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Characterization of the cDNAs Encoding Three GnRH Forms in the Pejerrey Fish Odontesthes bonariensis (Atheriniformes) and the Evolution of GnRH Precursors

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Abstract

Most vertebrates express two gonadotropin releasing hormone (GnRH) variants in brain tissue but there is an increasing number of fish species for which a third GnRH form has been detected. We characterized the precursors (cDNAs) of all three forms expressed in the brain of the pejerrey (silverside) fish, Odontesthes bonariensis (Atheriniformes): type I (GnRH-I; 440 bp), type II (GnRH-II; 529 bp), and type III (GnRH-III; 515 bp). The expression of these GnRHs precursors was also observed in peripheral tissues related to reproduction (gonads), visual and chemical senses (eye and olfactory epithelium), and osmoregulation (gill), suggesting that in teleost fish and possibly other vertebrates GnRH mediates directly or indirectly many other functions besides reproduction. We also present a comprehensive phylogenetic analysis including representatives of all chordate GnRH precursors characterized to date that supports the idea of two main paralogous GnRH lineages with different function. A “forebrain lineage” separates evolutionarily from the “midbrain lineage” as a result of an ancient duplication (ca. 600 million years ago). A third, fish-only clade of GnRH genes seems to have originated before the divergence of fish and tetrapods but retained only in fish. Phylogenetic analyses of GnRH precursors (DNA and protein sequences) under different optimality criteria converge on this result. Although alternative scenarios could not be statistically rejected in this study due to the relatively short size of the analyzed molecules, this hypothesis also receives support from chromosomal studies of synteny around the GnRH genes in vertebrates.

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Acknowledgments

This work was partially supported by grants from Agencia Nacional de Promoción Científica y Tecnológica (ANPCYT; Argentina), PICT 01-12168 to G.M.S., Consejo Nacional de Investigaciones Científicas y Técnicas (CONICET; Argentina), PEI 6439 and PIP 5425 to G.M.S., and Grant DEB-9985045 from the National Science Foundation (USA) to G.O.

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  1. Laboratorio de Ictiofisiología y Acuicultura, Instituto de Investigaciones Biotecnológicas/Instituto Tecnológico de Chascomús (CONICET-UNSAM), C.C. 164 (B7130IWA), Chascomús, Provincia de Buenos Aires, Argentina

    Leonardo G. Guilgur, Pablo H. Strobl-Mazzulla, Juan I. Fernandino, Leandro A. Miranda & Gustavo M. Somoza

  2. School of Biological Sciences, University of Nebraska, Lincoln, NE, 68588, USA

    Guillermo Ortí

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  1. Leonardo G. Guilgur
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  2. Guillermo Ortí
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  3. Pablo H. Strobl-Mazzulla
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  4. Juan I. Fernandino
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  5. Leandro A. Miranda
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  6. Gustavo M. Somoza
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Correspondence to Gustavo M. Somoza.

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Appendix 1

Appendix 1

Nomenclature of the GnRH Variants Used in the Endocrinological Literature and Their Primary References

Usually, the different GnRH variants are known by the name of the species in which they were first isolated, except for the first characterized GnRH from mammalian hypothalamic tissues (pig and sheep), now generally referred to as mammalian GnRH (mGnRH). Eight out of the 14 vertebrate GnRH variants known to date have been characterized and/or detected in teleosts and six are exclusive of this lineage. The latter include: salmon GnRH (sGnRH; Sherwood et al. 1983), catfish GnRH (cfGnRH; Bogerd et al. 1992; Ngamvongchon et al. 1992), seabream GnRH (sbGnRH; Powell et al. 1994), herring GnRH (hrGnRH; Carolsfeld et al. 2000), pejerrey GnRH (pjGnRH; Montaner et al. 2001; also named as mdGnRH; Okubo et al. 2000) and whitefish GnRH (wfGnRH; Adams et al. 2002). Two other forms present in bony fish species also are found in mammals and other tetrapods: mammalian GnRH (mGnRH) and chicken GnRH-II (cGnRH-II). In fishes, mGnRH was first identified in eels (King et al. 1990; Okubo et al. 1999), and the chicken form (cGnRH-II) in the goldfish (Yu et al. 1988), and subsequently in all teleost species examined to date (see Somoza et al. 2002a).

Accession numbers of the GnRH sequences from jawless fishes, ray-finned fishes, and tetrapods downloaded from GenBank.

GnRH I clade: Alosa sapidissima: AF536381; Anguilla japonica: AB026989; Astatotilapia burtoni: U31865; Cavia porcellus: AF033346; Clarias gariepinus: X78049; Coregonus clupeaformis: AY245104; Cynoscion nebulosus: AY796308; Dicentrarchus labrax: AF224279; Gallus gallus: X69491; Homo sapiens: NM_000825; Micropogonias undulatus: AY324668; Monopterus albus: AY858056; Morone saxatilis: AF056314; Mugil cephalus: AY373450; Odontesthes bonariensis: AY744689; Oreochromis niloticus: AB101665; Oryzias latipes: AB041333; Pagrus major: D86582; Rachycentron canadum: AY677175; Rana catesbeiana: AF188754; Rana dybowskii: AF139911; Rattus norvegicus: NM_012767; Sciaenops ocellatus: AY677172; Sparus aurata: U30320; Sus scrofa: L32864; Tupaia belangeri: U63326; Verasper moseri: AB066360; Xenopus laevis: L28040.

GnRH II clade: Anguilla japonica: AB026990; Astatotilapia burtoni: AF076962; Carassius auratus: U30386; Clarias gariepinus: X78047; Coregonus clupeaformis: AY245102; Cynoscion nebulosus: AY796309; Cyprinus carpio: AY147400; Danio rerio: AF511531; Dicentrarchus labrax: AF224281; Eublepharis macularius: AB104485; Homo sapiens: AF036329; Macaca mulatta: AF097356 ; Micropogonias undulatus: AY324669; Monopterus albus: AY786183; Morone saxatilis: AF056313; Mugil cephalus: AY373451; Odontesthes bonariensis: AY744687; Oncorhynchus mykiss: AF125973; Oreochromis niloticus: AB101666; Oryzias latipes: AB041330; Rachycentron canadum: AY677174; Rana catesbeiana: AF186096; Rutilus rutilus: U60668; Sciaenops ocellatus: AY677171; Scleropages jardinii: AB047326; Sparus aurata: U30325; Suncus murinus: AF107315; Trichosurus vulpecula: AF193516; Tupaia belangeri: U63327; Typhlonectes natans: AF167558; Verasper moseri: AB066359.

GnRH III clade: Astatotilapia burtoni: AF076963; Carassius auratus: AB017271; Coregonus clupeaformis: AY245103; Cynoscion nebulosus: AY796310; Cyprinus carpio: AY189960; Danio rerio: NM_182887; Dicentrarchus labrax: AF224280; Micropogonias undulatus: AY324670; Monopterus albus: AY858055; Mugil cephalus: AY373449; Odontesthes bonariensis: AY744688; Oncorhynchus masou: S44614; Oncorhynchus mykiss: AF232212; Oncorhynchus nerka: D31868; Oreochromis niloticus: AB101667; Oryzias latipes: AB041332; Pagrus major: D26108; Porichthys notatus: U41669; Rachycentron canadum: AY677173; Rutilus rutilus: U60667; Salmo salar: X79709; Salmo trutta: X79713; Salvelinus fontinalis: X79712; Sciaenops ocellatus: AY677170; Scleropages jardinii: AB047325; Sparus aurata: U30311; Verasper moseri: AB066358.

GnRH Jawless fish: Geotria australis: AY307172; Ichthyomyzon fossor: AY307174; Ichthyomyzon unicuspis: AY307175; Lampetra appendix: AY307176; Lampetra richardsoni: AY307177; Lampetra tridentatus: AY307178; Mordacia mordax: AY307173; Petromyzon marinus I: AF144479; Petromyzon marinus III: AY052628.

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Guilgur, L.G., Ortí, G., Strobl-Mazzulla, P.H. et al. Characterization of the cDNAs Encoding Three GnRH Forms in the Pejerrey Fish Odontesthes bonariensis (Atheriniformes) and the Evolution of GnRH Precursors. J Mol Evol 64, 614–627 (2007). https://doi.org/10.1007/s00239-006-0125-8

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