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EST analysis of Ostreococcus lucimarinus, the most compact eukaryotic genome, shows an excess of introns in highly expressed genes.

Lanier W, Moustafa A, Bhattacharya D, Comeron JM - PLoS ONE (2008)

Bottom Line: The presence of introns in the highly reduced O. lucimarinus genome appears to be in opposition to simple explanations of genome evolution based on unidirectional tendencies, either neutral or selective.In a species with a genome that has been recently subjected to a great reduction of non-coding DNA, these results imply the existence of selective/functional roles for introns that are principally detectable in highly expressed genes.In these cases, introns are likely maintained by balancing the selective forces favoring their maintenance with other mutational and/or selective forces acting on genome size.

View Article: PubMed Central - PubMed

Affiliation: Interdisciplinary Program in Genetics, University of Iowa, Iowa, United States of America.

ABSTRACT

Background: The genome of the pico-eukaryotic (bacterial-sized) prasinophyte green alga Ostreococcus lucimarinus has one of the highest gene densities known in eukaryotes, yet it contains many introns. Phylogenetic studies suggest this unusually compact genome (13.2 Mb) is an evolutionarily derived state among prasinophytes. The presence of introns in the highly reduced O. lucimarinus genome appears to be in opposition to simple explanations of genome evolution based on unidirectional tendencies, either neutral or selective. Therefore, patterns of intron retention in this species can potentially provide insights into the forces governing intron evolution.

Methodology/principal findings: Here we studied intron features and levels of expression in O. lucimarinus using expressed sequence tags (ESTs) to annotate the current genome assembly. ESTs were assembled into unigene clusters that were mapped back to the O. lucimarinus Build 2.0 assembly using BLAST and the level of gene expression was inferred from the number of ESTs in each cluster. We find a positive correlation between expression levels and both intron number (R = +0.0893, p = <0.0005) and intron density (number of introns/kb of CDS; R = +0.0753, p = <0.005).

Conclusions/significance: In a species with a genome that has been recently subjected to a great reduction of non-coding DNA, these results imply the existence of selective/functional roles for introns that are principally detectable in highly expressed genes. In these cases, introns are likely maintained by balancing the selective forces favoring their maintenance with other mutational and/or selective forces acting on genome size.

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Related in: MedlinePlus

Levels of gene expression for intron containing and intronless genes in Ostreococcus lucimarinus.(a) Mean expression values and +/− standard errors for clusters lacking introns and all clusters containing introns. Expression values are in terms of the number of sequenced clones represented within a single unigene cluster. Boxplots showing the clustered contig lengths (b) and longest open reading frames (c) for contigs without introns (red, n = 265), contigs with introns (green, n = 1405), the combined data set of intron containing and intronless contigs (blue n = 1670), and for the complete EST library (yellow, n = 2050).
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pone-0002171-g002: Levels of gene expression for intron containing and intronless genes in Ostreococcus lucimarinus.(a) Mean expression values and +/− standard errors for clusters lacking introns and all clusters containing introns. Expression values are in terms of the number of sequenced clones represented within a single unigene cluster. Boxplots showing the clustered contig lengths (b) and longest open reading frames (c) for contigs without introns (red, n = 265), contigs with introns (green, n = 1405), the combined data set of intron containing and intronless contigs (blue n = 1670), and for the complete EST library (yellow, n = 2050).

Mentions: Nonparametric Spearman's rank correlation analysis using intron number in relation to the number of overlapping sequenced clones contained within unique gene clusters (used as a proxy for expression levels) returned a positive correlation between intron presence and increased expression (R = +0.0893, p<0.0005); an equivalent result is observed after excluding clusters mapped to Chromosome 2 (R = +0.0972, p<0.0005; see Table 3). Congruent with the Spearman's rank correlation, the comparison of intron-less and intron-containing genes showed significantly reduced expression for intron-less genes (Mann-Whitney U-test; Z = 3.95, p<0.0001; Figure 2a). Note that these results remain consistent if ribosomal proteins (n = 20) are excluded from the analysis, which results in a positive correlation between intron presence and expression levels (R = +0.0970, p<0.0005) and significantly reduced expression for intron-less genes when compared to intron-containing genes (Mann-Whitney U-test; Z = 4.18, p<0.0001). These latter results are not surprising given the limited contribution of ribosomal proteins to the EST library (Table S1; see Discussion).


EST analysis of Ostreococcus lucimarinus, the most compact eukaryotic genome, shows an excess of introns in highly expressed genes.

Lanier W, Moustafa A, Bhattacharya D, Comeron JM - PLoS ONE (2008)

Levels of gene expression for intron containing and intronless genes in Ostreococcus lucimarinus.(a) Mean expression values and +/− standard errors for clusters lacking introns and all clusters containing introns. Expression values are in terms of the number of sequenced clones represented within a single unigene cluster. Boxplots showing the clustered contig lengths (b) and longest open reading frames (c) for contigs without introns (red, n = 265), contigs with introns (green, n = 1405), the combined data set of intron containing and intronless contigs (blue n = 1670), and for the complete EST library (yellow, n = 2050).
© Copyright Policy
Related In: Results  -  Collection

Show All Figures
getmorefigures.php?uid=PMC2367439&req=5

pone-0002171-g002: Levels of gene expression for intron containing and intronless genes in Ostreococcus lucimarinus.(a) Mean expression values and +/− standard errors for clusters lacking introns and all clusters containing introns. Expression values are in terms of the number of sequenced clones represented within a single unigene cluster. Boxplots showing the clustered contig lengths (b) and longest open reading frames (c) for contigs without introns (red, n = 265), contigs with introns (green, n = 1405), the combined data set of intron containing and intronless contigs (blue n = 1670), and for the complete EST library (yellow, n = 2050).
Mentions: Nonparametric Spearman's rank correlation analysis using intron number in relation to the number of overlapping sequenced clones contained within unique gene clusters (used as a proxy for expression levels) returned a positive correlation between intron presence and increased expression (R = +0.0893, p<0.0005); an equivalent result is observed after excluding clusters mapped to Chromosome 2 (R = +0.0972, p<0.0005; see Table 3). Congruent with the Spearman's rank correlation, the comparison of intron-less and intron-containing genes showed significantly reduced expression for intron-less genes (Mann-Whitney U-test; Z = 3.95, p<0.0001; Figure 2a). Note that these results remain consistent if ribosomal proteins (n = 20) are excluded from the analysis, which results in a positive correlation between intron presence and expression levels (R = +0.0970, p<0.0005) and significantly reduced expression for intron-less genes when compared to intron-containing genes (Mann-Whitney U-test; Z = 4.18, p<0.0001). These latter results are not surprising given the limited contribution of ribosomal proteins to the EST library (Table S1; see Discussion).

Bottom Line: The presence of introns in the highly reduced O. lucimarinus genome appears to be in opposition to simple explanations of genome evolution based on unidirectional tendencies, either neutral or selective.In a species with a genome that has been recently subjected to a great reduction of non-coding DNA, these results imply the existence of selective/functional roles for introns that are principally detectable in highly expressed genes.In these cases, introns are likely maintained by balancing the selective forces favoring their maintenance with other mutational and/or selective forces acting on genome size.

View Article: PubMed Central - PubMed

Affiliation: Interdisciplinary Program in Genetics, University of Iowa, Iowa, United States of America.

ABSTRACT

Background: The genome of the pico-eukaryotic (bacterial-sized) prasinophyte green alga Ostreococcus lucimarinus has one of the highest gene densities known in eukaryotes, yet it contains many introns. Phylogenetic studies suggest this unusually compact genome (13.2 Mb) is an evolutionarily derived state among prasinophytes. The presence of introns in the highly reduced O. lucimarinus genome appears to be in opposition to simple explanations of genome evolution based on unidirectional tendencies, either neutral or selective. Therefore, patterns of intron retention in this species can potentially provide insights into the forces governing intron evolution.

Methodology/principal findings: Here we studied intron features and levels of expression in O. lucimarinus using expressed sequence tags (ESTs) to annotate the current genome assembly. ESTs were assembled into unigene clusters that were mapped back to the O. lucimarinus Build 2.0 assembly using BLAST and the level of gene expression was inferred from the number of ESTs in each cluster. We find a positive correlation between expression levels and both intron number (R = +0.0893, p = <0.0005) and intron density (number of introns/kb of CDS; R = +0.0753, p = <0.005).

Conclusions/significance: In a species with a genome that has been recently subjected to a great reduction of non-coding DNA, these results imply the existence of selective/functional roles for introns that are principally detectable in highly expressed genes. In these cases, introns are likely maintained by balancing the selective forces favoring their maintenance with other mutational and/or selective forces acting on genome size.

Show MeSH
Related in: MedlinePlus