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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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Related in: MedlinePlus

Combinatorial grouping of 10 species according to the number of shared introns. Gray squares indicate presence of introns.
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pone-0042523-g003: Combinatorial grouping of 10 species according to the number of shared introns. Gray squares indicate presence of introns.

Mentions: To further explore introns' characteristics, 55 RPGs from sponge AQ were compared with orthologs from each of the following nine organisms whose whole genomes have been sequenced: H. sapiens (HS), S. purpuratus (SP), D. melanogaster (DM), C. elegans (CE), N. vectensis (NV), T. adhaerens (TA), M. brevicollis (MB), S. cerevisiae (SC) and A. thaliana (AT). The total number of analyzed introns within the coding regions of the RPGs in ten organisms was 1491 (Table S4). There are significant differences in intron number and length among these organisms causing variation in gene size. Characteristics of each RPG from model organisms used in this research (that are not included in Table S3) are given in Table S1. The position and phase of RPG introns were also compared in these ten organisms. The highest ratio of “unique” introns, those that are specific for a particular species, was found in yeast, 79.4%, and the lowest in placozoan, 3.1%. In all analyzed metazoans, except fruit fly and nematode worm, the ratio of “unique” introns was less than 10% (Table S4). Most positions, phases, and numbers of RPG introns, as well as RPs themselves (Table S5), were not drastically changed in metazoans from sponge to human. Fruit fly and nematode worm are the exceptions. 84.8% of sponge RPG introns are found in humans and 76.2% of human RPG introns are also present in sponge (Table S6). Our results support previously observed extensive intron loss in fruit fly and nematode worm [44]. Intron-sharing among all ten organisms is shown in Fig. 3. The highest number of RPG introns is shared between human, sea urchin, sea anemone, placozoan and sponge. The same organisms occur in other highly represented combinations of shared introns.


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)

Combinatorial grouping of 10 species according to the number of shared introns. Gray squares indicate presence of introns.
© Copyright Policy
Related In: Results  -  Collection

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

pone-0042523-g003: Combinatorial grouping of 10 species according to the number of shared introns. Gray squares indicate presence of introns.
Mentions: To further explore introns' characteristics, 55 RPGs from sponge AQ were compared with orthologs from each of the following nine organisms whose whole genomes have been sequenced: H. sapiens (HS), S. purpuratus (SP), D. melanogaster (DM), C. elegans (CE), N. vectensis (NV), T. adhaerens (TA), M. brevicollis (MB), S. cerevisiae (SC) and A. thaliana (AT). The total number of analyzed introns within the coding regions of the RPGs in ten organisms was 1491 (Table S4). There are significant differences in intron number and length among these organisms causing variation in gene size. Characteristics of each RPG from model organisms used in this research (that are not included in Table S3) are given in Table S1. The position and phase of RPG introns were also compared in these ten organisms. The highest ratio of “unique” introns, those that are specific for a particular species, was found in yeast, 79.4%, and the lowest in placozoan, 3.1%. In all analyzed metazoans, except fruit fly and nematode worm, the ratio of “unique” introns was less than 10% (Table S4). Most positions, phases, and numbers of RPG introns, as well as RPs themselves (Table S5), were not drastically changed in metazoans from sponge to human. Fruit fly and nematode worm are the exceptions. 84.8% of sponge RPG introns are found in humans and 76.2% of human RPG introns are also present in sponge (Table S6). Our results support previously observed extensive intron loss in fruit fly and nematode worm [44]. Intron-sharing among all ten organisms is shown in Fig. 3. The highest number of RPG introns is shared between human, sea urchin, sea anemone, placozoan and sponge. The same organisms occur in other highly represented combinations of shared introns.

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