Abstract
The threespot wrasse (Halichoeres trimaculatus; Family Labridae) is a common coral reef species of the Indo-Pacific Ocean. Given that this species spawns daily at high tide (HT), we hypothesized that endocrine changes in relation to gonadal development are synchronized with the tidal cycle. To test this, we examined the transcript abundance of two cytochrome P450 aromatases (cyp19a and cyp19b) and two estrogen receptors (erα and erβ) in the ovary and brain of this species in response to tidal change. When fish were collected around four tidal points [low tide (LT), flood tide (FT), high tide (HT), and ebb tide (ET)], gonadosomatic index and oocyte diameter increased around HT and FT, respectively. Ovulatory follicles were observed in ovaries around HT. Real-time quantitative polymerase-chain reaction revealed that mRNA abundance of cyp19a and erα, but not erβ, in the ovary increased around ET and HT, respectively. On the other hand, mRNA levels of cyp19b in the forebrain were significantly higher around FT. Increases of erα and erβ mRNA abundance around FT were observed in all areas of the brain and the midbrain, respectively. The changes in mRNA abundance of key genes involved in reproduction at specific tidal cycles, along with the development of the vitellogenic oocytes in the ovary, support our hypothesis that synchronization of endocrine changes to the tidal periodicity plays a role in the gonadal development of this species. We hypothesize that conversion of testosterone to E2 in the brain may be associated with the spawning behavior given that the wrasse exhibits group spawning with a territory-holding male around HT.
Similar content being viewed by others
References
Afonso LOB, Iwama GK, Smith J, Donaldson EM (1999) Effects of the aromatase inhibitor Fadrozole on plasma sex steroid secretion and oocytematuration in female coho salmon (Oncorhynchus kisutch) during vitellogenesis. Fish Physiol Biochem 20:231–241
Asahina K, Kambegawa A, Higashi T (1995) Development of a microtiter plate enzyme-linked immunosorbent assay for 17α,20β,21-trihydroxy-4-pregnen-3-one, a teleost gonadal steroid. Fish Sci 61:491–494
Blázquez M, Piferrer F (2004) Cloning, sequence analysis, tissue distribution, and sex-specific expression of the neural form of P450 aromatase in juvenile sea bass (Dicentrarchus labrax). Mol Cell Endocrinol 219:83–94
Chang XT, Kobayashi T, Kajiura H, Nakamura M, Nagahama Y (1997) Isolation and characterization of the cDNA encoding the tilapia (Oreochromis niloticus) cytochrome P450 aromatase (P450arom): changes in P450arom mRNA, protein, and enzyme activity in ovarian follicles during oogenesis. J Mol Endocrinol 18:57–66
Chang X, Kobayashi T, Senthilkumaran B, Kobayashi-Kajura H, Sudhakumari CC, Nagahama Y (2005) Two types of aromatase with different encoding genes, tissue distribution and developmental expression in Nile tilapia (Oreochromis niloticus). Gen Comp Endocr 141:101–115
Chaube R, Rawat A, Joy KP (2015) Molecular cloning and characterization of brain and ovarian cytochrome P450 aromatase genes in the catfish Heteropneustes fossilis: sex, tissue and seasonal variation in, and effects of gonadotropin on gene expression. Gen Comp Endocr 221:120–133
Chen H, Zhang Y, Li S, Lin M, Shi Y, Sang Q, Liu M, Zhang H, Lu D, Meng Z, Liu X, Lin H (2011) Molecular cloning, characterization and expression profiles of three estrogen receptors in protogynous hermaphroditic orange-spotted grouper (Epinephelus coioides). Gen Comp Endocr 172:371–381
Choi CY, Habibi HR (2003) Molecular cloning of estrogen receptor alpha and expression pattern of estrogen receptor subtypes in male and female goldfish. Mol Cell Endocr 204:169–177
Colin PL, Bell LJ (1991) Aspects of the spawning of labrid and scarid fishes (Pisces: Labroidei) at Enewetak Atoll, Marshall Islands with notes on other families. Environ Biol Fish 31:229–260
Filby AL, Thorpe KL, Tyler CR (2006) Multiple molecular effect pathways of an environmental oestrogen in fish. J Mol Endocrinol 37:121–134
Halm S, Martínez-Rodrígueza G, Rodrígueza L, Prat F, Mylonas CC, Carrillo M, Zanuy S (2004) Cloning, characterisation, and expression of three oestrogen receptors (ERα, ERβ1 and ERβ2) in the European sea bass, Dicentrarchus labrax. Mol Cell Endocrinol 223:63–75
Hawkins MB, Thornton JW, Crews D, Skipper JK, Dotte A, Thomas P (2000) Identification of a third distinct estrogen receptor and reclassification of estrogen receptors in teleosts. P Natl Acad Sci USA 97:10751–10756
Hojo Y, Hattori TA, Enami T, Furukawa A, Suzuki K, Ishii HT, Mukai H, Morrison JH, Janssen WG, Kominami S, Harada N, Kimoto T, Kawato S (2003) Adult male rat hippocampus synthesizes estradiol from pregnenolone by cytochromes P45017? and P450 aromatase localized in neurons. P Natl Acad Sci USA 101:865–870
Hoffman KS, Grau EG (1989) Daytime changes in oocyte development with relation to the tide for the Hawaiian saddleback wrasse, Thalassoma duperrey. J Fish Biol 34:529–546
Holloway CC, Clayton DF (2001) Estrogen synthesis in the male brain triggers development of the avian song control pathway in vitro. Nat Neurosci 4:170–175
Hoque MM, Takemura A, Takano K (1998) Annual changes in oocyte development and serum vitellogenin level in the rabbitfish, Siganus canaliculatus (Park), in Okinawa, southern Japan. Fish Sci 64:44–52
Huffman LS, O’Connell LA, Hofmann HA (2013) Aromatase regulates aggression in the African cichlid fish Astatotilapia burtoni. Physiol Behav 112–113:77–83
Kazeto Y, Trant JM (2005) Molecular biology of channel catfish brain cytochrome P450 aromatase (CYP19A2): cloning, preovulatory induction of gene expression, hormonal gene regulation and analysis of promoter region. J Mol Endocrinol 35:571–583
Li GL, Liu XC, Lin HR (2007) Seasonal changes of serum sex steroids concentration and aromatase activity of gonad and brain in red-spotted grouper (Epinephelus akaara). Anim Reprod Sci 99:156–166
Ma CH, Dong KW, Yu KL (2000) CDNA cloning and expression of a novel estrogen receptor beta-subtype in goldfish (Carassius auratus). Biochim Biophys Acta 1490:145–152
McEwen BS (1981) Neural gonadal steroid actions. Science 211:1303–1311
Matsuyama M, Adachi S, Nagahama Y, Maruyama K, Matsura S (1990) Diurnal rhythm of serum steroid hormone levels in the Japanese whiting, Sillago japonica, a daily-spawning teleost. Fish Physiol Biochem 8:329–338
Matsuyama M, Morita S, Nasu T, Kashiwagi M (1998) Daily spawning and development of sensitivity to gonadotropin and maturation-inducing steroid in the oocytes of the bambooleaf wrasse, Pseudolabrus japonicas. Environ Biol Fish 52:281–290
Matsuyama M, Onozato S, Kashiwagi M (2002) Endocrine control of diurnal oocyte maturation in the kyusen wrasse, Halichoeres poecilopterus. Zool Sci 19:1045–1053
Menuet A, Pellegrini E, Anglade I, Blaise O, Laudet V, Kah O, Pakdel F (2002) Molecular characterization of three estrogen receptor forms in zebrafish: binding characteristics, transactivation properties, and tissue distributions. Biol Reprod 66:1881–1892
Mu WJ, Wen HS, Shi D, Yang YP (2013) Molecular cloning and expression analysis of estrogen receptor betas (ERβ1 and ERβ2) during gonad development in the Korean rockfish, Sebastes schlegeli. Gene 523:39–49
Nagahama Y (1994) Endocrine regulation of gametogenesis in fish. Int J Dev Biol 38:217–229
Nagler JJ, Cavileer T, Sullivan J, Cyr DG, Rexroad III C (2007) The complete nuclear estrogen receptor family in the rainbow trout: discovery of the novel ERα2 and both ERβ isoforms. Gene 392:164–173
Nagler JJ, Cavileer TD, Verducci JS, Schultz IR, Hook SE, Hayton WL (2012) Estrogen receptor mRNA expression patterns in the liver and ovary of female rainbow trout over a complete reproductive cycle. Gen Comp Endocr 178:556–561
Nelson ER, Habibi HR (2013) Estrogen receptor function and regulation in fish and other vertebrates. Gen Comp Endocr 192:15–24
Nelson ER, Wiehler WB, Cole WC, Habibi HR (2007) Homologous regulation of estrogen receptor subtypes in goldfish (Carassius auratus). Mol Reprod Dev 74:1105–1112
O’Connell LA, Hofmann HA (2012) Social status predicts how sex steroid receptors regulate complex behavior across levels of biological organization. Endocrinology 153:1341–1351
Rasheeda MK, Sridevi P, Senthilkumaran B (2010) Cytochrome P450 aromatases: impact on gonadal development, recrudescence and effect of hCG in the catfish, Clarias gariepinus. Gen Comp Endocr 167:234–245
Ross RM (1983) Annual, semilunar, and diel reproductive rhythms in the Hawaiian labrid Thalassoma duperrey. Mar Biol 72:311–318
Sabo-Attwood T, Kroll KJ, Denslow ND (2004) Differential expression of largemouth bass (Micropterus salmoides) estrogen receptor isotypes alpha, beta, and gamma by estradiol. Mol Cell Endocrinol 218:107–118
Suzuki S, Kuwamura T, Nakashima Y, Karino K, Kohda M (2010) Social factors of group spawning as an alternative mating tactic in the territorial males of the threespot wrasse Halichoeres trimaculatus. Environ Biol Fish 89:71–77
Takemura A, Oya R, Shibata Y, Enomoto Y, Uchimura M, Nakamura S (2008) Role of the tidal cycle in the gonadal development and spawning of the tropical wrasse Halichoeres trimaculatus. Zool Sci 25:572–579
Takemura A, Shibata Y, Takeuchi Y, Hur SP, Sugama N, Badruzzaman M (2012) Effects of hydrostatic pressure on monoaminergic activity in the brain of a tropical wrasse, Halicoeres trimaculatus: possible implication for controlling tidal-related reproductive activity. Gen Comp Endocr 175:173–179
Tchoudakova A, Callard GV (1998) Identification of multiple cyp19 genes encoding different cytochrome p450 aromatase isozymes in brain and ovary. Endocrinology 139:2179–2189
Tchoudakova A, Kishida M, Wood E, Callard GV (2001) Promoter characteristics of two cyp19 genes differentially expressed in the brain and ovary of teleost fish. J Steroid Biochem 78:427–439
Villeneuve DL, Knoebl I, Kahl MD, Jensen KM, Hammermeister DE, Greene KJ, Blake LS, Ankley GT (2006) Relationship between brain and ovary aromatase activity and isoformspecific aromatase mRNA expression in the fathead minnow (Pimephales promelas). Aquat Toxicol 76:353–368
Wallace RA, Selman K (1981) Cellular and dynamic aspects of oocyte growth in teleost. Amer Zool 21:325–343
Warner RR (1982) Mating systems, sex change and sexual demography in the rainbow wrasse, Thalassoma lucasanum. Copeia 1982: 653–661
Zwain IH, Yen SS (1999) Neurosteroidogenesis in astrocytes, oligo-dendrocytes, and neurons of the cerebral cortex of rat brain. Endocrinology 140:3843–3852
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Oh, DJ., Hur, SP., Bouchekioua, S. et al. Tide-related Changes in mRNA Abundance of Aromatases and Estrogen Receptors in the Ovary and Brain of the Threespot Wrasse Halichoeres trimaculatus. Ocean Sci. J. 53, 239–249 (2018). https://doi.org/10.1007/s12601-018-0016-0
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s12601-018-0016-0