Evolution of Receptors for Growth Hormone and Somatolactin in Fish and Land Vertebrates: Lessons from the Lungfish and Sturgeon Orthologues
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Two cognate hormones, growth hormone (GH) and somatolactin (SL), control several important physiological processes in vertebrates. Knowledge about GH and its receptor (GHR) has accumulated over the last decades. However, much less is known about SL and its receptor (SLR). SL is found only in fish (including lungfish), suggesting that it was present in the common ancestor of vertebrates, but was lost secondarily in the lineage leading to land vertebrates after the lungfish branched off. SLR was suggested to be a duplicated copy of GHR acquired only in teleosts via the fish-specific genome duplication (FSGD). This scenario (i.e., the existence of SL but not SLR in the vertebrate ancestors) is intriguing but contested. In this study, we first evaluated the plausibility of this scenario through synteny analyses and found that the loci for GHR and SLR are located in syntenic genomic positions, whereas the loci for GH and SL are not. Next, we cloned GHRs of lungfish and sturgeon, which possess SL but did not undergo the FSGD (i.e., they should not possess SLR). Their phylogenetic positions in the GHR/SLR gene tree further support the fish-specific scenario for the GHR–SLR duplication. Interestingly, their sequences share greater similarity with teleost SLRs and reptilian/amphibian GHRs than with the GHRs of mammals, birds, and teleosts. On the basis of these results, we discuss the validity of the nomenclature of the teleost-specific copy of GHR as SLR and an ancestral receptor(s) for SL before the evolution of SLR during the FSGD.
KeywordsSomatolactin receptor (SLR) Growth hormone receptor (GHR) Lungfish Sturgeon Fish-specific genome duplication (FSGD) Synteny Sub-functionalization
The authors would like to thank S. Hoegg of the University of Konstanz and J. G. Inoue of Florida State University for the lungfish and sturgeon samples, and for advice on the phylogenetic reconstruction; Y. Minegishi and J. Aoyama of the University of Tokyo for the eel genomic DNA; Y. Ozaki of National Institute of Genetics and H. Fukada of Kochi University for detailed information about the eel GHR; and D. Gerrard for the idea of the relative-rate test and comments on the manuscript. The authors would also like to thank H. Mitani of the University of Tokyo and T. Yada of the National Research Institute of Fisheries Science for comments on the manuscript. This research was supported by a long-term fellowship (#LT00059/2005-L) from the International Human Frontier Science Program Organization to S.F., and grants from the Deutsche Forschungsgemeinschaft and the University of Konstanz to A.M.
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