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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

Over-represented elements in sponge A. queenslandica RPG introns composed of three motifs.Full tripartite motifs are circled. The E-value and combined p-value were extracted from MEME.
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pone-0042523-g002: Over-represented elements in sponge A. queenslandica RPG introns composed of three motifs.Full tripartite motifs are circled. The E-value and combined p-value were extracted from MEME.

Mentions: Full-length cDNA sequences coding for 79 RPs were identified in the marine sponge A. queenslandica (AQ) genome, and the gene structure for 78 of them was completely ascertained. The RPS14 gene was not completely determined due to the absence of WGS sequences indispensable for assembling one long intron. This gene was not considered in calculating the average values shown in Table S3. 76 RPGs from cnidarian N. vectensis and 73 from placozoan T. adhaerens were used as control. Sponge AQ RPGs contained an average of 4.01 introns. The RPP0 gene had the largest number of introns - 10, while the only gene without introns was RPL35 (Table S3). In 78 complete RPGs a total of 312 introns with an average length of 164 bp were found. However, three quarters of the introns were shorter than the average value (Fig. 1), which indicates that only a few long ones contribute considerably in accretion of average intron length. The median value of RPG intron length was 68 bp, which is slightly lower than the median intron length for the published draft genome (81 bp) [12]. The longest was the second intron of the RPS27 gene (2263 bp), and the shortest one was the first intron of the RPS21 gene (37 bp). Human RPGs have significantly longer introns of 760 bp on average [39]. Transposable element insertions play an important role in the evolution of intron size [40]. Therefore we checked for over-represented elements in sponge AQ RPG introns. We found 24 copies of a tripartite element in ten introns of ten RPGs present in one to four copies (Fig. 2). The average intron length of these ten introns was 780 bp, and each one of them is longer than 500 bp. Only 23 of 312 sponge RPG introns are longer than 500 bp, which indicates that these element insertions contribute to sponge AQ RPG intron length. The average coding sequence (CDS) length did not differ as drastically as intron length. AQ had an average of 504 bp long CDSs, while human had 521 bp [39]. Most AQ introns, 285 of them, were found between translational start and stop codons, 26 introns were found in the 5′ untranslated region (5′ - UTR) and only one in the 3′ UTR of the RPS9 gene. Most of the introns found between translational start and stop codons, were phase 0 (52%), 27% were phase 1 and 21% were phase 2. These results support the so-called “50/30/20 rule” of intron phase distributions. It has been found that across many studied organisms, approximately 50% of introns are phase 0, 30% are phase 1 and 20% are phase 2 [41]. Almost all introns found in sponge AQ RPGs start with GT and end with AG (so called GT-AG introns). Only 2% were GC-AG introns, and AT-AC introns were not found. The average guanine and cytosine (GC) content of introns was 31.2%, which is considerably smaller than the GC content of coding sequences (44.2%). Moreover, a higher GC content in exons was observed in every RPG, without exception (Table S3). A similar effect has been found in human, where exons generally also have higher GC content than introns and intergenic regions [42]. It has also been shown that the sponge S. domunucula (SD) RPGs have a preference for C- and G- ending codons [43] and that the genome has a GC content of 39%. Based on our estimate of a similar amount of GC content (36%) in the genome of AQ we predict that this effect is probably also pronounced in this Demospongiae.


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)

Over-represented elements in sponge A. queenslandica RPG introns composed of three motifs.Full tripartite motifs are circled. The E-value and combined p-value were extracted from MEME.
© Copyright Policy
Related In: Results  -  Collection

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

pone-0042523-g002: Over-represented elements in sponge A. queenslandica RPG introns composed of three motifs.Full tripartite motifs are circled. The E-value and combined p-value were extracted from MEME.
Mentions: Full-length cDNA sequences coding for 79 RPs were identified in the marine sponge A. queenslandica (AQ) genome, and the gene structure for 78 of them was completely ascertained. The RPS14 gene was not completely determined due to the absence of WGS sequences indispensable for assembling one long intron. This gene was not considered in calculating the average values shown in Table S3. 76 RPGs from cnidarian N. vectensis and 73 from placozoan T. adhaerens were used as control. Sponge AQ RPGs contained an average of 4.01 introns. The RPP0 gene had the largest number of introns - 10, while the only gene without introns was RPL35 (Table S3). In 78 complete RPGs a total of 312 introns with an average length of 164 bp were found. However, three quarters of the introns were shorter than the average value (Fig. 1), which indicates that only a few long ones contribute considerably in accretion of average intron length. The median value of RPG intron length was 68 bp, which is slightly lower than the median intron length for the published draft genome (81 bp) [12]. The longest was the second intron of the RPS27 gene (2263 bp), and the shortest one was the first intron of the RPS21 gene (37 bp). Human RPGs have significantly longer introns of 760 bp on average [39]. Transposable element insertions play an important role in the evolution of intron size [40]. Therefore we checked for over-represented elements in sponge AQ RPG introns. We found 24 copies of a tripartite element in ten introns of ten RPGs present in one to four copies (Fig. 2). The average intron length of these ten introns was 780 bp, and each one of them is longer than 500 bp. Only 23 of 312 sponge RPG introns are longer than 500 bp, which indicates that these element insertions contribute to sponge AQ RPG intron length. The average coding sequence (CDS) length did not differ as drastically as intron length. AQ had an average of 504 bp long CDSs, while human had 521 bp [39]. Most AQ introns, 285 of them, were found between translational start and stop codons, 26 introns were found in the 5′ untranslated region (5′ - UTR) and only one in the 3′ UTR of the RPS9 gene. Most of the introns found between translational start and stop codons, were phase 0 (52%), 27% were phase 1 and 21% were phase 2. These results support the so-called “50/30/20 rule” of intron phase distributions. It has been found that across many studied organisms, approximately 50% of introns are phase 0, 30% are phase 1 and 20% are phase 2 [41]. Almost all introns found in sponge AQ RPGs start with GT and end with AG (so called GT-AG introns). Only 2% were GC-AG introns, and AT-AC introns were not found. The average guanine and cytosine (GC) content of introns was 31.2%, which is considerably smaller than the GC content of coding sequences (44.2%). Moreover, a higher GC content in exons was observed in every RPG, without exception (Table S3). A similar effect has been found in human, where exons generally also have higher GC content than introns and intergenic regions [42]. It has also been shown that the sponge S. domunucula (SD) RPGs have a preference for C- and G- ending codons [43] and that the genome has a GC content of 39%. Based on our estimate of a similar amount of GC content (36%) in the genome of AQ we predict that this effect is probably also pronounced in this Demospongiae.

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