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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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Ostreococcus lucimarinus and length distribution of clustered contigs and open reading frames.The prasinophyte green algal genus Ostreococcus is the smallest-known free-living eukaryotes, with an average size of 0.8 μm. (a) Image of Ostreococcus strain RCC 143 kindly provided by W. Eikrem and J. Throndsen (University of Oslo) (image also available in Wiki Commons). (b) and (c) Histograms showing the frequency and length distribution for clustered contigs (b) and longest open reading frames (c) for the Ostreococcus lucimarinus EST library.
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pone-0002171-g001: Ostreococcus lucimarinus and length distribution of clustered contigs and open reading frames.The prasinophyte green algal genus Ostreococcus is the smallest-known free-living eukaryotes, with an average size of 0.8 μm. (a) Image of Ostreococcus strain RCC 143 kindly provided by W. Eikrem and J. Throndsen (University of Oslo) (image also available in Wiki Commons). (b) and (c) Histograms showing the frequency and length distribution for clustered contigs (b) and longest open reading frames (c) for the Ostreococcus lucimarinus EST library.

Mentions: The genus Ostreococcus encompasses a group of globally distributed photosynthetic, unicellular green algae in the anciently diverged class Prasinophyta [1]. These cells are the smallest known eukaryotes [2], with cell sizes smaller than 1 μm (Figure 1a). Among free-living taxa, Ostreococcus species also contain the most compact (i.e., gene-dense) genomes [3]. For example, in comparison to the compact genome of Saccharomyces cerevisiae (12.1 Mbp) that contains ∼6000 open reading frames, with one gene every 2.0 kb, O. tauri and O. lucimarinus have genomes sizes of 12.6 and 13.2 Mbp with a gene occurring every 1.6 and 1.7 kb, respectively [3]–[5]. This degree of genome miniaturization is unparalleled among free-living eukaryotes and has led to the contraction of intergenic regions to an average of less than 200 bp in O. tauri, which is the smallest among eukaryotes [6], [7]. Yet surprisingly, the dearth of noncoding DNA is not maintained across the Ostreococcus genomes because introns are present in an estimated 20–25% of transcripts, compared to less than 4% of intron-containing genes in the budding yeast [4], [5]. This algal genome structure is in sharp contrast to the general positive relationship between intron and intergenic size, and ultimately genome size, observed across a broad range of eukaryotes [7]. In fact, Ostreococcus species display the highest ratio of intragenic to intergenic noncoding DNA detected thus far.


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)

Ostreococcus lucimarinus and length distribution of clustered contigs and open reading frames.The prasinophyte green algal genus Ostreococcus is the smallest-known free-living eukaryotes, with an average size of 0.8 μm. (a) Image of Ostreococcus strain RCC 143 kindly provided by W. Eikrem and J. Throndsen (University of Oslo) (image also available in Wiki Commons). (b) and (c) Histograms showing the frequency and length distribution for clustered contigs (b) and longest open reading frames (c) for the Ostreococcus lucimarinus EST library.
© Copyright Policy
Related In: Results  -  Collection

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

pone-0002171-g001: Ostreococcus lucimarinus and length distribution of clustered contigs and open reading frames.The prasinophyte green algal genus Ostreococcus is the smallest-known free-living eukaryotes, with an average size of 0.8 μm. (a) Image of Ostreococcus strain RCC 143 kindly provided by W. Eikrem and J. Throndsen (University of Oslo) (image also available in Wiki Commons). (b) and (c) Histograms showing the frequency and length distribution for clustered contigs (b) and longest open reading frames (c) for the Ostreococcus lucimarinus EST library.
Mentions: The genus Ostreococcus encompasses a group of globally distributed photosynthetic, unicellular green algae in the anciently diverged class Prasinophyta [1]. These cells are the smallest known eukaryotes [2], with cell sizes smaller than 1 μm (Figure 1a). Among free-living taxa, Ostreococcus species also contain the most compact (i.e., gene-dense) genomes [3]. For example, in comparison to the compact genome of Saccharomyces cerevisiae (12.1 Mbp) that contains ∼6000 open reading frames, with one gene every 2.0 kb, O. tauri and O. lucimarinus have genomes sizes of 12.6 and 13.2 Mbp with a gene occurring every 1.6 and 1.7 kb, respectively [3]–[5]. This degree of genome miniaturization is unparalleled among free-living eukaryotes and has led to the contraction of intergenic regions to an average of less than 200 bp in O. tauri, which is the smallest among eukaryotes [6], [7]. Yet surprisingly, the dearth of noncoding DNA is not maintained across the Ostreococcus genomes because introns are present in an estimated 20–25% of transcripts, compared to less than 4% of intron-containing genes in the budding yeast [4], [5]. This algal genome structure is in sharp contrast to the general positive relationship between intron and intergenic size, and ultimately genome size, observed across a broad range of eukaryotes [7]. In fact, Ostreococcus species display the highest ratio of intragenic to intergenic noncoding DNA detected thus far.

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