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Sequence and organization of coelacanth neurohypophysial hormone genes: evolutionary history of the vertebrate neurohypophysial hormone gene locus.

Gwee PC, Amemiya CT, Brenner S, Venkatesh B - BMC Evol. Biol. (2008)

Bottom Line: Our results indicate that the neurohypophysial hormone gene locus has experienced independent rearrangements in both placental mammals and teleost fishes.The coelacanth genome appears to be more stable than mammalian and teleost fish genomes.As such, it serves as a valuable outgroup for studying the evolution of mammalian and teleost fish genomes.

View Article: PubMed Central - HTML - PubMed

Affiliation: Institute of Molecular and Cell Biology, A*STAR (Agency for Science, Technology and Research), Biopolis, 138673, Singapore. pcgwee@imcb.a-star.edu.sg

ABSTRACT

Background: The mammalian neurohypophysial hormones, vasopressin and oxytocin are involved in osmoregulation and uterine smooth muscle contraction respectively. All jawed vertebrates contain at least one homolog each of vasopressin and oxytocin whereas jawless vertebrates contain a single neurohypophysial hormone called vasotocin. The vasopressin homolog in non-mammalian vertebrates is vasotocin; and the oxytocin homolog is mesotocin in non-eutherian tetrapods, mesotocin and [Phe2]mesotocin in lungfishes, and isotocin in ray-finned fishes. The genes encoding vasopressin and oxytocin genes are closely linked in the human and rodent genomes in a tail-to-tail orientation. In contrast, their pufferfish homologs (vasotocin and isotocin) are located on the same strand of DNA with isotocin gene located upstream of vasotocin gene separated by five genes, suggesting that this locus has experienced rearrangements in either mammalian or ray-finned fish lineage, or in both lineages. The coelacanths occupy a unique phylogenetic position close to the divergence of the mammalian and ray-finned fish lineages.

Results: We have sequenced a coelacanth (Latimeria menadoensis) BAC clone encompassing the neurohypophysial hormone genes and investigated the evolutionary history of the vertebrate neurohypophysial hormone gene locus within a comparative genomics framework. The coelacanth contains vasotocin and mesotocin genes like non-mammalian tetrapods. The coelacanth genes are present on the same strand of DNA with no intervening genes, with the vasotocin gene located upstream of the mesotocin gene. Nucleotide sequences of the second exons of the two genes are under purifying selection implying a regulatory function. We have also analyzed the neurohypophysial hormone gene locus in the genomes of opossum, chicken and Xenopus tropicalis. The opossum contains two tandem copies of vasopressin and mesotocin genes. The vasotocin and mesotocin genes in chicken and Xenopus, and the vasopressin and mesotocin genes in opossum are linked tail-to-head similar to their orthologs in coelacanth and unlike their homologs in human and rodents.

Conclusion: Our results indicate that the neurohypophysial hormone gene locus has experienced independent rearrangements in both placental mammals and teleost fishes. The coelacanth genome appears to be more stable than mammalian and teleost fish genomes. As such, it serves as a valuable outgroup for studying the evolution of mammalian and teleost fish genomes.

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Comparison of nucleotide and deduced amino acid sequences of coelacanth vasotocin and mesotocin genes. Conserved nucleotides are indicated by an asterisk and identical amino acid residues are shown in bold font. Sequential Arg residues, N-glycosylation sites and Leu-rich core segment in the vasotocin precursor are boxed. The sequential Arg residues serve as a processing signal between the neurophysin and copeptin. Intronic sequences are shown in lower case.
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Figure 3: Comparison of nucleotide and deduced amino acid sequences of coelacanth vasotocin and mesotocin genes. Conserved nucleotides are indicated by an asterisk and identical amino acid residues are shown in bold font. Sequential Arg residues, N-glycosylation sites and Leu-rich core segment in the vasotocin precursor are boxed. The sequential Arg residues serve as a processing signal between the neurophysin and copeptin. Intronic sequences are shown in lower case.

Mentions: The coelacanth vasotocin gene encodes a 162-amino acid protein comprising a signal peptide, vasotocin, a neurophysin and a copeptin moiety (Fig 3). Vasotocin is linked to the neurophysin by a tripeptide sequence Gly-Lys-Arg which serves as a signal for proteolytic processing and carboxyl-terminal amidation of vasotocin (Fig 3). The two arginine residues at the end of the neurophysin (Figs 3 and 4A) are likely to serve as a processing signal between the neurophysin and the copeptin. All the cysteine residues that are considered important for the conformation of neurophysin are conserved in the coelacanth vasotocin neurophysin (Figs 3 and 4A). The copeptin includes a leucine-rich core segment like the copeptin of vasopressin-family precursors in other vertebrates, and an N-linked glycosylation site that is conserved in tetrapods, Australian lungfish and dogfish but absent in teleost fishes (Fig 4A).


Sequence and organization of coelacanth neurohypophysial hormone genes: evolutionary history of the vertebrate neurohypophysial hormone gene locus.

Gwee PC, Amemiya CT, Brenner S, Venkatesh B - BMC Evol. Biol. (2008)

Comparison of nucleotide and deduced amino acid sequences of coelacanth vasotocin and mesotocin genes. Conserved nucleotides are indicated by an asterisk and identical amino acid residues are shown in bold font. Sequential Arg residues, N-glycosylation sites and Leu-rich core segment in the vasotocin precursor are boxed. The sequential Arg residues serve as a processing signal between the neurophysin and copeptin. Intronic sequences are shown in lower case.
© Copyright Policy - open-access
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC2315648&req=5

Figure 3: Comparison of nucleotide and deduced amino acid sequences of coelacanth vasotocin and mesotocin genes. Conserved nucleotides are indicated by an asterisk and identical amino acid residues are shown in bold font. Sequential Arg residues, N-glycosylation sites and Leu-rich core segment in the vasotocin precursor are boxed. The sequential Arg residues serve as a processing signal between the neurophysin and copeptin. Intronic sequences are shown in lower case.
Mentions: The coelacanth vasotocin gene encodes a 162-amino acid protein comprising a signal peptide, vasotocin, a neurophysin and a copeptin moiety (Fig 3). Vasotocin is linked to the neurophysin by a tripeptide sequence Gly-Lys-Arg which serves as a signal for proteolytic processing and carboxyl-terminal amidation of vasotocin (Fig 3). The two arginine residues at the end of the neurophysin (Figs 3 and 4A) are likely to serve as a processing signal between the neurophysin and the copeptin. All the cysteine residues that are considered important for the conformation of neurophysin are conserved in the coelacanth vasotocin neurophysin (Figs 3 and 4A). The copeptin includes a leucine-rich core segment like the copeptin of vasopressin-family precursors in other vertebrates, and an N-linked glycosylation site that is conserved in tetrapods, Australian lungfish and dogfish but absent in teleost fishes (Fig 4A).

Bottom Line: Our results indicate that the neurohypophysial hormone gene locus has experienced independent rearrangements in both placental mammals and teleost fishes.The coelacanth genome appears to be more stable than mammalian and teleost fish genomes.As such, it serves as a valuable outgroup for studying the evolution of mammalian and teleost fish genomes.

View Article: PubMed Central - HTML - PubMed

Affiliation: Institute of Molecular and Cell Biology, A*STAR (Agency for Science, Technology and Research), Biopolis, 138673, Singapore. pcgwee@imcb.a-star.edu.sg

ABSTRACT

Background: The mammalian neurohypophysial hormones, vasopressin and oxytocin are involved in osmoregulation and uterine smooth muscle contraction respectively. All jawed vertebrates contain at least one homolog each of vasopressin and oxytocin whereas jawless vertebrates contain a single neurohypophysial hormone called vasotocin. The vasopressin homolog in non-mammalian vertebrates is vasotocin; and the oxytocin homolog is mesotocin in non-eutherian tetrapods, mesotocin and [Phe2]mesotocin in lungfishes, and isotocin in ray-finned fishes. The genes encoding vasopressin and oxytocin genes are closely linked in the human and rodent genomes in a tail-to-tail orientation. In contrast, their pufferfish homologs (vasotocin and isotocin) are located on the same strand of DNA with isotocin gene located upstream of vasotocin gene separated by five genes, suggesting that this locus has experienced rearrangements in either mammalian or ray-finned fish lineage, or in both lineages. The coelacanths occupy a unique phylogenetic position close to the divergence of the mammalian and ray-finned fish lineages.

Results: We have sequenced a coelacanth (Latimeria menadoensis) BAC clone encompassing the neurohypophysial hormone genes and investigated the evolutionary history of the vertebrate neurohypophysial hormone gene locus within a comparative genomics framework. The coelacanth contains vasotocin and mesotocin genes like non-mammalian tetrapods. The coelacanth genes are present on the same strand of DNA with no intervening genes, with the vasotocin gene located upstream of the mesotocin gene. Nucleotide sequences of the second exons of the two genes are under purifying selection implying a regulatory function. We have also analyzed the neurohypophysial hormone gene locus in the genomes of opossum, chicken and Xenopus tropicalis. The opossum contains two tandem copies of vasopressin and mesotocin genes. The vasotocin and mesotocin genes in chicken and Xenopus, and the vasopressin and mesotocin genes in opossum are linked tail-to-head similar to their orthologs in coelacanth and unlike their homologs in human and rodents.

Conclusion: Our results indicate that the neurohypophysial hormone gene locus has experienced independent rearrangements in both placental mammals and teleost fishes. The coelacanth genome appears to be more stable than mammalian and teleost fish genomes. As such, it serves as a valuable outgroup for studying the evolution of mammalian and teleost fish genomes.

Show MeSH
Related in: MedlinePlus