A Comprehensive Transcriptome Provides Candidate Genes for Sex Determination/Differentiation and SSR/SNP Markers in Yellow Catfish

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.

[1]  Wei Huang,et al.  Expression pattern, cellular localization and promoter activity analysis of ovarian aromatase (Cyp19a1a) in protogynous hermaphrodite red-spotted grouper , 2009, Molecular and Cellular Endocrinology.

[2]  J. Gui,et al.  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. , 2010, Journal of experimental zoology. Part A, Ecological genetics and physiology.

[3]  M. Vandeputte,et al.  Different growth and processing traits in males and females of European catfish, Silurus glanis , 1998 .

[4]  Li Zhou,et al.  Genetic basis and breeding application of clonal diversity and dual reproduction modes in polyploid Carassius auratus gibelio , 2010, Science China Life Sciences.

[5]  G. Qiu,et al.  Transcriptome Analysis of the Oriental River Prawn, Macrobrachium nipponense Using 454 Pyrosequencing for Discovery of Genes and Markers , 2012, PloS one.

[6]  A. Sinclair,et al.  The avian Z-linked gene DMRT1 is required for male sex determination in the chicken , 2009, Nature.

[7]  J. Gui,et al.  Zebrafish dmrta2 Regulates the Expression of cdkn2c in Spermatogenesis in the Adult Testis1 , 2013, Biology of reproduction.

[8]  S. Brenner,et al.  A Trans-Species Missense SNP in Amhr2 Is Associated with Sex Determination in the Tiger Pufferfish, Takifugu rubripes (Fugu) , 2012, PLoS genetics.

[9]  Abhishek Kumar,et al.  Transcriptome sequencing and de novo annotation of the critically endangered Adriatic sturgeon , 2013, BMC Genomics.

[10]  Hao Chen,et al.  Isolation of Y- and X-linked SCAR markers in yellow catfish and application in the production of all-male populations. , 2009, Animal genetics.

[11]  U. Boehm,et al.  Embryonic gonadotropin-releasing hormone signaling is necessary for maturation of the male reproductive axis , 2010, Proceedings of the National Academy of Sciences.

[12]  Zuoyan Zhu,et al.  Progress in studies of fish reproductive development regulation , 2013 .

[13]  Wensheng Li,et al.  The endocrine regulation network of growth hormone synthesis and secretion in fish: Emphasis on the signal integration in somatotropes , 2010, Science China Life Sciences.

[14]  Wei-min Wang,et al.  Transcriptome Analysis and SSR/SNP Markers Information of the Blunt Snout Bream (Megalobrama amblycephala) , 2012, PloS one.

[15]  J. Gui,et al.  Molecular and expression characterization of three gonadotropin subunits common α, FSHβ and LHβ in groupers , 2005, Molecular and Cellular Endocrinology.

[16]  L. Han YY SUPERMALE GENERATED GYNOGENETICALLY FROM XY FEMALE IN PELTEOBAGRUS FULVIDRACO (RICHARDSON) , 2007 .

[17]  B. McAndrew,et al.  Production and propagation of fully inbred clonal lines in the Nile tilapia (Oreochromis niloticus L.). , 1999, The Journal of experimental zoology.

[18]  Li Zhou,et al.  Evolutionary conservation of Dazl genomic organization and its continuous and dynamic distribution throughout germline development in gynogenetic gibel carp. , 2009, Journal of experimental zoology. Part B, Molecular and developmental evolution.

[19]  J. Gui,et al.  Type-IV Antifreeze Proteins are Essential for Epiboly and Convergence in Gastrulation of Zebrafish Embryos , 2014, International journal of biological sciences.

[20]  J. Gui,et al.  Expression characterization of testicular DMRT1 in both Sertoli cells and spermatogenic cells of polyploid gibel carp. , 2014, Gene.

[21]  K. Jeong,et al.  CHAPTER 31 – Gonadotropin-Releasing Hormone Regulation of Gonadotropin Biosynthesis and Secretion , 2006 .

[22]  M. Nakamura Is a Sex-Determining Gene(s) Necessary for Sex-Determination in Amphibians? Steroid Hormones May Be the Key Factor , 2012, Sexual Development.

[23]  J. I. Fernandino,et al.  A Y-linked anti-Müllerian hormone duplication takes over a critical role in sex determination , 2012, Proceedings of the National Academy of Sciences.

[24]  S. Roth,et al.  Developmental Gene Discovery in a Hemimetabolous Insect: De Novo Assembly and Annotation of a Transcriptome for the Cricket Gryllus bimaculatus , 2013, PloS one.

[25]  Hua Tian,et al.  Genetic Manipulation of Sex Ratio for the Large-Scale Breeding of YY Super-Male and XY All-Male Yellow Catfish (Pelteobagrus fulvidraco (Richardson)) , 2012, Marine Biotechnology.

[26]  Yong Zhang,et al.  Molecular identification of an androgen receptor and its changes in mRNA levels during 17α-methyltestosterone-induced sex reversal in the orange-spotted grouper Epinephelus coioides. , 2012, Comparative biochemistry and physiology. Part B, Biochemistry & molecular biology.

[27]  Xiao-lin Liu,et al.  Mitochondrial DNA sequence of yellow catfish (Pelteobagrus fulvidraco) , 2012, Mitochondrial DNA.

[28]  J. Gui,et al.  Molecular basis and genetic improvement of economically important traits in aquaculture animals , 2012 .

[29]  R. Guyomard,et al.  An Immune-Related Gene Evolved into the Master Sex-Determining Gene in Rainbow Trout, Oncorhynchus mykiss , 2012, Current Biology.

[30]  T. Todo,et al.  Dmrt1 mutation causes a male-to-female sex reversal after the sex determination by Dmy in the medaka , 2011, Chromosome Research.

[31]  D. Crews,et al.  Steroid signaling and temperature-dependent sex determination-Reviewing the evidence for early action of estrogen during ovarian determination in turtles. , 2009, Seminars in cell & developmental biology.

[32]  J. Gui,et al.  Genetic Differentiation and Efficient Sex-specific Marker Development of a Pair of Y- and X-linked Markers in Yellow Catfish , 2013, International journal of biological sciences.

[33]  J. Baroiller,et al.  Tilapia sex determination: Where temperature and genetics meet. , 2009, Comparative biochemistry and physiology. Part A, Molecular & integrative physiology.

[34]  H. Yue,et al.  C1q-like Factor, a Target of miR-430, Regulates Primordial Germ Cell Development in Early Embryos of Carassius auratus , 2013, International journal of biological sciences.

[35]  J. D. Neill,et al.  Knobil and Neill's Physiology of reproduction , 2006 .

[36]  W. Liu,et al.  Evolutionary history of two divergent Dmrt1 genes reveals two rounds of polyploidy origins in gibel carp. , 2014, Molecular phylogenetics and evolution.

[37]  Qi-ya Zhang,et al.  Genome architecture changes and major gene variations of Andrias davidianus ranavirus (ADRV) , 2013, Veterinary Research.

[38]  A. Gómez-Tato,et al.  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) , 2013, BMC Genomics.

[39]  F. Weltzien,et al.  Control of puberty in farmed fish. , 2010, General and comparative endocrinology.

[40]  Masahisa Nakamura The mechanism of sex determination in vertebrates-are sex steroids the key-factor? , 2010, Journal of experimental zoology. Part A, Ecological genetics and physiology.

[41]  J. Yao,et al.  Characterization of the rainbow trout transcriptome using Sanger and 454-pyrosequencing approaches , 2010, BMC Genomics.

[42]  A microsatellite-based linkage map of salt tolerant tilapia (Oreochromis mossambicus x Oreochromis spp.) and mapping of sex-determining loci , 2013, BMC Genomics.

[43]  O. Kah,et al.  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. , 2011, General and comparative endocrinology.

[44]  J. Gui,et al.  Genetic basis and biotechnological manipulation of sexual dimorphism and sex determination in fish , 2015, Science China Life Sciences.

[45]  Wei Hu,et al.  Antisense for gonadotropin-releasing hormone reduces gonadotropin synthesis and gonadal development in transgenic common carp (Cyprinus carpio) , 2007 .

[46]  C. ozouF-cosTaz,et al.  Genetic and Physical Mapping of Sex-Linked AFLP Markers in Nile Tilapia (Oreochromis niloticus) , 2011, Marine Biotechnology.

[47]  Shuichi Asakawa,et al.  DMY is a Y-specific DM-domain gene required for male development in the medaka fish , 2002, Nature.

[48]  K. Zhao,et al.  Microsatellite Development for an Endangered Bream Megalobrama pellegrini (Teleostei, Cyprinidae) Using 454 Sequencing , 2012, International journal of molecular sciences.

[49]  J. Gui,et al.  Molecular mechanisms underlying sex change in hermaphroditic groupers , 2010, Fish Physiology and Biochemistry.

[50]  Songlin Chen,et al.  Transcriptome Analysis of Crucian Carp (Carassius auratus), an Important Aquaculture and Hypoxia-Tolerant Species , 2013, PloS one.

[51]  Masaru Nakamura,et al.  Diversity and Plasticity of Sex Determination and Differentiation in Fishes , 2012, Sexual Development.

[52]  A. Henken,et al.  Differences in growth rate and feed utilization between male and female African catfish, Clarias gariepinus (Burchell 1822). , 1987 .

[53]  E. Raz,et al.  Development without germ cells: the role of the germ line in zebrafish sex differentiation. , 2005, Proceedings of the National Academy of Sciences of the United States of America.

[54]  Robin Lovell-Badge,et al.  A gene from the human sex-determining region encodes a protein with homology to a conserved DNA-binding motif , 1990, Nature.

[55]  Tohru Kobayashi,et al.  Sexual Dimorphic Expression of Genes in Gonads During Early Differentiation of a Teleost Fish, the Nile Tilapia Oreochromis niloticus1 , 2008, Biology of reproduction.

[56]  C. Atwood,et al.  The role of hypothalamic-pituitary-gonadal hormones in the normal structure and functioning of the brain. , 2005, Cellular and molecular life sciences : CMLS.

[57]  N. Hong,et al.  Medaka piwi is essential for primordial germ cell migration. , 2012, Current molecular medicine.

[58]  J. Gui,et al.  Differential and spermatogenic cell-specific expression of DMRT1 during sex reversal in protogynous hermaphroditic groupers , 2007, Molecular and Cellular Endocrinology.