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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 preprodynorphin 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. Dynorphin-like motifs (YGGF…) are shaded.
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pone-0010512-g003: Alignment of the preprodynorphin 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. Dynorphin-like motifs (YGGF…) are shaded.

Mentions: The PDYN gene (Fig. 3) encodes three opioid core motifs in placental mammals and two more in opossum and amphibians. The PDYN gene is missing in the chicken genome, but a portion of PDYN was detected in the zebra finch genome by using BLAST searches. This fragment includes the sequences for dynorphin A and dynorphin B and is located on chromosome 20, a chromosome that displays conserved synteny to chicken chromosome 20 (data not shown), indicating that the PDYN gene once was located there in chicken, on the same chromosome as the gene for the orphanin receptor. Due to the poor assembly of the western clawed frog genome it was only possible to detect a partial dynorphin sequence, but full length sequences have previously been found in other amphibians [27], [28]. The first and second opioid core sequences in PDYN have previously been defined as a relic sequences in mammals [25] but they are less degenerate in opossum and intact in amphibians and teleost fishes (Fig. 3). The zebra finch sequence does not cover this part of the alignment, but the core sequence is intact in the green anole lizard (Anolis carolinensis) (data not shown). Stickleback and medaka have a deviating second core sequence as described earlier for eel, tilapia and zebrafish [25], [29]. This core sequence is intact in amphibians and less degenerate in opossum than in placental mammals (Fig. 3).


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 preprodynorphin 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. Dynorphin-like motifs (YGGF…) are shaded.
© Copyright Policy
Related In: Results  -  Collection

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

pone-0010512-g003: Alignment of the preprodynorphin 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. Dynorphin-like motifs (YGGF…) are shaded.
Mentions: The PDYN gene (Fig. 3) encodes three opioid core motifs in placental mammals and two more in opossum and amphibians. The PDYN gene is missing in the chicken genome, but a portion of PDYN was detected in the zebra finch genome by using BLAST searches. This fragment includes the sequences for dynorphin A and dynorphin B and is located on chromosome 20, a chromosome that displays conserved synteny to chicken chromosome 20 (data not shown), indicating that the PDYN gene once was located there in chicken, on the same chromosome as the gene for the orphanin receptor. Due to the poor assembly of the western clawed frog genome it was only possible to detect a partial dynorphin sequence, but full length sequences have previously been found in other amphibians [27], [28]. The first and second opioid core sequences in PDYN have previously been defined as a relic sequences in mammals [25] but they are less degenerate in opossum and intact in amphibians and teleost fishes (Fig. 3). The zebra finch sequence does not cover this part of the alignment, but the core sequence is intact in the green anole lizard (Anolis carolinensis) (data not shown). Stickleback and medaka have a deviating second core sequence as described earlier for eel, tilapia and zebrafish [25], [29]. This core sequence is intact in amphibians and less degenerate in opossum than in placental mammals (Fig. 3).

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