Abstract
Sex dimorphic growth pattern has significant theory and application implications in fish. Recently, a Y- and X-specific allele marker-assisted sex control technique has been developed for mass production of all-male population in yellow catfish (Pelteobagrus fulvidraco), but the genetic information for sex determination and sex control breeding has remained unclear. Here, we attempted to provide the first insight into a comprehensive transcriptome covering multiple tissues from XX females, XY males, and YY super-males of yellow catfish by using 454 GS-FLX platform, for a better assembly and gene coverage. A total of 1,202,933 high quality reads (about 540 Mbp) were obtained and assembled into 28,297 contigs and 141,951 singletons. BLASTX searches against the NCBI non-redundant protein database (nr) led a total of 52,564 unique sequences including 18,748 contigs and 33,816 singletons to match 25,669 known or predicted unique proteins. All of them with annotated function were categorized by gene ontology (GO) analysis, and 712 were assigned to reproduction and reproductive process. Some potential genes relevant to reproductive system including steroid hormone biosynthesis and GnRH (gonadotropin-releasing hormone) signaling pathway were further identified by Kyoto Encyclopedia of Genes and Genomes (KEGG) analysis; and at least 21 sex determination and differentiation-related genes, such as Dmrt1, Sox9a/b, Cyp19b, WT1, and AMH were identified and characterized. Additionally, a total of 82,794 simple sequence repeats (SSRs), 26,450 single nucleotide polymorphisms (SNPs), and 4,145 insertions and deletions (INDELs) were revealed from the transcriptome data. Therefore, the current transcriptome resources highlight further studies on sex-control breeding in yellow catfish and will benefit future studies on reproduction and sex determination in teleost fish.
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References
Baroiller JF, D’Cotta H, Bezault E, Wessels S, Hoerstgen-Schwark G (2009) Tilapia sex determination: where temperature and genetics meet. Comp Biochem Physiol A Mol Integr Physiol 153:30–38
Chen J, Hu W, Zhu ZY (2013a) Progress in studies of fish reproductive development regulation. Chin Sci Bull 58:7–16
Chen Z, Gui J, Gao X, Pei C, Hong Y, Zhang Q (2013b) Genome architecture changes and major gene variations of Andrias davidianus ranavirus (ADRV). Vet Res 44:101
Dan C, Mei J, Wang D, Gui J (2013) Genetic differentiation and efficient sex-specific marker development of a pair of Y- and X-linked marker in yellow catfish. Int J Biol Sci 9:1043–1049
Gao Z, Luo W, Liu H, Zeng C, Liu X et al (2012) Transcriptome analysis and SSR/SNP markers information of the blunt snout bream (Megalobrama amblycephala). PLoS ONE 7:e42637
Gui J (2007) Genetic basis and artificial control of sexuality and reproduction in fish. Science Press, Beijing
Gui J, Zhou L (2010) Genetic basis and breeding application of clonal diversity and dual reproduction modes in polyploid Carassius auratus gibelio. Sci China Life Sci 53:409–415
Gui J, Zhu Z (2012) Molecular basis and genetic improvement of economically important traits in aquaculture animals. Chin Sci Bull 57:1751–1760
Haffray P, Vauchez C, Vandeputte M, Linhart O (1998) Different growth and processing traits in males and females of European catfish, Silurus glanis. Aquat Living Resour 11:341–345
Hattori RS, Murai Y, Oura M, Masuda S, Majhi SK et al (2012) A Y-linked anti-Mullerian hormone duplication takes over a critical role in sex determination. Proc Natl Acad Sci U S A 109:2955–2959
Henken A, Brunink A, Richter C (1987) Differences in growth rate and feed utilization between diploid and triploid African catfish, Clarias gariepinus (Burchell 1822). Aquaculture 63:233–242
Hu W, Li SF, Tang B, Wang YP, Lin HR et al (2007) Antisense for gonadotropin-releasing hormone reduces gonadotropin synthesis and gonadal development in transgenic common carp (Cyprinus carpio). Aquaculture 271:498–506
Huang F, Yan A, Xiong C, Zhen R, Zhang G (1999) Evaluation of the nutrition and the rate of flesh in the whole body of Pelteobagrus fulvidraco rich. Freshw Fish 29:3–6
Huang W, Zhou L, Li Z, Gui JF (2009) Expression pattern, cellular localization and promoter activity analysis of ovarian aromatase (Cyp19a1a) in protogynous hermaphrodite red-spotted grouper. Mol Cell Endocrinol 307:224–236
Ijiri S, Kaneko H, Kobayashi T, Wang DS, Sakai F et al (2008) Sexual dimorphic expression of genes in gonads during early differentiation of a teleost fish, the Nile tilapia Oreochromis niloticus. Biol Reprod 78:333–341
Jeong K, Kaiser U (2006) Gonadotropin-releasing hormone regulation of gonadotropin biosynthesis and secretion. In: Neill JD (ed) Knobil and Neill’s physiology of reproduction. Elsevier, Amsterdam, pp 1635–1726
Kamiya T, Kai W, Tasumi S, Oka A, Matsunaga T et al (2012) A trans-species missense SNP in Amhr2 is associated with sex determination in the tiger pufferfish, Takifugu rubripes (fugu). PLoS Genet 8:e1002798
Kobayashi Y, Nagahama Y, Nakamura M (2013) Diversity and plasticity of sex determination and differentiation in fishes. Sex Dev 7:115–125
Lee BY, Coutanceau JP, Ozouf-Costaz C, D’Cotta H, Baroiller JF et al (2011) Genetic and physical mapping of sex-linked AFLP markers in Nile tilapia (Oreochromis niloticus). Mar Biotechnol (NY) 13:557–562
Li CJ, Zhou L, Wang Y, Hong YH, Gui JF (2005) Molecular and expression characterization of three gonadotropin subunits common alpha, FSHbeta and LHbeta in groupers. Mol Cell Endocrinol 233:33–46
Li M, Hong N, Gui J, Hong Y (2012) Medaka piwi is essential for primordial germ cell migration. Curr Mol Med 12:1040–1049
Li WS, Lin HR (2010) The endocrine regulation network of growth hormone synthesis and secretion in fish: Emphasis on the signal integration in somatotropes. Sci China Life Sci 53:462–470
Li XY, Zhang XJ, Li Z, Hong W, Liu W, Zhang J, Gui JF (2014a) Evolutionary history of two divergent Dmrt1 genes reveals two rounds of polyploidy origins in gibel carp. Mol Phylogenet Evol 78:96–104
Li XY, Li Z, Zhang XJ, Zhou L, Gui JF (2014b) Expression characterization of testicular DMRT1 in both Sertoli cells and spermatogenic cells of polyploid gibel carp. Gene 548:119–125
Liang HW, Hu GF, Li Z, Zou GW, Liu XL (2012) Mitochondrial DNA sequence of yellow catfish (Pelteobagrus fulvidraco). Mitochondrial DNA 23:170–172
Liao X, Cheng L, Xu P, Lu G, Wachholtz M et al (2013) Transcriptome analysis of Crucian Carp (Carassius auratus), an important aquaculture and hypoxia-tolerant species. PLoS ONE 8:e62308
Liu H, Cui S, Hou C, Xu J, Chen H (2007) YY super-male generated gynogenetically from XY female in Pelteobagrus fulvidraco (Richardson). Acta Hydrobiol Sin 31:718–725
Liu F, Sun F, Li J, Xia JH, Lin G et al (2013a) A microsatellite-based linkage map of salt tolerant tilapia (Oreochromis mossambicus x Oreochromis spp.) and mapping of sex-determining loci. BMC Genomics 14:58
Liu H, Guan B, Xu J, Hou C, Tian H et al (2013b) Genetic manipulation of sex ratio for the large-scale breeding of YY super-male and XY all-male yellow catfish (Pelteobagrus fulvidraco (Richardson)). Mar Biotechnol (NY) 15:321–328
Ma K, Qiu G, Feng J, Li J (2012) Transcriptome analysis of the oriental river prawn, Macrobrachium nipponense using 454 pyrosequencing for discovery of genes and markers. PLoS ONE 7:e39727
Masuyama H, Yamada M, Kamei Y, Fujiwara-Ishikawa T, Todo T et al (2012) Dmrt1 mutation causes a male-to-female sex reversal after the sex determination by Dmy in the medaka. Chromosome Res 20:163–176
Matsuda M, Nagahama Y, Shinomiya A, Sato T, Matsuda C et al (2002) DMY is a Y-specific DM-domain gene required for male development in the medaka fish. Nature 417:559–563
Mei J, Gui JF (2014) Genetic basis and biotechnological manipulation of sexual dimorphism and sex determination in fish. Sci China Life Sci 57: in press
Mei J, Yue HM, Li Z, Chen B, Zhong JX et al (2013) C1q-like Factor, a Target of miR-430, Regulates Primordial Germ Cell Development in Early Embryos of Carassius auratus. Int J Biol Sci 10:15–24
Nakamura M (2010) The mechanism of sex determination in vertebrates-are sex steroids the key-factor? J Exp Zool A Ecol Genet Physiol 313:381–398
Nakamura M (2013) Is a sex-determining gene(s) necessary for sex-determination in amphibians? Steroid hormones may be the key factor. Sex Dev 7:104–114
Peng JX, Xie JL, Zhou L, Hong YH, Gui JF (2009) Evolutionary conservation of Dazl genomic organization and its continuous and dynamic distribution throughout germline development in gynogenetic gibel carp. J Exp Zool B Mol Dev Evol 312:855–871
Ramsey M, Crews D (2009) Steroid signaling and temperature-dependent sex determination-Reviewing the evidence for early action of estrogen during ovarian determination in turtles. Semin Cell Dev Biol 20:283–292
Ribas L, Pardo BG, Fernandez C, Alvarez-Dios JA, Gomez-Tato A et al (2013) A combined strategy involving Sanger and 454 pyrosequencing increases genomic resources to aid in the management of reproduction, disease control and genetic selection in the turbot (Scophthalmus maximus). BMC Genomics 14:180
Salem M, Rexroad CE 3rd, Wang J, Thorgaard GH, Yao J (2010) Characterization of the rainbow trout transcriptome using Sanger and 454-pyrosequencing approaches. BMC Genomics 11:564
Sarder MR, Penman DJ, Myers JM, McAndrew BJ (1999) Production and propagation of fully inbred clonal lines in the Nile tilapia (Oreochromis niloticus L.). J Exp Zool 284:675–685
Shi Y, Liu X, Zhang H, Zhang Y, Lu D et al (2012) Molecular identification of an androgen receptor and its changes in mRNA levels during 17alpha-methyltestosterone-induced sex reversal in the orange-spotted grouper Epinephelus coioides. Comp Biochem Physiol B Biochem Mol Biol 163:43–50
Sinclair AH, Berta P, Palmer MS, Hawkins JR, Griffiths BL et al (1990) A gene from the human sex-determining region encodes a protein with homology to a conserved DNA-binding motif. Nature 346:240–244
Slanchev K, Stebler J, de la Cueva-Mendez G, Raz E (2005) Development without germ cells: the role of the germ line in zebrafish sex differentiation. Proc Natl Acad Sci U S A 102:4074–4079
Smith CA, Roeszler KN, Ohnesorg T, Cummins DM, Farlie PG et al (2009) The avian Z-linked gene DMRT1 is required for male sex determination in the chicken. Nature 461:267–271
Sun M, Li Z, Gui JF (2010) Dynamic distribution of spindlin in nucleoli, nucleoplasm and spindle from primary oocytes to mature eggs and its critical function for oocyte-to-embryo transition in gibel carp. J Exp Zool A Ecol Genet Physiol 313:461–473
Taranger GL, Carrillo M, Schulz RW, Fontaine P, Zanuy S et al (2010) Control of puberty in farmed fish. Gen Comp Endocrinol 165:483–515
Vadakkadath Meethal S, Atwood CS (2005) The role of hypothalamic-pituitary-gonadal hormones in the normal structure and functioning of the brain. Cell Mol Life Sci 62:257–270
Vidotto M, Grapputo A, Boscari E, Barbisan F, Coppe A et al (2013) Transcriptome sequencing and de novo annotation of the critically endangered Adriatic sturgeon. BMC Genomics 14:407
Vizziano-Cantonnet D, Anglade I, Pellegrini E, Gueguen MM, Fostier A et al (2011) Sexual dimorphism in the brain aromatase expression and activity, and in the central expression of other steroidogenic enzymes during the period of sex differentiation in monosex rainbow trout populations. Gen Comp Endocrinol 170:346–355
Wang D, Mao HL, Chen HX, Liu HQ, Gui JF (2009) Isolation of Y- and X-linked SCAR markers in yellow catfish and application in the production of all-male populations. Anim Genet 40:978–981
Wang J, Yu X, Zhao K, Zhang Y, Tong J et al (2012) Microsatellite development for an endangered bream Megalobrama pellegrini (Teleostei, Cyprinidae) using 454 sequencing. Int J Mol Sci 13:3009–3021
Wen S, Ai W, Alim Z, Boehm U (2010) Embryonic gonadotropin-releasing hormone signaling is necessary for maturation of the male reproductive axis. Proc Natl Acad Sci U S A 107:16372–16377
Xia W, Zhou L, Yao B, Li CJ, Gui JF (2007) Differential and spermatogenic cell-specific expression of DMRT1 during sex reversal in protogynous hermaphroditic groupers. Mol Cell Endocrinol 263:156–172
Xiao Q, Xia JH, Zhang XJ, Li Z, Wang Y, Zhou L, Gui JF (2014) Type-IV antifreeze proteins are essential for epiboly and convergence in gastrulation of zebrafish embryos. Int J Biol Sci 10:715–732
Xu S, Xia W, Zohar Y, Gui JF (2013) Zebrafish dmrta2 regulates the expression of cdkn2c in spermatogenesis in the adult testis. Biol Reprod 88:14
Yano A, Guyomard R, Nicol B, Jouanno E, Quillet E et al (2012) An immune-related gene evolved into the master sex-determining gene in rainbow trout, Oncorhynchus mykiss. Curr Biol 22:1423–1428
Yin HB, Jia ZH, Yao DX, Sun ZW, Yu B et al (2008) Sex differentiation in Pelteobagrus fulvidraco. Chin J Zool 43:103–108
Zeng V, Ewen-Campen B, Horch HW, Roth S, Mito T et al (2013) Developmental gene discovery in a hemimetabolous insect: de novo assembly and annotation of a transcriptome for the cricket Gryllus bimaculatus. PLoS ONE 8(5):e61479
Zhou L, Gui JF (2010) Molecular mechanisms underlying sex change in hermaphroditic groupers. Fish Physiol Biochem 36:181–193
Acknowledgments
This work was supported by grants to Jie Mei from the Fundamental Research Funds for the Central Universities (2013PY068, 52902–0900202496, 52204–12018) and the National Natural Science Foundation of China (31301931), and to Jian-Fang Gui from the special Fund for Agro-scientific Research in the Public Interest from the Ministry of Agriculture of China (2009030406), the National Key Basic Research Program (2010CB126301). The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.
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Figure S1
Length distribution of Open reading frame (ORF) from all contigs of the transcriptome. (GIF 7 kb)
Table S1
Summary of BLAST nr result for all unique sequences in the transcriptome. (XLSX 1404 kb)
Table S2
List of all the reproduction and reproductive process related genes found in GO analysis of the yellow catfish transcriptome. (XLSX 107 kb)
Table S3
KEGG pathways discovered in the unigenes, contigs and singletons of yellow catfish transcriptome (XLSX 790 kb)
Table S4
The primer sequences for real-time PCR study. (DOCX 17 kb)
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Chen, X., Mei, J., Wu, J. et al. A Comprehensive Transcriptome Provides Candidate Genes for Sex Determination/Differentiation and SSR/SNP Markers in Yellow Catfish. Mar Biotechnol 17, 190–198 (2015). https://doi.org/10.1007/s10126-014-9607-7
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DOI: https://doi.org/10.1007/s10126-014-9607-7