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The non-LTR retrotransposons in Ciona intestinalis: new insights into the evolution of chordate genomes.

Permanyer J, Gonzàlez-Duarte R, Albalat R - Genome Biol. (2003)

Bottom Line: The copy number per haploid genome of each element is low, less than 100, far below the values reported for vertebrate counterparts but within the range for protostomes.Genomic and sequence analysis shows that the ascidian non-LTR elements are unmethylated and flanked by genomic segments with a gene density lower than average for the genome.The analysis provides valuable data for understanding the evolution of early chordate genomes and enlarges the view on the distribution of the non-LTR retrotransposons in eukaryotes.

View Article: PubMed Central - HTML - PubMed

Affiliation: Departament de Genètica, Facultat de Biologia, Universitat de Barcelona, Av Diagonal 645, E-08028 Barcelona, Spain.

ABSTRACT

Background: Non-long terminal repeat (non-LTR) retrotransposons have contributed to shaping the structure and function of genomes. In silico and experimental approaches have been used to identify the non-LTR elements of the urochordate Ciona intestinalis. Knowledge of the types and abundance of non-LTR elements in urochordates is a key step in understanding their contribution to the structure and function of vertebrate genomes.

Results: Consensus elements phylogenetically related to the I, LINE1, LINE2, LOA and R2 elements of the 14 eukaryotic non-LTR clades are described from C. intestinalis. The ascidian elements showed conservation of both the reverse transcriptase coding sequence and the overall structural organization seen in each clade. The apurinic/apyrimidinic endonuclease and nucleic-acid-binding domains encoded upstream of the reverse transcriptase, and the RNase H and the restriction enzyme-like endonuclease motifs encoded downstream of the reverse transcriptase were identified in the corresponding Ciona families.

Conclusions: The genome of C. intestinalis harbors representatives of at least five clades of non-LTR retrotransposons. The copy number per haploid genome of each element is low, less than 100, far below the values reported for vertebrate counterparts but within the range for protostomes. Genomic and sequence analysis shows that the ascidian non-LTR elements are unmethylated and flanked by genomic segments with a gene density lower than average for the genome. The analysis provides valuable data for understanding the evolution of early chordate genomes and enlarges the view on the distribution of the non-LTR retrotransposons in eukaryotes.

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Multiple-sequence alignments of the Ciona non-LTR retrotransposons. (a) The APE region. Only blocks of highly similar residues are shown. The Roman numerals above the alignments correspond to those defined by Tu et al. [17]. Highly conserved residues, as convenient landmarks, are shaded. (b) Reverse transcriptase sequences. Numbers above the sequences and the black-shaded residues refer to the conserved peaks described by Malik et al. [11]. Gray-shaded residues correspond to the CRE/R2/R4/L1/RTE and Tad/R1/LOA/Jockey/CR1/I subgroups described in [11]. (c) CiR2 domains. The CCHH and c-Myb DNA-binding motifs are shown in the amino-terminal domain and the REL-endo domain with the CCHC and KPDI motifs in the carboxy-terminal domain [18]. (d) CiLOA and CiI RNH domains. Only the highly conserved regions of the RNase H domain of the blocks defined by Tu et al. [17] are depicted. The three amino-acid residues identified in the active site of E. coli RNase H are shaded. (e) CCHC motif of the putative CiI-ORF1 as defined by Fawcett et al. [32].
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Figure 2: Multiple-sequence alignments of the Ciona non-LTR retrotransposons. (a) The APE region. Only blocks of highly similar residues are shown. The Roman numerals above the alignments correspond to those defined by Tu et al. [17]. Highly conserved residues, as convenient landmarks, are shaded. (b) Reverse transcriptase sequences. Numbers above the sequences and the black-shaded residues refer to the conserved peaks described by Malik et al. [11]. Gray-shaded residues correspond to the CRE/R2/R4/L1/RTE and Tad/R1/LOA/Jockey/CR1/I subgroups described in [11]. (c) CiR2 domains. The CCHH and c-Myb DNA-binding motifs are shown in the amino-terminal domain and the REL-endo domain with the CCHC and KPDI motifs in the carboxy-terminal domain [18]. (d) CiLOA and CiI RNH domains. Only the highly conserved regions of the RNase H domain of the blocks defined by Tu et al. [17] are depicted. The three amino-acid residues identified in the active site of E. coli RNase H are shaded. (e) CCHC motif of the putative CiI-ORF1 as defined by Fawcett et al. [32].

Mentions: Five consensus non-LTR retrotransposons, termed CiI, CiL1, CiL2, CiLOA and CiR2, were derived from five, five, six, five and five C. intestinalis scaffolds, respectively (Figures 1, 2 and see Additional data file 1). TBLASTX comparisons showed that the ascidian elements belonged to the I, LINE1, LINE2, LOA and R2 clades (E-values: 4e-69 with Biomphalaria glabrata (snail) BGR, 2e-89 with Nycticebus coucang (slow loris) L1, 2e-50 with Danio rerio CR1Dr2, e-146 with Aedes aegypti Lian, and e-106 with Drosophila melanogaster R2, respectively). CiL1.2 (Figure 2b), derived from five scaffolds, was another ascidian LINE1 element. It showed homology with the Xenopus laevis Tx1 retroelement (E-value: 2e-40) but was not further analyzed because it was significantly shorter than CiL1 (CiL1.2 only encompassed the reverse transcriptase region).


The non-LTR retrotransposons in Ciona intestinalis: new insights into the evolution of chordate genomes.

Permanyer J, Gonzàlez-Duarte R, Albalat R - Genome Biol. (2003)

Multiple-sequence alignments of the Ciona non-LTR retrotransposons. (a) The APE region. Only blocks of highly similar residues are shown. The Roman numerals above the alignments correspond to those defined by Tu et al. [17]. Highly conserved residues, as convenient landmarks, are shaded. (b) Reverse transcriptase sequences. Numbers above the sequences and the black-shaded residues refer to the conserved peaks described by Malik et al. [11]. Gray-shaded residues correspond to the CRE/R2/R4/L1/RTE and Tad/R1/LOA/Jockey/CR1/I subgroups described in [11]. (c) CiR2 domains. The CCHH and c-Myb DNA-binding motifs are shown in the amino-terminal domain and the REL-endo domain with the CCHC and KPDI motifs in the carboxy-terminal domain [18]. (d) CiLOA and CiI RNH domains. Only the highly conserved regions of the RNase H domain of the blocks defined by Tu et al. [17] are depicted. The three amino-acid residues identified in the active site of E. coli RNase H are shaded. (e) CCHC motif of the putative CiI-ORF1 as defined by Fawcett et al. [32].
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Related In: Results  -  Collection

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Figure 2: Multiple-sequence alignments of the Ciona non-LTR retrotransposons. (a) The APE region. Only blocks of highly similar residues are shown. The Roman numerals above the alignments correspond to those defined by Tu et al. [17]. Highly conserved residues, as convenient landmarks, are shaded. (b) Reverse transcriptase sequences. Numbers above the sequences and the black-shaded residues refer to the conserved peaks described by Malik et al. [11]. Gray-shaded residues correspond to the CRE/R2/R4/L1/RTE and Tad/R1/LOA/Jockey/CR1/I subgroups described in [11]. (c) CiR2 domains. The CCHH and c-Myb DNA-binding motifs are shown in the amino-terminal domain and the REL-endo domain with the CCHC and KPDI motifs in the carboxy-terminal domain [18]. (d) CiLOA and CiI RNH domains. Only the highly conserved regions of the RNase H domain of the blocks defined by Tu et al. [17] are depicted. The three amino-acid residues identified in the active site of E. coli RNase H are shaded. (e) CCHC motif of the putative CiI-ORF1 as defined by Fawcett et al. [32].
Mentions: Five consensus non-LTR retrotransposons, termed CiI, CiL1, CiL2, CiLOA and CiR2, were derived from five, five, six, five and five C. intestinalis scaffolds, respectively (Figures 1, 2 and see Additional data file 1). TBLASTX comparisons showed that the ascidian elements belonged to the I, LINE1, LINE2, LOA and R2 clades (E-values: 4e-69 with Biomphalaria glabrata (snail) BGR, 2e-89 with Nycticebus coucang (slow loris) L1, 2e-50 with Danio rerio CR1Dr2, e-146 with Aedes aegypti Lian, and e-106 with Drosophila melanogaster R2, respectively). CiL1.2 (Figure 2b), derived from five scaffolds, was another ascidian LINE1 element. It showed homology with the Xenopus laevis Tx1 retroelement (E-value: 2e-40) but was not further analyzed because it was significantly shorter than CiL1 (CiL1.2 only encompassed the reverse transcriptase region).

Bottom Line: The copy number per haploid genome of each element is low, less than 100, far below the values reported for vertebrate counterparts but within the range for protostomes.Genomic and sequence analysis shows that the ascidian non-LTR elements are unmethylated and flanked by genomic segments with a gene density lower than average for the genome.The analysis provides valuable data for understanding the evolution of early chordate genomes and enlarges the view on the distribution of the non-LTR retrotransposons in eukaryotes.

View Article: PubMed Central - HTML - PubMed

Affiliation: Departament de Genètica, Facultat de Biologia, Universitat de Barcelona, Av Diagonal 645, E-08028 Barcelona, Spain.

ABSTRACT

Background: Non-long terminal repeat (non-LTR) retrotransposons have contributed to shaping the structure and function of genomes. In silico and experimental approaches have been used to identify the non-LTR elements of the urochordate Ciona intestinalis. Knowledge of the types and abundance of non-LTR elements in urochordates is a key step in understanding their contribution to the structure and function of vertebrate genomes.

Results: Consensus elements phylogenetically related to the I, LINE1, LINE2, LOA and R2 elements of the 14 eukaryotic non-LTR clades are described from C. intestinalis. The ascidian elements showed conservation of both the reverse transcriptase coding sequence and the overall structural organization seen in each clade. The apurinic/apyrimidinic endonuclease and nucleic-acid-binding domains encoded upstream of the reverse transcriptase, and the RNase H and the restriction enzyme-like endonuclease motifs encoded downstream of the reverse transcriptase were identified in the corresponding Ciona families.

Conclusions: The genome of C. intestinalis harbors representatives of at least five clades of non-LTR retrotransposons. The copy number per haploid genome of each element is low, less than 100, far below the values reported for vertebrate counterparts but within the range for protostomes. Genomic and sequence analysis shows that the ascidian non-LTR elements are unmethylated and flanked by genomic segments with a gene density lower than average for the genome. The analysis provides valuable data for understanding the evolution of early chordate genomes and enlarges the view on the distribution of the non-LTR retrotransposons in eukaryotes.

Show MeSH