the Suberites genus has been sequenced, nor a ncRNAs library made, therefore it is very speculative to hypothesize on the origin of these insertions, i.e. if for example these insertions originating from mobile genetic elements and/or parts of the genome inserted during crossover.

Bottom Line: Sponges from the Suberites genus show consistency in RPG intron position conservation.However, significant differences in some of the orthologous RPG introns of closely related sponges were observed.This indicates that RPG introns are dynamic even on these shorter evolutionary time scales.

View Article: PubMed Central - PubMed

Affiliation: Department of Molecular Biology, Rudjer Boskovic Institute, Zagreb, Croatia.

ABSTRACT
Ribosomal protein genes (RPGs) are a powerful tool for studying intron evolution. They exist in all three domains of life and are much conserved. Accumulating genomic data suggest that RPG introns in many organisms abound with non-protein-coding-RNAs (ncRNAs). These ancient ncRNAs are small nucleolar RNAs (snoRNAs) essential for ribosome assembly. They are also mobile genetic elements and therefore probably important in diversification and enrichment of transcriptomes through various mechanisms such as intron/exon gain/loss. snoRNAs in basal metazoans are poorly characterized. We examined 449 RPG introns, in total, from four demosponges: Amphimedon queenslandica, Suberites domuncula, Suberites ficus and Suberites pagurorum and showed that RPG introns from A. queenslandica share position conservancy and some structural similarity with "higher" metazoans. Moreover, our study indicates that mobile element insertions play an important role in the evolution of their size. In four sponges 51 snoRNAs were identified. The analysis showed discrepancies between the snoRNA pools of orthologous RPG introns between S. domuncula and A. queenslandica. Furthermore, these two sponges show as much conservancy of RPG intron positions between each other as between themselves and human. Sponges from the Suberites genus show consistency in RPG intron position conservation. However, significant differences in some of the orthologous RPG introns of closely related sponges were observed. This indicates that RPG introns are dynamic even on these shorter evolutionary time scales.

Show MeSH
Related in: MedlinePlus