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Concomitant duplications of opioid peptide and receptor genes before the origin of jawed vertebrates.

Sundström G, Dreborg S, Larhammar D - PLoS ONE (2010)

Bottom Line: The results show that the ancestral peptide gene gave rise to two additional copies in the genome doublings.However, subsequently genetic linkage has been lost.In conclusion, the system of opioid peptides and receptors was largely formed by the genome doublings that took place early in vertebrate evolution.

View Article: PubMed Central - PubMed

Affiliation: Department of Neuroscience, Uppsala University, Uppsala, Sweden.

ABSTRACT

Background: The opioid system is involved in reward and pain mechanisms and consists in mammals of four receptors and several peptides. The peptides are derived from four prepropeptide genes, PENK, PDYN, PNOC and POMC, encoding enkephalins, dynorphins, orphanin/nociceptin and beta-endorphin, respectively. Previously we have described how two rounds of genome doubling (2R) before the origin of jawed vertebrates formed the receptor family.

Methodology/principal findings: Opioid peptide gene family members were investigated using a combination of sequence-based phylogeny and chromosomal locations of the peptide genes in various vertebrates. Several adjacent gene families were investigated similarly. The results show that the ancestral peptide gene gave rise to two additional copies in the genome doublings. The fourth member was generated by a local gene duplication, as the genes encoding POMC and PNOC are located on the same chromosome in the chicken genome and all three teleost genomes that we have studied. A translocation has disrupted this synteny in mammals. The PDYN gene seems to have been lost in chicken, but not in zebra finch. Duplicates of some peptide genes have arisen in the teleost fishes. Within the prepropeptide precursors, peptides have been lost or gained in different lineages.

Conclusions/significance: The ancestral peptide and receptor genes were located on the same chromosome and were thus duplicated concomitantly. However, subsequently genetic linkage has been lost. In conclusion, the system of opioid peptides and receptors was largely formed by the genome doublings that took place early in vertebrate evolution.

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Alignment of the proopioimelanocortin protein sequences.Conserved cysteines in the N-terminal region are marked with an asterisk and regions corresponding to known mature peptides in either of the sequences are boxed. Enkephalin motifs (YGGFM) are shaded.
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pone-0010512-g005: Alignment of the proopioimelanocortin protein sequences.Conserved cysteines in the N-terminal region are marked with an asterisk and regions corresponding to known mature peptides in either of the sequences are boxed. Enkephalin motifs (YGGFM) are shaded.

Mentions: The POMC precursor contains a single opioid core sequence as part of endorphin and, in addition, 2–4 melanocortin motifs (HFRW). The number of melanocortin peptides varies depending on species. The gene is located next to the PNOC gene in chicken and in the teleost fishes, suggesting that these two genes are a result of a local duplication. Duplicates of the zebrafish POMC gene have previously been cloned and 3R has been suggested as the origin of the duplicates [33]. Our analysis confirms this and it was also possible to detect duplicates in medaka and stickleback. We have named the duplicates POMCa and POMCb in accordance with the PNOC genes (Fig. 5).


Concomitant duplications of opioid peptide and receptor genes before the origin of jawed vertebrates.

Sundström G, Dreborg S, Larhammar D - PLoS ONE (2010)

Alignment of the proopioimelanocortin protein sequences.Conserved cysteines in the N-terminal region are marked with an asterisk and regions corresponding to known mature peptides in either of the sequences are boxed. Enkephalin motifs (YGGFM) are shaded.
© Copyright Policy
Related In: Results  -  Collection

Show All Figures
getmorefigures.php?uid=PMC2865548&req=5

pone-0010512-g005: Alignment of the proopioimelanocortin protein sequences.Conserved cysteines in the N-terminal region are marked with an asterisk and regions corresponding to known mature peptides in either of the sequences are boxed. Enkephalin motifs (YGGFM) are shaded.
Mentions: The POMC precursor contains a single opioid core sequence as part of endorphin and, in addition, 2–4 melanocortin motifs (HFRW). The number of melanocortin peptides varies depending on species. The gene is located next to the PNOC gene in chicken and in the teleost fishes, suggesting that these two genes are a result of a local duplication. Duplicates of the zebrafish POMC gene have previously been cloned and 3R has been suggested as the origin of the duplicates [33]. Our analysis confirms this and it was also possible to detect duplicates in medaka and stickleback. We have named the duplicates POMCa and POMCb in accordance with the PNOC genes (Fig. 5).

Bottom Line: The results show that the ancestral peptide gene gave rise to two additional copies in the genome doublings.However, subsequently genetic linkage has been lost.In conclusion, the system of opioid peptides and receptors was largely formed by the genome doublings that took place early in vertebrate evolution.

View Article: PubMed Central - PubMed

Affiliation: Department of Neuroscience, Uppsala University, Uppsala, Sweden.

ABSTRACT

Background: The opioid system is involved in reward and pain mechanisms and consists in mammals of four receptors and several peptides. The peptides are derived from four prepropeptide genes, PENK, PDYN, PNOC and POMC, encoding enkephalins, dynorphins, orphanin/nociceptin and beta-endorphin, respectively. Previously we have described how two rounds of genome doubling (2R) before the origin of jawed vertebrates formed the receptor family.

Methodology/principal findings: Opioid peptide gene family members were investigated using a combination of sequence-based phylogeny and chromosomal locations of the peptide genes in various vertebrates. Several adjacent gene families were investigated similarly. The results show that the ancestral peptide gene gave rise to two additional copies in the genome doublings. The fourth member was generated by a local gene duplication, as the genes encoding POMC and PNOC are located on the same chromosome in the chicken genome and all three teleost genomes that we have studied. A translocation has disrupted this synteny in mammals. The PDYN gene seems to have been lost in chicken, but not in zebra finch. Duplicates of some peptide genes have arisen in the teleost fishes. Within the prepropeptide precursors, peptides have been lost or gained in different lineages.

Conclusions/significance: The ancestral peptide and receptor genes were located on the same chromosome and were thus duplicated concomitantly. However, subsequently genetic linkage has been lost. In conclusion, the system of opioid peptides and receptors was largely formed by the genome doublings that took place early in vertebrate evolution.

Show MeSH