TY - JOUR
T1 - Evolution of multiple phosphodiesterase isoforms in stickleback involved in cAMP signal transduction pathway
AU - Sato, Yukuto
AU - Hashiguchi, Yasuyuki
AU - Nishida, Mutsumi
N1 - Funding Information:
The Tetraodon, stickleback, medaka, and zebrafish sequence data were produced by Genoscope and the Broad Institute, the Broad Institute, and the National Institute of Genetics, Japan, and the Sanger Institute respectively. The frog, chicken, and human sequence data were produced by the Joint Genome Institute, the Genome Sequencing Center at Washington University, St Louis, and the International Human Genome Sequencing Consortium, respectively. We thank our colleagues at the Ocean Research Institute of the University of Tokyo for helpful discussions. This work was supported by Grants-in-Aid from the Japan Society for the Promotion of Science to MN.
PY - 2009/2/20
Y1 - 2009/2/20
N2 - Background: Duplicate genes are considered to have evolved through the partitioning of ancestral functions among duplicates (subfunctionalization) and/or the acquisition of novel functions from a beneficial mutation (neofunctionalization). Additionally, an increase in gene dosage resulting from duplication may also confer an advantageous effect, as has been suggested for histone, tRNA, and rRNA genes. Currently, there is little understanding of the effect of increased gene dosage on subcellular networks like signal transduction pathways. Addressing this issue may provide further insights into the evolution by gene duplication. Results: We analyzed the evolution of multiple stickleback phosphodiesterase (PDE, EC: 3.1.4.17) 1C genes involved in the cyclic nucleotide signaling pathway. Stickleback has 8-9 copies of this gene, whereas only one or two loci exist in other model vertebrates. Our phylogenetic and synteny analyses suggested that the multiple PDE1C genes in stickleback were generated by repeated duplications of >100-kbp chromosome segments. Sequence evolution analysis did not provide strong evidence for neofunctionalization in the coding sequences of stickleback PDE1C isoforms. On the other hand, gene expression analysis suggested that the derived isoforms acquired expression in new organs, implying their neofunctionalization in terms of expression patterns. In addition, at least seven isoforms of the stickleback PDE1C were co-expressed with olfactory-type G-proteins in the nose, suggesting that PDE1C dosage is increased in the stickleback olfactory transduction (OT) pathway. In silico simulations of OT implied that the increased PDE1C dosage extends the longevity of the depolarization signals of the olfactory receptor neuron. Conclusion: The predicted effect of the increase in PDE1C products on the OT pathway may play an important role in stickleback behavior and ecology. However, this possibility should be empirically examined. Our analyses imply that an increase in gene product sometimes has a significant, yet unexpected, effect on the functions of subcellular networks.
AB - Background: Duplicate genes are considered to have evolved through the partitioning of ancestral functions among duplicates (subfunctionalization) and/or the acquisition of novel functions from a beneficial mutation (neofunctionalization). Additionally, an increase in gene dosage resulting from duplication may also confer an advantageous effect, as has been suggested for histone, tRNA, and rRNA genes. Currently, there is little understanding of the effect of increased gene dosage on subcellular networks like signal transduction pathways. Addressing this issue may provide further insights into the evolution by gene duplication. Results: We analyzed the evolution of multiple stickleback phosphodiesterase (PDE, EC: 3.1.4.17) 1C genes involved in the cyclic nucleotide signaling pathway. Stickleback has 8-9 copies of this gene, whereas only one or two loci exist in other model vertebrates. Our phylogenetic and synteny analyses suggested that the multiple PDE1C genes in stickleback were generated by repeated duplications of >100-kbp chromosome segments. Sequence evolution analysis did not provide strong evidence for neofunctionalization in the coding sequences of stickleback PDE1C isoforms. On the other hand, gene expression analysis suggested that the derived isoforms acquired expression in new organs, implying their neofunctionalization in terms of expression patterns. In addition, at least seven isoforms of the stickleback PDE1C were co-expressed with olfactory-type G-proteins in the nose, suggesting that PDE1C dosage is increased in the stickleback olfactory transduction (OT) pathway. In silico simulations of OT implied that the increased PDE1C dosage extends the longevity of the depolarization signals of the olfactory receptor neuron. Conclusion: The predicted effect of the increase in PDE1C products on the OT pathway may play an important role in stickleback behavior and ecology. However, this possibility should be empirically examined. Our analyses imply that an increase in gene product sometimes has a significant, yet unexpected, effect on the functions of subcellular networks.
UR - http://www.scopus.com/inward/record.url?scp=62649155906&partnerID=8YFLogxK
UR - http://www.scopus.com/inward/citedby.url?scp=62649155906&partnerID=8YFLogxK
U2 - 10.1186/1752-0509-3-23
DO - 10.1186/1752-0509-3-23
M3 - Article
C2 - 19232106
AN - SCOPUS:62649155906
VL - 3
JO - BMC Systems Biology
JF - BMC Systems Biology
SN - 1752-0509
M1 - 23
ER -