Evolution of Receptors for Growth Hormone and Somatolactin in Fish and Land Vertebrates: Lessons from the Lungfish and Sturgeon Orthologues

Abstract

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.

Regulation of endocrine and paracrine sources of Igfs and Gh receptor during compensatory growth in hybrid striped bass (Morone chrysops×Morone saxatilis)

“…Recent phylogentic and evolutionary analysis suggests that the SLR may in fact be a duplicated Ghr that occurred during the fish-specific genome duplication (Fukamachi & Meyer 2007). The striped bass ghr1 amplicon showed 70 and 72% nucleotide identity with medaka (Oryzias latipes; DQ002886; Fukamachi et al 2005), and masu salmon (Oncorhynchus masou; AB121047; Fukada et al 2005) slr respectively, while our striped bass ghr2 amplicon only showed 50 and 53% nucleotide identity to these same slr sequences.…”

Fitness difference between cryptic salinity-related phenotypes of sea bass (<em>Dicentrarchus labrax</em>)

“…Two transcripts (Genbank accessions: AF438177 and AY642116) were available in databases as GHR1 and GHR2, respectively. Fukamachi and Meyer (2007) demonstrated that sequences available in databases and reported as GHR (1 or 2) could be somatolactin receptors (SLR). We performed alignments of sequences, and unambiguously linked the sea bass GHR sequence to the transcript with accession AY642116 (GHR2, the alternate transcript being SLR; details not shown).…”

A study of somatolactin actions by ectopic expression in transgenic zebrafish larvae

“…According to sequence comparisons, it is generally believed that SL and PRL evolved from a common ancestral gene related to GH with two successive rounds of gene duplication before the divergence between vertebrates and invertebrates (Chen et al 1994, Fukamachi & Meyer 2007. However, the SL gene is not found in tetrapods and might have been lost during the evolution of early land vertebrates (Fukamachi & Meyer 2007).…”

“…According to sequence comparisons, it is generally believed that SL and PRL evolved from a common ancestral gene related to GH with two successive rounds of gene duplication before the divergence between vertebrates and invertebrates (Chen et al 1994, Fukamachi & Meyer 2007. However, the SL gene is not found in tetrapods and might have been lost during the evolution of early land vertebrates (Fukamachi & Meyer 2007). Fish SL is mainly expressed in the pars intermedia of the pituitary gland and distinct from proopiomelanocortin (POMC)-producing cells (Kaneko 1996); hence, it should have physiological actions different from those of GH and PRL.…”

“…Fish SL is mainly expressed in the pars intermedia of the pituitary gland and distinct from proopiomelanocortin (POMC)-producing cells (Kaneko 1996); hence, it should have physiological actions different from those of GH and PRL. In addition, despite the conserved helical bundles, the number of disulfide bonds (6 or 7) is different from that found in GH and PRL (4), and the low sequence identity found between SL and GH (50-60%) also suggests that they have dissimilar functions in fish (Chen et al 1994, Fukamachi & Meyer 2007.…”