Abstract
The growth hormone (GH) gene isolated and cloned from various Labeo species (L. rohita, L. calbasu, L. fimbriatus, L. gonius, L. bata, and L. kontius) is shown to contain a single copy in the haploid genome, with an overall size of ∼2.5 kb. The GH gene in all the Labeo species studied has five exons and four introns of various sizes with the exon/intron boundary sequence of GT/AG. The length variation of the GH gene between the species is found to be due to length variation in the form of several deletions in the third intron. The length of individual exons is the same in all the species with an open reading frame (ORF) of 630 bp (210 amino acids) except in L. rohita, which has a 9 bp deletion in the fourth exon, resulting in a shorter GH of 621 bp (207 amino acids). The similarity in the nucleotide and amino acid sequences between the different Labeo species is greater than 97%, in spite of eight amino acids being altered in the GH protein of Labeo that reside outside the conserved domain sequence required for its function. Nucleotide substitutions are seen in the form of 20 transitions and three transversions in the ORF of the GH gene. Both types of transitions (A–G; T–C) and only one type of transversion (A–C) are detected in the GH gene. Codon preference in GH gene shows a strong preference for G and C in the wobble position of the codons. Genetic interrelationships determined between Labeo and other species of fishes using nucleotide sequence of GH cDNA supports the overall teleost classification of Nelson (Fishes of the World. Wiley, New York, 1984) with separate clades for Ostariophysi, Protacanthopterygii, and Acanthopterygii. Besides, the unweighted pair group method with arithmetic means (UPGMA) analysis clearly distinguishes between the species having five exons and four introns in the GH gene from the species having six exons and five introns in the same gene. The Labeo species analyzed in the present study could be clustered into two groups using the maximum-parsimony method on the intron sequences data of the GH gene.
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Abbreviations
- BLAST:
-
Basic local alignment search tool
- cDNA:
-
Complementary deoxyribonucleic acid
- GH:
-
Growth hormone
- LR:
-
Labeo rohita
- LC:
-
Labeo calbasu
- LF:
-
Labeo fimbriatus
- LG:
-
Labeo gonius
- LK:
-
Labeo kontius
- LB:
-
Labeo bata
- ORF:
-
Open reading frame
- Pit 1:
-
Pituitary transcription factor 1
- UPGMA:
-
Unweighted pair group method with arithmetic means
References
Agellon LB, Chen TT, (1986) Rainbow trout growth hormone: molecular cloning of cDNA and expression in Escherichia coli. DNA 5:463–471
Agellon LB, Emery CJ, Jones JM, Davies SL, Dingle AD, Chen TT (1988a) Promotion of rapid growth of rainbow trout (Salmo gairdneri) by a recombinant fish growth hormone. Can J Fish Aquat Sci 45:146–151
Agellon LB, Davies SL, Chen TT, Powers DA (1988b) Structure of fish (rainbow trout) growth hormone gene and its evolutionary implications. Proc Natl Acad Sci USA 85:5136–5140
Almuly R, Cavari B, Ferstman H, Koloduy O, Funkenstein B (2000) Genomic structure and sequence of the gilthead seabream (Sparus aurata) growth hormone encoding gene: identification of minisatellite polymorphism in intron I. Genome 43:836–845
Almuly R, Poleg-Danin Y, Gorshkov G, Rapport B, Soller M, Kashi Y, Funkenstein B (2005) Characterization of the 5′ flanking region of the growth hormone gene of the marine teleost, gilthead seabream, Sparus aurata: analysis of a polymorphic microsatellite in the proximal promoter. Fisheries Sci 71:479–490
Anathy V, Venugopal T, Koteeswaran R, Pandian TJ, Mathavan S (2001) Cloning, sequencing and expression of cDNA encoding growth hormone from Indian catfish (Heteropneustes fossilis). J Biosci 26:315–324
Barta A, Richards RI, Baxter JD, Shine J (1991) Primary structure and evaluation of rat growth hormone gene. Proc Natl Acad Sci 78:4867–4871
Ber R, Daniel V (1993) Sequence analysis suggests a recent duplication of growth hormone encoding gene in Tilapia nilotica. Gene 125:143–150
Bernardi G, D’Onofrio G, Caccio S (1993) Molecular phylogeny of bony fishes, based on the amino acid sequence of the growth hormone. J Mol Evol 37:644–649
Bernardini S, Argenton F, Vianello S, Colombo L, Bortolussi M (1999) Regulatory regions in the promoter and third intron of the growth hormone gene in rainbow trout, Oncorhynchus mykiss Walbaum. Gen Comp Endocrinol 116:261–271
Biju SD, Bossuyt F (2003) New frog family from India reveals an ancient biogeographical link with Scychelles. Nature 425:711–714
Bolton JP, Collie NL, Kawauchi H, Hirano T (1987) Osmoregulatory actions of growth hormone in rainbow trout (Salmo gairdneri). J Endocrinol 112:63– 68
Buggioti L, Primmier CR (2006) Molecular evolution of the avian growth hormone gene and comparison with its mammalian counterpart. J Evol Biol 19:844–854
Calduch-Giner JA, Sitja-Bobadilla A, Alvarez-Pellitero P, Perez-Sanchez J (1997) Growth hormone as an in vitro phagocyte-activating factor in the gilthead seabream (Sparus aurata). Cell Tiss Res 287:535–540
Cavari B, Funkenstein B, Chen TT, Gonsalez-Villasenor LI, Schartl M (1993) Effect of growth hormone on the growth rate of the gilthead seabream (Sparus aurata), and use of different construct for the production of transgenic fish. Aquaculture 111:189–197
Chang YS, Liu CS, Huang FL, Lo TB (1992) The primary structures of growth hormones of three cyprinid species: bighead carp, silver carp and grass carp. Gen Comp Endocrinol 87:385–393
Chao S, Pan F, Chang W (1989) Purification of carp growth hormone and cloning of the complementary DNA. Biochim Biophys Acta 1007:233–236
Chiou CS, Chen HT, Chang W-C (1990) The complete nucleotide sequence of the growth hormone gene from common carp (Cyprinus carpio). Biochim Biophys Acta 1087:91–94
Crick F H C (1966) Codon-anticodon pairing: the wobble hypothesis. J Mol Biol 19:548–555
De Noto FM, Moore DD, Goodman HM (1981) Human growth DNA sequence and mRNA structure: possible alternative splicing. Nucl Acids Res 9:3719–3730
Devlin RH (1993) Sequence of sockeye salmon type 1 and 2 growth hormone genes and the relationship of rainbow trout with Atlantic and Pacific salmon. Can J Fish Aquat Sci 50:1738–1748
Dutta SK, Vasudevan K, Chaitra MS, Shanker K, Aggarwal RK (2004) Jurassic frogs and the evolution of amphibian endemism in the Western Ghats. Curr Sci 86:211–216
Feinberg AP, Vogelstein B (1983) A technique for radiolabeling DNA restriction endonuclease fragments to high specific activity. Anal Biochem 132:6–13
Felsenstein J (1989) PHYLIP-phylogeny inference package. Cladistics 5:164–166
Fine M, Sakal E, Vashdi D, Daniel V, Lavanon A, Lipshitz O, Gertler A (1993) Recombinant carp growth hormone (Cyprinus carpio): expression, purification and determination of biological activity in vitro and in vivo. Gen Comp Endocrinol 89:51–61
FitzGerald LM, Rodriguez A, Smutzs G (1993) Codon usage in bony fishes. Mol Mar Biol Biotechnol 2:112–119
Forbes SH, Knudsen KL, North TW, Allendorf FW (1994) One of the two growth hormone genes in coho salmon are sex linked. Proc Natl Acad Sci USA 91:1628–1631
Forsyth I-A, Wallis M (2002) Growth hormone and prolactin-molecular and functional evolution. J Mammary Gland Biol Neopla 7:291–312
Grantham R (1978) Viral, prokaryote and eukaryote genes contrasted by mRNA sequence indexes. FEBS Lett 95:1–11
Grantham R, Gautier C, Guoy M, Mercier R, Pave A (1980) Codon catalog usage and genome hypothesis. Nucl Acids Res 8:r49–r62
Gross R, Nilsson J (1999) Restriction fragment length polymorphism at the growth hormone 1 gene in Atlantic salmon (Salmo salar L.) and its association with weight among the offspring of a hatchery stock. Aquaculture 173:73–80
Ho WK, Tsang WH, Dias NP (1989) Cloning of the grass carp growth hormone cDNA. Biochem Biophys Res Commun 161:1239–1243
Ho WK, Wong MW, Chan AP (1991) Cloning and sequencing of the grass carp (Ctenopharyngodon idellus) growth hormone gene. Biochim Biophys Acta 1090:245–248
Hoj S, Fredholm M, Larsen NJ, Nielsen VH (1993) Growth hormone gene polymorphism associated with selection for milk fat production in lines of cattle. Anim Genet 24:9–96
Hong Y, Schartl M (1993) Sequence of growth hormone (GH) from silver carp (Hypophthalmicthys molitrix) and evolution of GH genes in vertebrates. Biochim Biophys Acta 1174:285–288
Huising MO, Kruiswijk CP (2004a) Cloning and characterization of the common carp (Cyprinus carpio) growth hormone 1 (GH1) gene. NCBI Genbank Accession AJ640135
Huising MO, Kruiswijk CP (2004b) Cloning and characterization of the common carp (Cyprinus carpio) growth hormone 2 (GH2) gene. NCBI Genbank Accession AJ640136
Jayaram KC, Dhas JJ (2000) Revision of the genus Labeo Cuvier from the Indian region with a discussion on its phylogeny and Zoogeography. (Pisces: Cypriniformes: Cyprinidae, Cyprininae) Occ Paper No 183: Rec Zool Surv India
Jhingran VG (1975) Fish and fisheries of India. Hindustan, Delhi, India
Johnson AM (1990) Comparison of dinucleotide frequency and codon usage in Toxoplasma and Plasmodium: evolutionary implications. J Mol Evol 30:383–387
Kaplan SL (1999) Hormonal regulation of growth and metabolic effects of growth hormone. In: Kostyo JL, Goodman HM (Eds) Handbook of Physiology. The endocrine system, Vol V: Hormonal control of growth. Oxford University Press, New York, pp 129–143
Knorr C, Moser G, Muller E, Geldermann H (1997) Association of GH gene variants with performance traits in F2 generations of European wild boar, Pietrain and Meishan pigs. Anim Genet 28:124–128
Koren Y, Sarid S, Ber R, Daniel V (1989) Carp growth hormone: molecular cloning and sequencing of cDNA. Gene 77:309–315
Kuhnlein U, Ni L, Weigend S, Gavora J S, Fairfull W, Zandworny D (1997) DNA polymorphisms in the chicken growth hormone gene: Response to selection for disease resistance and association with egg production. Anim Genet 28:116–123
Kyte J, Doolittle R (1982) A simple method for displaying the hydropathic character of a protein. J Mol Biol 157:105–132
Lagziel A, Lipkin E, Soller M (1996) Association between SSCP haplotypes at the bovine growth hormone and milk protein percentage. Genetics 142:945–951
Law MS, Cheng KW, Fung TK, Chan YH, Yu KL, Chan KM (1996) Isolation and characterization of two distinct growth hormone cDNAs from the goldfish, Carassius auratus. Arch Biochim Biophys 330:19–23
Li X, Wang Y and Zhu Z (2002) Megalobrama amblycephala growth hormone (GH) mRNA, complete cds. Genbank Accession AY170124
Lira S A, Crenshaw E B, Glass C K, Swanson L W, Rosenfeld M G (1988) Identification of rat growth hormone genomic sequences targeting pituitary expression in transgenic mice. Proc Natl Acad Sci USA 85:4755–4759
Lucy MC, Hauser SD, Eppard PJ, Krivi GG, Clark JH, Bauman DE, Collier RJ (1993) Variants of somatotropin in cattle: gene frequencies in major dairy breeds and associated milk production. Domest Anim Endocrinol 10:325–333
Majumdar KC, Ray-Chaudhuri SP (1988) On the morphometrics of hybrids of Indian major carps. Proc Zool Soc (Calcutta) 37:63–69
Majumdar K C, Ravinder K, Nasaruddin K (1997) DNA fingerprinting in Indian major carps and tilapia by Bkm 2 (8) and M 13 probes. Aquacul Res 28:129–138
Marins LF, Levy JA, Folch JM, Sanchez A (2003) A growth hormone-based phylogenetic analysis of euteleostean fishes including a representative species of the Atheriformes order, Odontesthes argentinensis. Gen Mol Biol 26:295–300
McKay SJ, Devlin RH, Smith MJ (1996) Phylogeny of Pacific salmon and trout based on growth hormone type-2 (GH2) and mitochondrial NADH dehydrogenase subunit 3 (ND3) DNA sequences. Can J Fish Aquat Sci 53:1165–1174
McLean E, Donaldson EM (1993) The growth of poikilotherms. In: Schreibman MP, Scanes CG, Pang PKT (eds) The endocrinology of growth, development and metabolism in vertebrates. Academic, New York, pp 43–71
McLean E, Donaldson EM, Dye HM, Souza LM (1990) Growth acceleration of the coho salmon Oncorhynchus kisutch following oral administration of recombinant bovine somatotropin. Aquaculture 91:197–203
McLean E, Donaldson E M, Teskeridzic E, Souza L M (1993) Growth enhancement following dietary delivery of recombinant porcine somatotropin to diploid and tetraploid coho salmon (Oncorhynchus kisutch). Fish Physiol Biochem 11:363–369
Meiri I, Knibb WR, Zohar Y, Elizur A (2004) Temporal profile of beta follicle-stimulating hormone, beta luteinizing hormone, and growth hormone gene expression in the protandrous hermaphrodite, gilthead seabream, Sparus aurata. Gen Comp Endocrinol 137:288–299
Natarajan AV, Desai VR, Mishra DN (1976) On the natural occurrence of the intergeneric catla-rohu hybrid in Rihand (Uttar Pradesh) with an account of its potential role in reservoir fisheries development in India. J Inland Fish Soc India 8:83–90
Nelson JS (1984) Fishes of the world. Wiley, New York
Nicoll CS, Rodgers BD, Kelly KM (1999) Hormonal regulation of growth and development of nonmammalian vertebrates. In: Kotsyo JL, Goodman HM (Eds) Handbook of physiology. The endocrine system, Vol V, Hormonal control of growth. Oxford University Press, NY, pp 73–98
Nielsen VH, Larsen NJ, Agergaard N (1995) Association of DNA polymorphism in the growth hormone gene with basal-plasma growth hormone concentration and production traits in pigs. J Anim Breed Genet 112:205–212
Noh JK, Cho KN, Nam YK, Kim DS, Kim CG (1999) Genomic organization and sequence of the mud loach (Misgurnus mizolepis) growth hormone gene: a comparative analysis of teleost growth hormone genes. Mol Cells 9:638–645
Oakley TH, Phillips RB (1999) Phylogeny of Salmonine fshes based on growth hormone introns: Atlantic (Salmo) and Pacifc (Oncorhynchus) salmon are not sister taxa. Mol Phylogenet Evol 11:381–393
Ohkubo T, Araki M, Tanaka M, Sudo S, Nakashima K (1996) Molecular cloning and characterization of the yellowtail GH gene and its promoter: a consensus sequence for teleost and avian Pit-1/GHF-1 binding sites. J Mol Endocrinol 16:63–72
Ohno S (1970) Evolution by gene duplication. Springer Verlag, New York
Ohno S, Wolf U, Atkin NB (1968) Evolution from fish to mammals by gene duplication. Hereditas 59:169–187
Park LK, Moran P, Dightman DA (1995) A polymorphism in intron D of the Chinook salmon growth hormone 2 gene. Anim Genet 26:285
Phillips RB, Matsuoka MP, Konkol NR, McKay S (2004) Molecular systematics and evolution of growth hormone introns in the Salmonidae. Env Biol Fish 69:433–440
Proudfoot NJ, Brownlee GG (1976) 3′ Non-coding region sequences in eukaryotic messenger RNA. Nature 263:211–214
Reddy PVGK (1997) Genetic resources of Indian major carps. FAO fisheries technical paper 387
Rentier-Delrue F, Swennen D, Mercier L, Lion M, Benrubi O, Martial J A (1989) Molecular cloning and characterization of two forms of trout growth hormone cDNA: expression and secretion of tGH-II by Escherichia coli. DNA 8:109–117
Rubin D A, Dores RM (1994) Cloning of a growth hormone from a primitive bony fish and its phylogenetic relationships. Gen Comp Endocrinol 95:71–83
Rubin DA, Dores RM (1995) Obtaining a more resolute teleost growth hormone phylogeny by the introduction of gaps in sequence alignment. Mol Phylogenet Evol 4:129–138
Sakata S, Noso T, Moriyama S, Hirano T, Kawauchi H (1993) Flounder growth hormone: isolation, characterization, and effects on growth of juvenile rainbow trout. Gen Comp Endocrinol 89:396–404
Sambrook J, Fritsch EF, Maniatis T (1989) Molecular cloning—a laboratory manual, 2nd edn. Cold Spring Harbor Laboratory, Cold Spring Harbor, New York
Scully KM, Jacobson EM, Jepsen K, Lunyak V, Viadiu H, Carriere C, Rose DW, Hooshmand F, Aggarwal AK, Rosenfeld MG (2000) Allosteric effects of Pit 1 DNA sites on long-term repression in cell type specification. Science 290:1127–1131
Sekkali B, Brim H, Muller M, Argenton F, Bortolussi M, Colombo L, Belayew A, Martial JA (1999) Structure and functional analysis of a Tilapia (Oreochromis mossambicus) growth hormone gene: activation and repression by pituitary transcription factor Pit 1. DNA Cell Biol 18:489–502
Spruell P, Pilgrim KL, Greene BA, Habicht C, Knudsen KL, Lindner KR, Olsen JB, Sage GK, Seeb JE, Allendorf FW (1999) Inheritance of nuclear DNA markers in gynogenetic haploid pink salmon. J Heredit 90:289–296
Tang Y, Lin CM, Chen TT, Kawauchi H, Dunham RA, Powers DA (1993) Structure of channel cat fish (Ictalurus punctatus) growth hormone gene and its evolutionary implications. Mol Mar Biol Biotechnol 2:198–206
Thompson JD, Higgins DG, Gibson TJ (1994) CLUSTAL W: improving sensitivity of progressive multiple sequence alignment through sequence weighting, positions-specific gap penalties and weight matrix choice. Nucl Acids Res 22:4673–4680
Tsai HJ, Kuo JC, Lou SW, Kuo TT (1994) Growth enhancement of juvenile striped mullet by feeding recombinant yeast containing fish growth hormone. Prog Fish Cult 56:7–12
Van Der Kraak G, Rosenblum PM, Peter RE (1990) Growth hormone dependent potentiation of gonadotropin stimulated steroid production by ovarian follicles of the goldfish. Gen Comp Endocrinol 79:233–239
Vences M, Freyhof J, Sounenberg R, Kosuch J, Veith M (2001) Reconciling fossils and molecules: Coenozoic divergence of chichlid fishes and the biogeography of Madagascar. J Biogeogr 28:1091–1099
Venkatesh B, Brenner S (1997) Genomic structure and sequence of the pufferfish (Fugu rubripes) growth hormone-encoding gene: a comparative analysis of teleost growth hormone genes. Gene 187:211–215
Venugopal T, Anathy V, Pandian TJ, Gong GZ, Mathavan S (2002a) Molecular cloning of growth hormone-encoding cDNA of an Indian major carp, Labeo rohita, and its expression in Escherichia coli and Zebrafish. Gen Comp Endocrinol 125:236–247
Venugopal T, Mathavan S, Pandian TJ (2002b) Molecular cloning of growth hormone encoding cDNA of Indian major carps by a modified rapid amplification of cDNA ends strategy. J Biosci 27:261–272
Vestling M, Murphy C, Fenselau C, Chen T T (1991) Disulfide bonds in native and recombinant fish growth hormones. Mol Mar Biol Biotechnol 1:73–77
Wallis M (1996) The molecular evolution of vertebrate growth hormones: a pattern of near-stasis interrupted by sustained bursts of rapid change. J Mol Evol 43:93–100
Watahiki M, Yamamoto M, Yamakawa M, Tanala M, Nakashima K (1989) Conserved and unique amino acid residues in the domains of the growth hormones. J Biol Chem 264:312–316
Westerich KM, Konkol NR, Matsuoka MP, Phillips RB (2002) Interspecific relationships among charrs based on phylogenetic analysis of nuclear growth hormone intron sequences. Env Biol Fish 64:217–222
Woychik RP, Camper SA, Lyons RH, Horowitz S, Goodwin EC, Rottman FM (1982) Cloning and nucleotide sequencing of the bovine growth hormone gene. Nucl Acids Res 10:7197–7210
Yowe DL, Epping RJ (1995) Cloning of the barramundi growth hormone-encoding gene: a comparative analysis of higher and lower vertebrate GH genes. Gene 162:255–259
Acknowledgements
We are grateful to Dr. L. Singh, Director CCMB for support and encouragement, Dr. K. Uma Devi for correcting the manuscript and Mr. Ranga Rao for typing the manuscript. We thank Mr. R. Purushotham (Department of Fisheries, Andhra Pradesh) and Mr. K. Ravinder for collection of fish samples, Dr. J.C. Dhas (Fisheries Survey of India, Vishakhapatnam) and Dr. R.P. Burman (Zoological Survey of India, Kolkata) for identification of species. Financial assistance from the Department of Biotechnology, Government of India through grant no. BT/AA/03/70(A)/94 to KCM is gratefully acknowledged.
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Rajesh, R., Majumdar, K.C. A comparative account of the structure of the growth hormone encoding gene and genetic interrelationship in six species of the genus Labeo . Fish Physiol Biochem 33, 311–333 (2007). https://doi.org/10.1007/s10695-007-9164-3
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DOI: https://doi.org/10.1007/s10695-007-9164-3
Keywords
- Codon preference
- DNA phylogeny
- Growth hormone gene
- Intron sequences
- Labeo