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Huntingtin gene evolution in Chordata and its peculiar features in the ascidian Ciona genus.

Gissi C, Pesole G, Cattaneo E, Tartari M - BMC Genomics (2006)

Bottom Line: The C. intestinalis htt transcript exhibits some peculiar features, such as spliced leader trans-splicing in the 98 nt-long 5' untranslated region (UTR), an alternative splicing in the coding region, eight alternative polyadenylation sites, and no similarities of both 5' and 3'UTRs compared to homologs of the cogeneric C. savignyi.On the contrary, the 3'-half of the gene is highly conserved in all chordates at the level of both gene structure and protein sequence.Between the two Ciona species, a fast evolutionary rate and/or an early divergence time is suggested by the absence of significant similarity between UTRs, protein divergence comparable to that observed between mammals and fishes, and different distribution of repetitive elements.

View Article: PubMed Central - HTML - PubMed

Affiliation: Dipartimento di Scienze Biomolecolari e Biotecnologie, Università di Milano, Milano, Italy. carmela.gissi@unimi.it <carmela.gissi@unimi.it>

ABSTRACT

Background: To gain insight into the evolutionary features of the huntingtin (htt) gene in Chordata, we have sequenced and characterized the full-length htt mRNA in the ascidian Ciona intestinalis, a basal chordate emerging as new invertebrate model organism. Moreover, taking advantage of the availability of genomic and EST sequences, the htt gene structure of a number of chordate species, including the cogeneric ascidian Ciona savignyi, and the vertebrates Xenopus and Gallus was reconstructed.

Results: The C. intestinalis htt transcript exhibits some peculiar features, such as spliced leader trans-splicing in the 98 nt-long 5' untranslated region (UTR), an alternative splicing in the coding region, eight alternative polyadenylation sites, and no similarities of both 5' and 3'UTRs compared to homologs of the cogeneric C. savignyi. The predicted protein is 2946 amino acids long, shorter than its vertebrate homologs, and lacks the polyQ and the polyP stretches found in the the N-terminal regions of mammalian homologs. The exon-intron organization of the htt gene is almost identical among vertebrates, and significantly conserved between Ciona and vertebrates, allowing us to hypothesize an ancestral chordate gene consisting of at least 40 coding exons.

Conclusion: During chordate diversification, events of gain/loss, sliding, phase changes, and expansion of introns occurred in both vertebrate and ascidian lineages predominantly in the 5'-half of the htt gene, where there is also evidence of lineage-specific evolutionary dynamics in vertebrates. On the contrary, the 3'-half of the gene is highly conserved in all chordates at the level of both gene structure and protein sequence. Between the two Ciona species, a fast evolutionary rate and/or an early divergence time is suggested by the absence of significant similarity between UTRs, protein divergence comparable to that observed between mammals and fishes, and different distribution of repetitive elements.

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Percentage amino acid identity calculated for each Equivalent exon (E, in yellow) and exon-Block (B, in gray). The percentage amino acid identity was calculated from the chordate protein alignment for each of the equivalent exons and exon-blocks described in Figure 1. Numbers refer to the Ciona exon numbering. Bold-dashed line represents the mean % identity (21.2%) calculated over the entire alignment length. Normal-dashed lines represent mean value +/- standard deviation (7.1).
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Figure 4: Percentage amino acid identity calculated for each Equivalent exon (E, in yellow) and exon-Block (B, in gray). The percentage amino acid identity was calculated from the chordate protein alignment for each of the equivalent exons and exon-blocks described in Figure 1. Numbers refer to the Ciona exon numbering. Bold-dashed line represents the mean % identity (21.2%) calculated over the entire alignment length. Normal-dashed lines represent mean value +/- standard deviation (7.1).

Mentions: The existence of a possible correlation between gene structure conservation and protein conservation was examined by calculating the percentage amino acid identity (% aa id) for each gene structural element shared by all chordates, that is equivalent exons and exon-blocks identified in Figure 3. Figure 4 reports the % aa identity for equivalent exons (E, in yellow) and exon-blocks (B, in gray) along the protein alignment, together with the mean % aa identity of the entire alignment (21.2 ± 7.1, bold dashed line in Figure 4). Equivalent exons are almost equally distributed above and below the mean % aa id, however the less conserved elements correspond to exon-blocks (B_8_9 and B_40_42), and the most conserved elements are equivalent exons (E_27, E_28, E_46, E_58 and E_59). Moreover, the most conserved equivalent exons belong to clusters of consecutive equivalent exons, indicative of a high conservation of gene structure, and are located in the central and C-terminal protein regions (Figure 4).


Huntingtin gene evolution in Chordata and its peculiar features in the ascidian Ciona genus.

Gissi C, Pesole G, Cattaneo E, Tartari M - BMC Genomics (2006)

Percentage amino acid identity calculated for each Equivalent exon (E, in yellow) and exon-Block (B, in gray). The percentage amino acid identity was calculated from the chordate protein alignment for each of the equivalent exons and exon-blocks described in Figure 1. Numbers refer to the Ciona exon numbering. Bold-dashed line represents the mean % identity (21.2%) calculated over the entire alignment length. Normal-dashed lines represent mean value +/- standard deviation (7.1).
© Copyright Policy - open-access
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC1636649&req=5

Figure 4: Percentage amino acid identity calculated for each Equivalent exon (E, in yellow) and exon-Block (B, in gray). The percentage amino acid identity was calculated from the chordate protein alignment for each of the equivalent exons and exon-blocks described in Figure 1. Numbers refer to the Ciona exon numbering. Bold-dashed line represents the mean % identity (21.2%) calculated over the entire alignment length. Normal-dashed lines represent mean value +/- standard deviation (7.1).
Mentions: The existence of a possible correlation between gene structure conservation and protein conservation was examined by calculating the percentage amino acid identity (% aa id) for each gene structural element shared by all chordates, that is equivalent exons and exon-blocks identified in Figure 3. Figure 4 reports the % aa identity for equivalent exons (E, in yellow) and exon-blocks (B, in gray) along the protein alignment, together with the mean % aa identity of the entire alignment (21.2 ± 7.1, bold dashed line in Figure 4). Equivalent exons are almost equally distributed above and below the mean % aa id, however the less conserved elements correspond to exon-blocks (B_8_9 and B_40_42), and the most conserved elements are equivalent exons (E_27, E_28, E_46, E_58 and E_59). Moreover, the most conserved equivalent exons belong to clusters of consecutive equivalent exons, indicative of a high conservation of gene structure, and are located in the central and C-terminal protein regions (Figure 4).

Bottom Line: The C. intestinalis htt transcript exhibits some peculiar features, such as spliced leader trans-splicing in the 98 nt-long 5' untranslated region (UTR), an alternative splicing in the coding region, eight alternative polyadenylation sites, and no similarities of both 5' and 3'UTRs compared to homologs of the cogeneric C. savignyi.On the contrary, the 3'-half of the gene is highly conserved in all chordates at the level of both gene structure and protein sequence.Between the two Ciona species, a fast evolutionary rate and/or an early divergence time is suggested by the absence of significant similarity between UTRs, protein divergence comparable to that observed between mammals and fishes, and different distribution of repetitive elements.

View Article: PubMed Central - HTML - PubMed

Affiliation: Dipartimento di Scienze Biomolecolari e Biotecnologie, Università di Milano, Milano, Italy. carmela.gissi@unimi.it <carmela.gissi@unimi.it>

ABSTRACT

Background: To gain insight into the evolutionary features of the huntingtin (htt) gene in Chordata, we have sequenced and characterized the full-length htt mRNA in the ascidian Ciona intestinalis, a basal chordate emerging as new invertebrate model organism. Moreover, taking advantage of the availability of genomic and EST sequences, the htt gene structure of a number of chordate species, including the cogeneric ascidian Ciona savignyi, and the vertebrates Xenopus and Gallus was reconstructed.

Results: The C. intestinalis htt transcript exhibits some peculiar features, such as spliced leader trans-splicing in the 98 nt-long 5' untranslated region (UTR), an alternative splicing in the coding region, eight alternative polyadenylation sites, and no similarities of both 5' and 3'UTRs compared to homologs of the cogeneric C. savignyi. The predicted protein is 2946 amino acids long, shorter than its vertebrate homologs, and lacks the polyQ and the polyP stretches found in the the N-terminal regions of mammalian homologs. The exon-intron organization of the htt gene is almost identical among vertebrates, and significantly conserved between Ciona and vertebrates, allowing us to hypothesize an ancestral chordate gene consisting of at least 40 coding exons.

Conclusion: During chordate diversification, events of gain/loss, sliding, phase changes, and expansion of introns occurred in both vertebrate and ascidian lineages predominantly in the 5'-half of the htt gene, where there is also evidence of lineage-specific evolutionary dynamics in vertebrates. On the contrary, the 3'-half of the gene is highly conserved in all chordates at the level of both gene structure and protein sequence. Between the two Ciona species, a fast evolutionary rate and/or an early divergence time is suggested by the absence of significant similarity between UTRs, protein divergence comparable to that observed between mammals and fishes, and different distribution of repetitive elements.

Show MeSH
Related in: MedlinePlus