Salinity and photoperiod modulate pubertal development in Atlantic salmon (Salmo salar)

Journal of Endocrinology

Volumn 220, Issue 3, 2014, Pages 319-332

  Melo, Michelle C ^a,b   Andersson, Eva ^c   Fjelldal, Per Gunnar ^c   Bogerd, Jan ^b   França, Luiz R ^a   Taranger, Geir Lasse ^c   Schulz, Rüdiger W ^b  

^a FEDERAL UNIVERSITY OF MINAS GERAIS   (Brazil)

^b UTRECHT UNIVERSITY   (Netherlands)

^c INSTITUTE OF MARINE RESEARCH   (Norway)

Author keywords

Atlantic salmon; Photoperiod; Pituitary gene expression; Salinity; Spermatogenesis

Indexed keywords

ATLANTIC SALMON; PHOTOPERIOD; PITUITARY GENE EXPRESSION; SALINITY; SPERMATOGENESIS;

ANIMALS; FISH PROTEINS; FRESH WATER; MALE; PHOTOPERIOD; PITUITARY GLAND; SALINITY; SALMO SALAR; SEASONS; SEAWATER; SEXUAL MATURATION; SPERMATOGENESIS; TESTIS; TESTOSTERONE;

EID: 84894386364     PISSN: 00220795     EISSN: 14796805     Source Type: Journal    
DOI: 10.1530/JOE-13-0240     Document Type: Article

References (50)

1. Almeida FFL, Kristoffersen C, Taranger GL & Schulz RW 2008 Spermatogenesis in Atlantic cod (Gadus morhua): a novel model of cystic germ cell development. Biology of Reproduction 78 27-34. (doi:10.1095/ biolreprod.107.063669)
2. Amano M, Ikuta K, Kitamura S & Aida K 1999 Effects of photoperiod on salmon GnRH mRNA levels in brain of castrated underyearling precocious male masu salmon. General and Comparative Endocrinology 115 70-75. (doi:10.1006/gcen.1999.7286)
3. Amano M, lkuta K, Kitamura S & Aida K 2001 Effects of photoperiod on pituitary gonadotropin levels in masu salmon. Journal of Experimental Zoology 289 449-455. (doi:10.1002/jez.1026)
4. Andersson E, Mayer I & Borg B 1988 Inhibitory effect of 11-ketoandrostenedione and androstenedione on spermatogenesis in the threespined stickleback, Gasterosteus aculeatus L. Journal of Fish Biology 33 835-840. (doi:10.1111/j.1095-8649.1988.tb05530.x)
5. Andersson E, Schulz RW, Male R, Bogerd J, Patiña D, Benedet S, Norberg B & Taranger GL 2013 Pituitary gonadotropin and ovarian gonadotropin receptor transcript levels: seasonal and photoperiod-induced changes in the reproductive physiology of female Atlantic salmon (Salmo salar). General and Comparative Endocrinology 191 247-258. (doi:10.1016/j.ygcen.2013.07.001)
6. Antonopoulou E, Swanson P & Borg P 2009 Effects of aromatase inhibitors and different doses of testosterone on gonadotropins in one year old male Atlantic salmon (Salmo salar). Comparative Biochemistry and Physiology. Part A, Molecular & Integrative Physiology 153 408-416. (doi:10.1016/j.cbpa.2009.03.019)
7. Arnesen AM, Toften H, Agustsson T, Stefansson SO, Handeland SO & Björnsson BTh 2003 Osmoregulation, feed intake, growth and growth hormone levels in OC Atlantic salmon (Salmo salar L.) transferred to seawater at different stages of smolt development. Aquaculture 222 167-187. (doi:10.1016/S0044-8486(03)00109-1)
8. Balment RJ, Weiqun LU, Weybourne E & Warne JM 2006 Arginine vasotocin a key hormone in Wsh salt and water balance and many other aspects of physiology and behaviour. General and Comparative Endocrinology 147 9-16. (doi:10.1016/j.ygcen.2005.12.022)
9. Berge AI, Berg A, Fyhn HJ, Barnung T, Hansen T & Stefansson SO 1995 Development of salinity tolerance in underyearling smolts of Atlantic salmon (Salmo salar L.) reared under different photoperiods. Canadian Journal of Fisheries and Aquatic Sciences 52 243-251. (doi:10.1139/f95-024)
10. Bogerd J, Blomenröhr M, Andersson E, van der Putten HHAGM, Tensen CP, Vischer HF, Granneman JCM, Janssen-Dommerholt C, Goos HJTh & Schulz RW 2001 Discrepancy between molecular structure and ligand selectivity of a testicular follicle-stimulating hormone receptor of the African catfish (Clarias gariepinus). Biology of Reproduction 64 1633-1643. (doi:10.1095/biolreprod64.6.1633)
11. Borg B, Antonopoulou E, Mayer I, Andersson E, Bergland I & Swanson P 1998 Effects of gonadectomy and androgen treatment on pituitary and plasma levels of gonadotropins in mature Atlantic salmon, Salmo salar, parr - positive feedback control of both gonadotropins. Biology of Reproduction 58 814-820. (doi:10.1095/biolreprod58.3.814)
12. Bromage N, Porter M & Randall C 2001 The environmental regulation of maturation in farmed finfish with special reference to the role of photoperiod and melatonin. Aquaculture 197 63-98. (doi:10.1016/S0044-8486(01)00583-X)
13. Campbell B, Dickey JT & Swanson P 2003 Endocrine changes during onset of puberty in male spring Chinook salmon, Oncorhynchus tshawytscha. Biology of Reproduction 69 2109-2117. (doi:10.1095/biolreprod.103.020560)
14. Chauvigné F, Verdura S,MazónMJ, Duncan N, Zanuy S, Gómez A & CerdáJ 2012 Follicle-stimulating hormone and luteinizing hormone mediate the androgenic pathway in Leydig cells of an evolutionary advanced teleost. Biology of Reproduction 87 1-11. (doi:10.1095/biolreprod.112.101691)
15. Cobb J, Miyaike M, Kikuchi A & Handel MA 1999 Meiotic events at the centromeric heterochromatin: histone H3 phosphorylation, topoisomerase II a localization and chromosome condensation. Chromosoma 108 412-425. (doi:10.1007/s004120050393)
16. Duncan NJ & Bromage N 1998 The effect of different periods of constant short days on smoltification in juvenile Atlantic salmon (Salmo salar). Aquaculture 168 369-386. (doi:10.1016/S0044-8486(98)00363-9)
17. Fjelldal PG, Hansen T & Huang T 2011 Continuous light and elevated temperature can trigger maturation both during and immediately after smoltification in male Atlantic salmon (Salmo salar). Aquaculture 321 93-100. (doi:10.1016/j.aquaculture.2011.08.017)
18. Garcia de Leaniz C, Fleming IA, Einum S, Verspoor E, Jordan WC, Consuegra S, Aubin-Horth N, Lajus D, Letcher BH, Youngson AF et al. 2007 A critical review of adaptive genetic variation in Atlantic salmon: implications for conservation. Biological Reviews of the Cambridge Philosophical Society 82 173-211. (doi:10.1111/j.1469-185X.2006.00004.x)
19. García-López A, Bogerd J, Granneman JC, van Dijk W, Trant JM, Taranger GL,amp; Schulz RW 2009 Leydig cells express FSH receptors in African catfish. Endocrinology 150 357-365. (doi:10.1210/en.2008- 0447)
20. García-López A, Jonge H, Nóbrega RH, Waal PP, Dijk W, Hemrika W, Taranger GL, Bogerd J & Schulz RW 2010 Studies in zebrafish reveal unusual cellular expression patterns of gonadotropin receptor messenger ribonucleic acids in the testis and unexpected functional
21. Gomez JM, Weil C, Ollitrault M, Le Bail PY, Breton B & Le Gac F 1999 Growth hormone (GH) and gonadotropin subunit gene expression and pituitary and plasma changes during spermatogenesis and oogenesis in rainbow trout (Oncorhynchus mykiss). General and Comparative Endocrinology 113 413-428. (doi:10.1006/gcen.1998.7222)
22. Good S, Yegorov S, Martijn J, Franck J & Bogerd J 2012 New insights into ligand-receptor pairing and coevolution of relaxin family peptides and their receptors in teleosts. International Journal of Evolutionary Biology 2012 310278. (doi:10.1155/2012/310278)
23. Hendzel MJ, Wei Y, Mancini MA, Van Hooser A, Ranalli T, Brinkley BR, Bazett-Jones DP DP & Allis CD 1997 Mitosis-specific phosphorylation of histone H3 initiates primarily within pericentromeric heterochromatin during G2 and spreads in an ordered fashion coincident with mitotic chromosome condensation. Chromosoma 106 348-360. (doi:10.1007/s004120050256)
24. Hutchings JA & Jones MEB 1998 Life history variation and growth rate thresholds for maturity in Atlantic salmon (Salmo salar). Canadian Journal of Fisheries and Aquatic Sciences 55 22-47. (doi:10.1139/d98-004)
25. Jonsson N & Jonsson B 2007 Sea growth, smolt age and age at sexual maturation in Atlantic salmon. Journal of Fish Biology 71 245-252. (doi:10.1111/j.1095-8649.2007.01488.x)
26. Jonsson B, Jonsson N, Brodtkorb E & Ingebrigtsen PJ 2001 Life-history traits of brown trout vary with the size of small streams. Functional Ecology 15 310-317. (doi:10.1046/j.1365-2435.2001.00528.x)
27. Luckenbach JA, Dickey JT & Swanson P 2010 Regulation of pituitary GnRH receptor and gonadotropin subunits by IGF1 and GnRH in prepubertal male coho salmon. General and Comparative Endocrinology 167 387-396. (doi:10.1016/j.ygcen.2009.09.010)
28. Maugars G & Schmitz M 2008a Expression of gonadotropin and gonadotropin receptor genes during early sexual maturation in male Atlantic salmon parr. Molecular Reproduction and Development 75 403-413. (doi:10.1002/mrd.20767)
29. Maugars G & Schmitz M 2008b Gene expression profiling during spermatogenesis in early maturing male Atlantic salmon parr testes. General and Comparative Endocrinology 159 178-187. (doi:10.1016/j.ygcen.2008.08.008)
30. Meier KM, Figueiredo MA, Kamimura MT, Laurino J, Maggioni R, Pinto LS, Dellagostin OA, Tesser MB, Sampaio LA & Marins LF 2009 Increased growth hormone (GH), growth hormone receptor (GHR), and insulinlike growth factor I (IGF-I) gene transcription after hyperosmotic stress in the Brazilian flounder Paralichthys orbignyanus. Fish Physiology and Biochemistry 35 501-509. (doi:10.1007/s10695-008-9287-1)
31. Ohta T, Miyake H, Miura C, Kamei H, Aida K & Miura T 2007 Folliclestimulating hormone induces spermatogenesis mediated by androgen production in Japanese eel, Anguilla japonica. Biology of Reproduction 77 970-977. (doi:10.1095/biolreprod.107.062299)
32. Olsvik PA, Lie KK, Jordal AEO, Nilsen TO & Hordvik I 2005 Evaluation of potential reference genes in real-time RT-PCR studies of Atlantic salmon. BMC Molecular Biology 6 1-9. (doi:10.1186/1471-2199-6-21)
33. Oppen-Berntsen DO, Olsen SO, Rong CJ, Taranger GL, Swanson P & Walther BT 1994 Plasma levels of eggshell ZR-proteins, estradiol-17b, and gonadotropins during an annual reproductive cycle of Atlantic salmon (Salmo salar). Journal of Experimental Zoology 268 59-70. (doi:10.1002/jez.1402680108)
34. Planas JV & Swanson P 1995 Maturation-associated changes in the response of the salmon testis to the steroidogenic actions of gonadotropins (GTH I and GTH II) in vitro. Biology of Reproduction 52 697-704. (doi:10.1095/biolreprod52.3.697)
35. Planas JV, Swanson P & DickhoffWW1993 Regulation of testicular steroid production in vitro by gonadotropins (GTH I and GTH II) and cyclic AMP in coho salmon (Oncorhynchus kisutch). General and Comparative Endocrinology 91 8-24. (doi:10.1006/gcen.1993.1099)
36. Rodríguez M & Specker JL 1991 In vitro effects of arginine vasotocin on testosterone production by testes of rainbow trout (Oncorhynchus mykiss). General and Comparative Endocrinology 83 249-257. (doi:10.1016/0016-6480(91)90028-5)
37. Sambroni E, Rolland AD, Lareyre J-J & Le Gac F 2013 Fsh and Lh have common and distinct effects on gene expression in rainbow trout testis. Journal of Molecular Endocrinology 50 1-18. (doi:10.1530/JME-12-0197)
38. Schulz RW 1985 Measurement of 5 androgens in the blood of immature and maturing male rainbow-trout (Salmo-gairdneri Richardson). Steroids 46 717-726. (doi:10.1016/0039-128X(85)90051-0)
39. Schulz RW & Nóbrega RH 2011 Anatomy and histology of fish testis. In Encyclopedia of Fish Physiology: From Genome to Environment, vol 1, pp 616-626. Ed. Anthony P Farrell. San Diego: Academic Press.
40. Scott AP & Sumpter JP 1989 Seasonal variations in testicular germ cell stages and plasma concentrations of sex steroids in male rainbow trout (Salmo gairdneri) maturing at 2 years old. General and Comparative Endocrinology 73 46-58. (doi:10.1016/0016-6480(89)90054-3)
41. Skaar KS, Nóbrega RH, Magaraki A, Olsen LC, Schulz RW & Male R 2011 Proteotytically activated, recombinant anti-Müllerian hormone inhibits androgen secretion, proliferation, and differentiation of spermatogonia in adult zebrafish testis organ culture. Endocrinologist 152 3527-3540. (doi:10.1210/en.2010-1469)
42. Skilbrei OT & Heino M 2011 Reduced daylength stimulates size-dependent precocious maturity in 0C male Atlantic salmon parr. Aquaculture 311 168-174. (doi:10.1016/j.aquaculture.2010.12.004)
43. Stefansson SO, Björnsson B Th, Hansen T, Haux C, Taranger GL & Saunders RL 1991 Growth, parr-smolt transformation and changes in growth hormone of Atlantic salmon (Salmo salar) reared under different photoperiods. Canadian Journal of Fisheries and Aquatic Sciences 48 2100-2108. (doi:10.1139/f91-249)
44. Suzuki K, Nagahama Y & Kawauchi H 1998 Steroidogenic activities of two distinct gonadotropins. General and Comparative Endocrinology 71 452-458. (doi:10.1016/0016-6480(88)90274-2)
45. Swanson P, Bernard M, Nozaki M, Suzuki K, Kawauchi H & Dickhoff WW 1989 Gonadotropins I and II in juvenile coho salmon. Fish Physiology and Biochemistry 7 169-176. (doi:10.1007/BF00004704)
46. Taranger GL, Carrillo M, Schulz RW, Fontaine P, Zanuy S, Felip A, Weltzien FA, Dufour S, Karlsen O, Norberg B et al. 2010 Control of puberty in farmed fish. General and Comparative Endocrinology 165 483-515. (doi:10.1016/j.ygcen.2009.05.004)
47. Taylor EB 1991 A review of local adaptation in Salmonidae, with special reference to Pacific and Atlantic salmon. Aquaculture 98 185-207. (doi:10.1016/0044-8486(91)90383-I)
48. Thrush MA, Duncan NJ,amp; Bromage NR 1994 The use of photoperiod in the production of out-of-season Atlantic salmon (Salmo salar) smolts. Aquaculture 121 29-44. (doi:10.1016/0044-8486(94)90005-1)
49. de Waal PP, Wang DS, Nijenhuis WA, Schulz RW & Bogerd J 2008 Functional characterization and expression analysis of the androgen receptor in zebrafish (Danio rerio) testis. Reproduction 136 225-234. (doi:10.1530/REP-08-0055)
50. Xiong F, Liu D, Elsholtz HP & Hew CL 1994 The Chinook salmon gonadotropin IIb subunit gene contains a strong minimal promoter with a proximal negative element. Molecular Endocrinology 8 771-781. (doi:10.1210/mend.8.6.7935492)