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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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Amino acid alignment of CSTs found in intron 12. The Conserved Sequence Tag (CST) corresponds to an internal cassette exon (12Bis) in non-mammalian tetrapods and to a longest splicing isoform of exon 12 (12L) in pufferfishes. Identical, similar and conserved positions are indicated with different background.
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Figure 5: Amino acid alignment of CSTs found in intron 12. The Conserved Sequence Tag (CST) corresponds to an internal cassette exon (12Bis) in non-mammalian tetrapods and to a longest splicing isoform of exon 12 (12L) in pufferfishes. Identical, similar and conserved positions are indicated with different background.

Mentions: A search for sequence similarities in intronic regions does not identify conserved sequence tags (CSTs) between the two Ciona species, nor between vertebrates and ascidians. On the contrary, intron 12 of vertebrates contains interesting CSTs in more than one species pair (Figure 5). Indeed, CSTs ranging from 102 to 177 bp were found in intron 12 in the species pairs Xenopus-Gallus, Tetraodon-Fugu, and Mus-Rattus. The Xenopus-Gallus CST has a high coding potential (CPS = 7.16) [31], whereas the Tetraodon-Fugu CST exhibits a marginal coding potential (CPS = 6.77), and the rodent CST is clearly non-coding, as indicated by a low CPS value (5.89). Moreover, the Xenopus-Gallus CST shows 34% amino acid sequence similarity to the CST of pufferfishes but no similarity to the rodent CST. The presence of a coding sequence in intron 12 is further confirmed by the prediction of a competing 5' splice site in exon 12 of Xenopus and Gallus, and of an internal cassette exon (that we called exon 12bis) in the two pufferfish species (SGP2 results), with all new putative introns following the GT-AG rule. This coding region, present only in some non-mammalian vertebrates and showing a low amino acid similarity (Figure 5), suggests the existence of an alternative splicing isoform due to a species-specific additional or longer exon located in intron 12.


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)

Amino acid alignment of CSTs found in intron 12. The Conserved Sequence Tag (CST) corresponds to an internal cassette exon (12Bis) in non-mammalian tetrapods and to a longest splicing isoform of exon 12 (12L) in pufferfishes. Identical, similar and conserved positions are indicated with different background.
© Copyright Policy - open-access
Related In: Results  -  Collection

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

Figure 5: Amino acid alignment of CSTs found in intron 12. The Conserved Sequence Tag (CST) corresponds to an internal cassette exon (12Bis) in non-mammalian tetrapods and to a longest splicing isoform of exon 12 (12L) in pufferfishes. Identical, similar and conserved positions are indicated with different background.
Mentions: A search for sequence similarities in intronic regions does not identify conserved sequence tags (CSTs) between the two Ciona species, nor between vertebrates and ascidians. On the contrary, intron 12 of vertebrates contains interesting CSTs in more than one species pair (Figure 5). Indeed, CSTs ranging from 102 to 177 bp were found in intron 12 in the species pairs Xenopus-Gallus, Tetraodon-Fugu, and Mus-Rattus. The Xenopus-Gallus CST has a high coding potential (CPS = 7.16) [31], whereas the Tetraodon-Fugu CST exhibits a marginal coding potential (CPS = 6.77), and the rodent CST is clearly non-coding, as indicated by a low CPS value (5.89). Moreover, the Xenopus-Gallus CST shows 34% amino acid sequence similarity to the CST of pufferfishes but no similarity to the rodent CST. The presence of a coding sequence in intron 12 is further confirmed by the prediction of a competing 5' splice site in exon 12 of Xenopus and Gallus, and of an internal cassette exon (that we called exon 12bis) in the two pufferfish species (SGP2 results), with all new putative introns following the GT-AG rule. This coding region, present only in some non-mammalian vertebrates and showing a low amino acid similarity (Figure 5), suggests the existence of an alternative splicing isoform due to a species-specific additional or longer exon located in intron 12.

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