Skip to main content
SpringerLink
Log in

Comparison of Growth-Related Traits and Gene Expression Profiles Between the Offspring of Neomale (XX) and Normal Male (XY) Rainbow Trout

  • Original Article
  • Published:
Marine Biotechnology Aims and scope Submit manuscript

Abstract

All-female lines of fish are created by crossing sex reversed (XX genotype) males with normal females. All-female lines avoid the deleterious phenotypic effects that are typical of precocious maturation in males. To determine whether all-female and mixed sex populations of rainbow trout (Oncorhynchus mykiss) differ in performance, we compared the growth and gene expression profiles in progeny groups produced by crossing a XX male and a XY male to the same five females. Body weight and length were measured in the resulting all-female (XX) and mixed sex (XX/XY) offspring groups. Microarray experiments with liver and white muscle were used to determine if the gene expression profiles of large and small XX offspring differ from those in large and small XX/XY offspring. We detected no significant differences in body length and weight between offspring groups but XX offspring were significantly less variable in the value of these traits. A large number of upregulated genes were shared between the large XX and large XX/XY offspring; the small XX and small XX/XY offspring also shared similar expression profiles. No GO category differences were seen in the liver or between the large XX and large XX/XY offspring in the muscle. The greatest differences between the small XX and small XX/XY offspring were in the genes assigned to the “small molecule metabolic process” and “cellular metabolic process” GO level 3 categories. Similarly, genes within these categories as well as the category “macromolecule metabolic process” were more highly expressed in small compared to large XX fish.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

Similar content being viewed by others

References

  • Amaral IP, Johnston IA (2011) Insulin-like growth factor (IGF) signalling and genome-wide transcriptional regulation in fast muscle of zebrafish following a single-satiating meal. J Exp Biol 214:2125–2139

  • Amaral IPG, Johnston IA (2012) Experimental selection for body size at age modifies early life-history traits and muscle gene expression in adult zebrafish. J Exp Biol 215:3895–3904

    Article  CAS  PubMed  Google Scholar 

  • Berejikian BA, Van Doornik DM, Endicott RC, Hoffnagle TL, Tezak EP, Moore ME, Atkins J (2010) Mating success of alternative male phenotypes and evidence for frequency-dependent selection in Chinook salmon, Oncorhynchus tshawytscha. Can J Fish Aquat Sci 67:1933–1941

    Article  Google Scholar 

  • Beshiri ML, Holmes KB, Richter WF, Hess S, Islam AB, Yan Q, Plante L, Litovchick L, Gévry N, Lopez-Bigas N, Kaelin WG Jr, Benevolenskaya EV (2012) Coordinated repression of cell cycle genes by KDM5A and E2F4 during differentiation. Proc Natl Acad Sci U S A 109:18499–18504

    Article  PubMed Central  PubMed  Google Scholar 

  • Brunelli JP, Wertzler KJ, Sundin K, Thorgaard GH (2008) Y-specific sequences and polymorphisms in rainbow trout and Chinook salmon. Genome 51:739–748

    Article  CAS  PubMed  Google Scholar 

  • Campbell B, Dickey JT, Swanson P (2003) Endocrine changes during onset of puberty in male spring Chinook salmon, Oncorhynchus tshawytscha. Biol Reprod 69:2109–2117

    Article  CAS  PubMed  Google Scholar 

  • Carpio Y, Acosta J, Morales R, Santisteban Y, Sanchéz A, Estrada MP (2009) Regulation of body mass growth through activin type IIB receptor in teleost fish. Gen Comp Endocrinol 160:158–167

    Article  CAS  PubMed  Google Scholar 

  • Cassie S, Koturbash I, Hudson D, Baker M, Ilnytskyy Y, Rodriguez-Juarez R, Weber E, Kovalchuk O (2006) Novel retinoblastoma binding protein RBBP9 modulates sex-specific radiation responses in vivo. Carcinogenesis 27:465–474

    Article  CAS  PubMed  Google Scholar 

  • Christensen LC, Jensen NW, Vala A, Kamarauskaite J, Johansson L, Winther JR, Hofmann K, Teilum K, Ellgaard L (2012) The human selenoprotein VCP-interacting membrane protein (VIMP) is non-globular and harbors a reductase function in an intrinsically disordered region. J Biol Chem 287:26388–26399

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Cohen PT (2002) Protein phosphatase 1—targeted in many directions. J Cell Sci 115:241–256

    CAS  PubMed  Google Scholar 

  • Danzmann RG, Davidson EA, Ferguson MM, Gharbi K, Koop BF, Hoyheim B, Lien S, Lubieniecki KP, Moghadam HK, Park J, Phillips RB, Davidson WS (2008) Distribution of ancestral proto-Actinopterygian chromosome arms within the genomes of 4R-derivative salmonid fishes (Rainbow trout and Atlantic salmon). BMC Genomics. doi:10.1186/1471-2164-9-557

    PubMed Central  PubMed  Google Scholar 

  • Devlin RH, Sakhrani D, White S, Overturf K (2013) Effects of domestication and growth hormone transgenesis on mRNA profiles in rainbow trout (Oncorhynchus mykiss). J Anim Sci. doi:10.2527/jas. 2013-6612

    PubMed  Google Scholar 

  • Dormoy-Raclet V, Markovits J, Malato Y, Huet S, Lagarde P, Montaudon D, Jacquemin-Sablon A, Jacquemin-Sablon H (2007) Unr, a cytoplasmic RNA-binding protein with cold-shock domains, is involved in control of apoptosis in ES and HuH7 cells. Oncogene 26:2595–2605

    Article  CAS  PubMed  Google Scholar 

  • Ducreux S, Gregory P, Schwaller B (2012) Inverse regulation of the cytosolic Ca2+ buffer parvalbumin and mitochondrial volume in muscle cells via SIRT1/PGC-1α axis. PLoS One. doi:10.1371/journal.pone.0044837

    PubMed Central  PubMed  Google Scholar 

  • Dumas A, France J, Bureau DP (2007) Evidence of three growth stanzas in rainbow trout (Oncorhynchus mykiss) across life stages and adaptation of the thermal-unit growth coefficient. Aquaculture 267:139–146

    Article  Google Scholar 

  • Espinosa E, Josa A, Gil L, González N (2011) Sex steroid levels in XY males and sex-reversed XX males, of rainbow trout (Oncorhynchus mykiss), during the reproductive cycle. Reprod Domest Anim 46:8–14

    Article  CAS  PubMed  Google Scholar 

  • Fuentes EN, Valdés JA, Molina A, Björnsson BT (2013) Regulation of skeletal muscle growth in fish by the growth hormone–insulin-like growth factor system. Gen Comp Endocrinol 192:136–148

    Article  CAS  PubMed  Google Scholar 

  • Guiry A, Flynn D, Hubert S, O’Keeffe AM, LeProvost O, White SL, Forde PF, Davoren P, Houeix B, Smith TJ, Cotter D, Wilkins NP, Cairns MT (2010) Testes and brain gene expression in precocious male and adult maturing Atlantic salmon (Salmo salar). BMC Genomics. doi:10.1186/1471-2164-11-211

    PubMed Central  PubMed  Google Scholar 

  • Haidle L, Janssen JE, Gharbi K, Moghadam HK, Ferguson MM, Danzmann RG (2008) Determination of quantitative trait loci (QTL) for early maturation in rainbow trout (Oncorhynchus mykiss). Mar Biotechnol 10:579–592

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Hamade A, Deries M, Begemann G, Bally-Cuif L, Genêt C, Sabatier F, Bonnieu A, Cousin X (2006) Retinoic acid activates myogenesis in vivo through Fgf8 signalling. Dev Biol 289:127–140

    Article  CAS  PubMed  Google Scholar 

  • Harr MW, Distelhorst CW (2010) Apoptosis and autophagy: decoding calcium signals that mediate life or death. Cold Spring Harb Perspect Biol. doi:10.1101/cshperspect.a005579

    PubMed Central  PubMed  Google Scholar 

  • Hevrøy EM, Azpeleta C, Shimizu M, Lanzén A, Kaiya H, Espe M, Olsvik PA (2011) Effects of short-term starvation on ghrelin, GH-IGF system, and IGF-binding proteins in Atlantic salmon. Fish Physiol Biochem 37:217–232

    Article  PubMed  Google Scholar 

  • Hofmann-Lehmann R, Holznagel E, Lutz H (1998) Female cats have lower rates of apoptosis in peripheral blood lymphocytes than male cats: correlation with estradiol-17 beta, but not with progesterone blood levels. Vet Immunol Immunopathol 65:151–160

    Article  CAS  PubMed  Google Scholar 

  • Hopkins CL, Todd PR (1991) Production of monosex and triploid salmon stocks. New Zealand Freshwater Fisheries Report No. 128. MAF Fisheries, Christchurch

  • Ji XS, Liu HW, Chen SL, Jiang YL, Tian YS (2011) Growth differences and dimorphic expression of growth hormone (GH) in female and male Cynoglossus semilaevis after male sexual maturation. Mar Genomics 4:9–16

    Article  PubMed  Google Scholar 

  • Kinyamu HK, Collins JB, Grissom SF, Hebbar PB, Archer TK (2008) Genome wide transcriptional profiling in breast cancer cells reveals distinct changes in hormone receptor target genes and chromatin modifying enzymes after proteasome inhibition. Mol Carcinog 47:845–885

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Kocmarek AL, Ferguson MM, Danzmann RG (2014) Differential gene expression in small and large rainbow trout derived from two seasonal spawning groups. BMC Genomics 15:57. doi:10.1186/1471-2164-15-57

    Article  PubMed Central  PubMed  Google Scholar 

  • Kocour M, Linhart O, Gela D, Rodina M (2005) Growth performance of all-female and mixed-sex common carp Cyprinus carpio L. populations in the central Europe climatic conditions. J World Aquacult Soc 36:103–113

    Article  Google Scholar 

  • Liu H, Guan B, Xu J, Changchun H, Tian H, Chen H (2012) Genetic manipulation of sex ratio for the large-scale breeding of YY super-male and XY all-male yellow catfish (Pelteobagrus fulvidraco (Richardson)) Mar. Biotechnologyl 15:321–328

    Google Scholar 

  • Luo K, Xiao J, Liu S, Wang J, He W, Hu J, Qin Q, Zhang C, Tao M, Liu Y (2011) Massive production of all-female diploids and triploids in the crucian carp. Int J Biol Sci 7:487–495

    Article  PubMed Central  PubMed  Google Scholar 

  • Molloy EJ, O’Neill AJ, Grantham JJ, Sheridan-Pereira M, Fitzpatrick JM, Webb DW, Watson RW (2003) Sex-specific alterations in neutrophil apoptosis: the role of estradiol and progesterone. Blood 102:2653–2659

    Article  CAS  PubMed  Google Scholar 

  • Moolmuang B, Tainsky MA (2011) CREG1 enhances p16(INK4a) -induced cellular senescence. Cell Cycle 10:518–530

  • Mora AL, LaVoy J, McKean M, Stecenko A, Brigham KL, Parker R, Rojas M (2005) Prevention of NF-kappaB activation in vivo by a cell-permeable NF-kappaB inhibitor peptide. Am J Physiol Lung Cell Mol Physiol 289:L536–L544

    Article  CAS  PubMed  Google Scholar 

  • Naevdal G, Holm M, Leroy R, Moller D (1979) Individual growth rate and age at sexual maturity in rainbow trout. FiskDir Skr Ser HavUnders 17:1–10

    Google Scholar 

  • Nynca J, Kuźmiński H, Dietrich GJ, Hliwa P, Dobosz S, Liszewska E, Karol H, Ciereszko A (2012a) Biochemical and physiological characteristics of semen of sex-reversed female rainbow trout (Oncorhynchus mykiss, Walbaum). Theriogenology 77:174–183

    Article  CAS  PubMed  Google Scholar 

  • Nynca J, Kuźmiński H, Dietrich GJ, Hliwa P, Dobosz S, Liszewska E, Karol H, Ciereszko A (2012b) Changes in sperm parameters of sex-reversed female rainbow trout during spawning season in relation to sperm parameters of normal males. Theriogenology 77:1381–1389

    Article  CAS  PubMed  Google Scholar 

  • Orrenius S, Nicotera P, Zhivotovsky B (2003) Cell death mechanisms and their implications in toxicology. Toxicol Sci 119:3–19

    Article  Google Scholar 

  • Parker EA, Hegde A, Buckley M, Barnes KM, Baron J, Nilsson O (2007) Spatial and temporal regulation of GH-IGF-related gene expression in growth plate cartilage. J Endocrinol 194:31–40

    Article  CAS  PubMed  Google Scholar 

  • Perera S, Mankoo B, Gautel M (2012) Developmental regulation of MURF E3 ubiquitin ligases in skeletal muscle. J Muscle Res Cell Motil 33:107–122

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Phumyu N, Boonanuntanasarn S, Jangprai A, Yoshizaki G, Na-Nakorn U (2012) Pubertal effects of 17α-methyltestosterone on GH-IGF-related genes of the hypothalamic-pituitary-liver-gonadal axis and other biological parameters in male, female and sex-reversed Nile tilapia. Gen Comp Endocrinol 177:287–292

    Article  Google Scholar 

  • Racay P, Gregory P, Schwaller B (2006) Parvalbumin deficiency in fast-twitch muscles leads to increased 'slow-twitch type' mitochondria, but does not affect the expression of fiber specific proteins. FEBS J 273:96–108

    Article  CAS  PubMed  Google Scholar 

  • Rescan P-Y, Montfort J, Rallière C, Le Cam A, Esquerré D, Hugot K (2007) Dynamic gene expression in fish muscle during recovery growth induced by a fasting-refeeding schedule. BMC Genomics 8:438–455

    Article  PubMed Central  PubMed  Google Scholar 

  • Rise ML, Douglas SE, Sakhrani D, Williams J, Ewart KV, Rise M, Davidson WS, Koop BF, Devlin RH (2006) Multiple microarray platforms utilized for hepatic gene expression profiling of GH transgenic coho salmon with and without ration restriction. J Mol Endocrinol 37:259–282

    Article  CAS  PubMed  Google Scholar 

  • Rougeot C, Nicayenzi F, Mandiki SN, Rurangwa E, Kestemont P, Mélard C (2004) Comparative study of the reproductive characteristics of XY male and hormonally sex-reversed XX male Eurasian perch, Perca fluviatilis. Theriogenology 62:790–800

    Article  PubMed  Google Scholar 

  • Salem M, Kenney PB, Rexroad CE 3rd, Yao J (2006a) Microarray gene expression analysis in atrophying rainbow trout muscle: a unique nonmammalian muscle degradation model. Physiol Genomics 28:33–45

    Article  CAS  PubMed  Google Scholar 

  • Salem M, Kenney PB, Rexroad CE 3rd, Yao J (2006b) Molecular characterization of muscle atrophy and proteolysis associated with spawning in rainbow trout. Comp Biochem Physiol D Genomics Proteomics 1:227–237

    Article  Google Scholar 

  • Seebacher F, Walter I (2012) Differences in locomotor performance between individuals: importance of parvalbumin, calcium handling and metabolism. J Exp Biol 215:663–670

    Article  CAS  PubMed  Google Scholar 

  • Small CM, Carney GE, Mo Q, Vannucci M, Jones AG (2009) A microarray analysis of sex- and gonad-biased gene expression in the zebrafish: evidence for masculinization of the transcriptome. BMC Genomics. doi:10.1186/1471-2164-10-579

    PubMed Central  PubMed  Google Scholar 

  • Sreenivasan R, Cai M, Bartfai R, Wang X, Christoffels A, Orban L (2008) Transcriptomic analyses reveal novel genes with sexually dimorphic expression in the zebrafish gonad and brain. PLoS One. doi:10.1371/journal.pone.0001791

    PubMed Central  PubMed  Google Scholar 

  • Stejskal V, Kouřil J, Musil J, Hamáčková J, Policar J (2009) Growth pattern of all-female perch (Perca fluviatilis L.) juveniles—is monosex perch culture beneficial? J Appl Ichthyol 25:432–437

    Article  Google Scholar 

  • Stokes EA, Lonergan W, Weber LP, Janz DM, Poznanski AA, Balch GC, Metcalfe CD, Grober MS (2004) Decreased apoptosis in the forebrain of adult male Medaka (Oryzias latipes) after aqueous exposure to ethinylestradiol. Comp Biochem Physiol C Toxicol Pharmacol 138:163–167

    Article  PubMed  Google Scholar 

  • Sun CF, Tao Y, Jiang XY, Zou SM (2011) IGF binding protein 1 is correlated with hypoxia-induced growth reduce and developmental defects in grass carp (Ctenopharyngodon idellus) embryos. Gen Comp Endocrinol 172:409–415

    Article  CAS  PubMed  Google Scholar 

  • Taggart JB, Hynes RA, Prodöuhl PA, Ferguson A (1992) A simplified protocol for routine total DNA isolation from salmonid fishes. J Fish Biol 40:963–965

    Article  CAS  Google Scholar 

  • Tan I, Ng CH, Lim L, Leung T (2001) Phosphorylation of a novel myosin binding subunit of protein phosphatase 1 reveals a conserved mechanism in the regulation of actin cytoskeleton. J Biol Chem 276:21209–21216

    Article  CAS  PubMed  Google Scholar 

  • Thrope JE (1977) Bimodal distribution of length of juvenile Atlantic salmon (Salmo salar L.) under artificial rearing conditions. J Fish Biol 11:175–184

    Article  Google Scholar 

  • Tymchuk W, Sakhrani D, Devlin R (2009) Domestication causes large-scale effects on gene expression in rainbow trout: analysis of muscle, liver and brain transcriptomes. Gen Comp Endocrinol 164:175–183

    Article  CAS  PubMed  Google Scholar 

  • Ulloa PE, Peña AA, Lizama CD, Araneda C, Iturra P, Neira R, Medrano JF (2013) Growth response and expression of muscle growth-related candidate genes in adult zebrafish fed plant and fishmeal protein-based diets. Zebrafish. doi:10.1089/zeb.2012.0823

    PubMed  Google Scholar 

  • von Schalburg KR, Rise ML, Cooper GA, Brown GD, Gibbs AR, Nelson CC, Davidson WS, Koop BF (2005) Fish and chips: various methodologies demonstrate utility of a 16,006-gene salmonid microarray. BMC Genomics 15:126–133

    Article  Google Scholar 

  • White SL, Sakhrani D, Danzmann RG, Devlin RH (2013) Influence of developmental stage and genotype on liver mRNA levels among wild, domesticated, and hybrid rainbow trout (Oncorhynchus mykiss). BMC Genomics. doi:10.1186/1471-2164-14-673

    Google Scholar 

  • Zheng W, Xu H, Lam SH, Luo H, Karuturi RK, Gong Z (2013) Transcriptomic analyses of sexual dimorphism of the zebrafish liver and the effect of sex hormones. PLoS One. doi:10.1371/journal.pone.0053562

    Google Scholar 

Download references

Acknowledgments

This investigation was supported by a Natural Sciences and Engineering Research Council of Canada Strategic Grant. For providing the experimental fish used in this study, the authors wish to thank Sean Pressey and Lynn and Clarke Rieck from Lyndon Fish Hatcheries Inc. We also wish to thank Michael Burke and the staff of the Alma Aquaculture Research Station for the care and maintenance of the experimental fish. Additionally, Xia Yue and Anne Easton helped with the collection of the phenotypic data and tissue samples.

Conflict of Interest

The authors state this research is free of conflicts of interest.

Author information

Authors and Affiliations

  1. Department of Integrative Biology, University of Guelph, 50 Stone Rd. East, Guelph, Ontario, N1G 2W1, Canada

    Andrea L. Kocmarek, Moira M. Ferguson & Roy G. Danzmann

Authors
  1. Andrea L. Kocmarek
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Moira M. Ferguson
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Roy G. Danzmann
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding authors

Correspondence to Andrea L. Kocmarek or Roy G. Danzmann.

Electronic Supplementary Material

Below is the link to the electronic supplementary material.

Online Resources 1–8

Tables displaying up-regulated genes in the large and small XX and XX/XY offspring for the liver and the white muscle. Tables contain gene names (when known), the Agilent identification numbers, the fold-change between the large and small fish, and the p-value. (DOCX 141 kb)

Online Resource 9

Displays the genes, with their Agilent identification numbers, fold-change between the large and small fish, and the p-values, up-regulated in the white muscle falling within the GO ‘cellular process category’ for the large and small XX offspring and the small XX/XY offspring in the white muscle. (DOCX 33 kb)

Online Resource 10

Displays the genes, with their Agilent identification numbers, fold-change between the large and small fish, and the p-values, up-regulated in the white muscle falling within the GO ‘metabolic process’ category for the large and small XX offspring and the small XX/XY offspring in the white muscle. (DOCX 29 kb)

Online Resource 11

Displays the genes, with their Agilent identification numbers, fold-change between the large and small fish, and the p-values, up-regulated in the white muscle falling within the GO ‘cellular component organization’ category for the large XX offspring and the small XX/XY offspring in the white muscle. (DOCX 22 kb)

Online Resource 12

Displays the genes, with their Agilent identification numbers, fold-change between the large and small fish, and the p-values, up-regulated in the white muscle falling within the GO ‘response to stimulus’ category for the large and small XX offspring in the white muscle. (DOCX 18 kb)

Online Resource 13–16

Contains the list of the sequences falling within each GO category in the liver and the white muscle for the XX/XY offspring and the XX offspring. (XLSX 52 kb)

Online Resource 17

Contains the G-test of heterogeneity results for the white muscle at GO level 2 (XLSX 13 kb)

Online Resource 18

Displays the genes, with their Agilent identification numbers, fold-change between the large and small fish, and the p-values, up-regulated in the white muscle falling within the GO ‘macromolecule metabolic process’ category for the large and small XX offspring in the white muscle. (DOCX 17 kb)

Online Resource 19

Displays the genes, with their Agilent identification numbers, fold-change between the large and small fish, and the p-values, up-regulated in the white muscle falling within the GO ‘small molecule metabolic process’ category for the small XX offspring in the white muscle. (DOCX 16 kb)

Online Resource 20

Displays the genes, with their Agilent identification numbers, fold-change between the large and small fish, and the p-values, up-regulated in the white muscle falling within the GO ‘cellular metabolic process’ category for the large and small XX offspring and the small XX/XY offspring in the white muscle. (DOCX 25 kb)

Online Resource 21

Contains the G-test of heterogeneity results for the white muscle at GO level 3. (XLSX 16 kb)

Online Resources 22 and 23

Contains the G-test of heterogeneity results for the liver at GO levels 2 and 3. (XLSX 22 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Kocmarek, A.L., Ferguson, M.M. & Danzmann, R.G. Comparison of Growth-Related Traits and Gene Expression Profiles Between the Offspring of Neomale (XX) and Normal Male (XY) Rainbow Trout. Mar Biotechnol 17, 229–243 (2015). https://doi.org/10.1007/s10126-015-9612-5

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10126-015-9612-5

Keywords

Search

Navigation