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LTR retrotransposons contribute to genomic gigantism in plethodontid salamanders.

Sun C, Shepard DB, Chong RA, López Arriaza J, Hall K, Castoe TA, Feschotte C, Pollock DD, Mueller RL - Genome Biol Evol (2011)

Bottom Line: The most abundant TE superfamilies found in the genomes of our six focal species are similar, despite substantial variation in genome size.However, our results demonstrate a major difference between salamanders and other vertebrates: salamander genomes contain much larger amounts of long terminal repeat (LTR) retrotransposons, primarily Ty3/gypsy elements.These results suggest that increased proliferation of LTR retrotransposons was a major molecular mechanism contributing to genomic expansion in salamanders.

View Article: PubMed Central - PubMed

Affiliation: Department of Biology, Colorado State University, CO, USA.

ABSTRACT
Among vertebrates, most of the largest genomes are found within the salamanders, a clade of amphibians that includes 613 species. Salamander genome sizes range from ~14 to ~120 Gb. Because genome size is correlated with nucleus and cell sizes, as well as other traits, morphological evolution in salamanders has been profoundly affected by genomic gigantism. However, the molecular mechanisms driving genomic expansion in this clade remain largely unknown. Here, we present the first comparative analysis of transposable element (TE) content in salamanders. Using high-throughput sequencing, we generated genomic shotgun data for six species from the Plethodontidae, the largest family of salamanders. We then developed a pipeline to mine TE sequences from shotgun data in taxa with limited genomic resources, such as salamanders. Our summaries of overall TE abundance and diversity for each species demonstrate that TEs make up a substantial portion of salamander genomes, and that all of the major known types of TEs are represented in salamanders. The most abundant TE superfamilies found in the genomes of our six focal species are similar, despite substantial variation in genome size. However, our results demonstrate a major difference between salamanders and other vertebrates: salamander genomes contain much larger amounts of long terminal repeat (LTR) retrotransposons, primarily Ty3/gypsy elements. Thus, the extreme increase in genome size that occurred in salamanders was likely accompanied by a shift in TE landscape. These results suggest that increased proliferation of LTR retrotransposons was a major molecular mechanism contributing to genomic expansion in salamanders.

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The structures of seven full-length TE sequences mined from salamander shotgun reads. Abbreviations: gag, capsid-like protein; pro, protease; RT, reverse transcriptase; rve, integrase; ENV, envelope protein; YR, tyrosine recombinase; EN, endonuclease.
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fig2: The structures of seven full-length TE sequences mined from salamander shotgun reads. Abbreviations: gag, capsid-like protein; pro, protease; RT, reverse transcriptase; rve, integrase; ENV, envelope protein; YR, tyrosine recombinase; EN, endonuclease.

Mentions: In addition, the assembly step of our TE-mining pipeline allowed us to successfully generate seven putatively full-length elements, composite sequences representative of salamander TE superfamilies. After verification and refinement, we confirmed contigs representing full-length sequences of several superfamilies of Class I TEs: Ty3/gypsy, ERV1, DIRS, and Ngaro elements (LTR retrotransposons), as well as L1 and L2/CR1 elements (non-LTR retrotransposons). In addition, we confirmed contigs representing a full-length rolling circle Helitron (Class II TE). The structures of the seven full-length TEs we assembled are summarized in figure 2, and each is largely consistent with the structure reported for the same superfamily from other eukaryotic genomes. Sequences of these complete elements, as well as the full-length elements identified from Ambystoma mexicanum BAC clones, are available as supplementary file 2, Supplementary Material online. To our knowledge, this is the first description of the structure of full-length TEs in salamander genomes. Our successful assembly of full-length contigs from ∼1% genome coverage (using a stringent assembly algorithm) indicates that all seven elements are present in very high copy number, and that little sequence divergence (<5–8% based on assembly parameters) exists among individual copies. This suggests that all seven TE superfamilies have been recently active and/or continue to be active in our focal salamander species. We tested whether ongoing transcription of these same superfamilies was also occurring in Ambystoma mexicanum using TBlastX against the A. mexicanum transcriptome (http://www.ambystoma.org/genome-resources/21-blast [date last accessed 26 Sep 2011]) and confirmed transcripts of all seven superfamilies.


LTR retrotransposons contribute to genomic gigantism in plethodontid salamanders.

Sun C, Shepard DB, Chong RA, López Arriaza J, Hall K, Castoe TA, Feschotte C, Pollock DD, Mueller RL - Genome Biol Evol (2011)

The structures of seven full-length TE sequences mined from salamander shotgun reads. Abbreviations: gag, capsid-like protein; pro, protease; RT, reverse transcriptase; rve, integrase; ENV, envelope protein; YR, tyrosine recombinase; EN, endonuclease.
© Copyright Policy - creative-commons
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC3318908&req=5

fig2: The structures of seven full-length TE sequences mined from salamander shotgun reads. Abbreviations: gag, capsid-like protein; pro, protease; RT, reverse transcriptase; rve, integrase; ENV, envelope protein; YR, tyrosine recombinase; EN, endonuclease.
Mentions: In addition, the assembly step of our TE-mining pipeline allowed us to successfully generate seven putatively full-length elements, composite sequences representative of salamander TE superfamilies. After verification and refinement, we confirmed contigs representing full-length sequences of several superfamilies of Class I TEs: Ty3/gypsy, ERV1, DIRS, and Ngaro elements (LTR retrotransposons), as well as L1 and L2/CR1 elements (non-LTR retrotransposons). In addition, we confirmed contigs representing a full-length rolling circle Helitron (Class II TE). The structures of the seven full-length TEs we assembled are summarized in figure 2, and each is largely consistent with the structure reported for the same superfamily from other eukaryotic genomes. Sequences of these complete elements, as well as the full-length elements identified from Ambystoma mexicanum BAC clones, are available as supplementary file 2, Supplementary Material online. To our knowledge, this is the first description of the structure of full-length TEs in salamander genomes. Our successful assembly of full-length contigs from ∼1% genome coverage (using a stringent assembly algorithm) indicates that all seven elements are present in very high copy number, and that little sequence divergence (<5–8% based on assembly parameters) exists among individual copies. This suggests that all seven TE superfamilies have been recently active and/or continue to be active in our focal salamander species. We tested whether ongoing transcription of these same superfamilies was also occurring in Ambystoma mexicanum using TBlastX against the A. mexicanum transcriptome (http://www.ambystoma.org/genome-resources/21-blast [date last accessed 26 Sep 2011]) and confirmed transcripts of all seven superfamilies.

Bottom Line: The most abundant TE superfamilies found in the genomes of our six focal species are similar, despite substantial variation in genome size.However, our results demonstrate a major difference between salamanders and other vertebrates: salamander genomes contain much larger amounts of long terminal repeat (LTR) retrotransposons, primarily Ty3/gypsy elements.These results suggest that increased proliferation of LTR retrotransposons was a major molecular mechanism contributing to genomic expansion in salamanders.

View Article: PubMed Central - PubMed

Affiliation: Department of Biology, Colorado State University, CO, USA.

ABSTRACT
Among vertebrates, most of the largest genomes are found within the salamanders, a clade of amphibians that includes 613 species. Salamander genome sizes range from ~14 to ~120 Gb. Because genome size is correlated with nucleus and cell sizes, as well as other traits, morphological evolution in salamanders has been profoundly affected by genomic gigantism. However, the molecular mechanisms driving genomic expansion in this clade remain largely unknown. Here, we present the first comparative analysis of transposable element (TE) content in salamanders. Using high-throughput sequencing, we generated genomic shotgun data for six species from the Plethodontidae, the largest family of salamanders. We then developed a pipeline to mine TE sequences from shotgun data in taxa with limited genomic resources, such as salamanders. Our summaries of overall TE abundance and diversity for each species demonstrate that TEs make up a substantial portion of salamander genomes, and that all of the major known types of TEs are represented in salamanders. The most abundant TE superfamilies found in the genomes of our six focal species are similar, despite substantial variation in genome size. However, our results demonstrate a major difference between salamanders and other vertebrates: salamander genomes contain much larger amounts of long terminal repeat (LTR) retrotransposons, primarily Ty3/gypsy elements. Thus, the extreme increase in genome size that occurred in salamanders was likely accompanied by a shift in TE landscape. These results suggest that increased proliferation of LTR retrotransposons was a major molecular mechanism contributing to genomic expansion in salamanders.

Show MeSH
Related in: MedlinePlus