Volume 43 Issue 2
Mar.  2022
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Zong-Xian Zhu, Yi-Long Lin, Chun-Hui Ai, Ying-Ying Xiong, Dan-Dan Huang, Yin-Yi Yao, Tong-De Liu, Chao-Hao Chen, Hao-Ran Lin, Jun-Hong Xia. First identification of two co-existing genome-wide significant sex quantitative trait loci (QTL) in red tilapia using integrative QTL mapping. Zoological Research, 2022, 43(2): 205-216. doi: 10.24272/j.issn.2095-8137.2021.402
Citation: Zong-Xian Zhu, Yi-Long Lin, Chun-Hui Ai, Ying-Ying Xiong, Dan-Dan Huang, Yin-Yi Yao, Tong-De Liu, Chao-Hao Chen, Hao-Ran Lin, Jun-Hong Xia. First identification of two co-existing genome-wide significant sex quantitative trait loci (QTL) in red tilapia using integrative QTL mapping. Zoological Research, 2022, 43(2): 205-216. doi: 10.24272/j.issn.2095-8137.2021.402

First identification of two co-existing genome-wide significant sex quantitative trait loci (QTL) in red tilapia using integrative QTL mapping

doi: 10.24272/j.issn.2095-8137.2021.402
Funds:  This work was supported by the Guangdong Provincial Key R&D Program (2021B0202020001), Independent Research and Development Projects of Maoming Laboratory (2021ZZ007), National Natural Science Foundation of China (32072970), and Special Science and Technology Program of Maoming, Guangdong, China (2019S002004)
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  • Corresponding author: E-mail: xiajunh3@mail.sysu.edu.cn
  • Received Date: 2022-01-05
  • Accepted Date: 2022-01-21
  • Published Online: 2022-01-25
  • Publish Date: 2022-03-18
  • Red tilapia (Oreochromis spp.) is one of the most popular fish in China due to its bright red appearance, fast growth rate, and strong adaptability. Understanding the sex determination mechanisms is of vital importance for the selection of all-male lines to increase aquacultural production of red tilapia. In this research, the genetic architecture for sex from four mapping populations (n=1 090) of red tilapia was analyzed by quantitative trait loci (QTL)-seq, linkage-based QTL mapping, and linkage disequilibrium (LD)-based genome-wide association studies. Two genome-wide significant QTL intervals associated with sex were identified on ChrLG1 (22.4–23.9 Mb) and ChrLG23 (32.0–35.9 Mb), respectively. The QTL on ChrLG1 was detected in family 1 (FAM1), FAM2, and FAM4, and the other QTL on ChrLG23 was detected in FAM3 and FAM4. Four microsatellite markers located within the QTL were successfully developed for marker-assisted selection. Interestingly, three (lpp, sox14, and amh) of the 12 candidate genes located near or on the two QTL intervals were abundantly expressed in males, while the remaining genes were more highly expressed in females. Seven genes (scly, ube3a, lpp, gpr17, oca2, cog4, and atp10a) were significantly differentially expressed between the male and female groups. Furthermore, LD block analysis suggested that a cluster of genes on ChrLG23 may participate in regulating sex development in red tilapia. Our study provides important information on the genetic architecture of sex in red tilapia and should facilitate further exploration of sex determination mechanisms in this species.
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  • [1]
    Alqudah AM, Sallam A, Baenziger PS, Börner A. 2020. GWAS: fast-forwarding gene identification and characterization in temperate Cereals: lessons from barley - a review. Journal of Advanced Research, 22: 119−135. doi: 10.1016/j.jare.2019.10.013
    Bachtrog D, Mank JE, Peichel CL, Kirkpatrick M, Otto SP, Ashman TL, et al. 2014. Sex determination: why so many ways of doing it?. PLoS Biology, 12(7): e1001899. doi: 10.1371/journal.pbio.1001899
    Barría A, Trịnh TQ, Mahmuddin M, Peñaloza C, Papadopoulou A, Gervais O, et al. 2021. A major quantitative trait locus affecting resistance to Tilapia lake virus in farmed Nile tilapia (Oreochromis niloticus). Heredity, 127(3): 334−343. doi: 10.1038/s41437-021-00447-4
    Carmina E, Azziz R. 2006. Diagnosis, phenotype, and prevalence of polycystic ovary syndrome. Fertility and Sterility, 86(Suppl 1): S7–S8.
    Catoe HW, Nawaz Z. 2011. E6-AP facilitates efficient transcription at estrogen responsive promoters through recruitment of chromatin modifiers. Steroids, 76(9): 897−902.
    Cnaani A, Lee BY, Zilberman N, Ozouf-Costaz C, Hulata G, Ron M, et al. 2008. Genetics of sex determination in tilapiine species. Sexual Development, 2(1): 43−54. doi: 10.1159/000117718
    Cnaani A, Zilberman N, Tinman S, Hulata G, Ron M. 2004. Genome-scan analysis for quantitative trait loci in an F2 tilapia hybrid. Molecular Genetics and Genomics, 272(2): 162−172. doi: 10.1007/s00438-004-1045-1
    Conte MA, Joshi R, Moore EC, Nandamuri SP, Gammerdinger WJ, Roberts RB, et al. 2019. Chromosome-scale assemblies reveal the structural evolution of african cichlid genomes. Gigascience, 8(4): giz030.
    Courtois B, Audebert A, Dardou A, Roques S, Ghneim-Herrera T, Droc G, et al. 2013. Genome-wide association mapping of root traits in a japonica rice panel. PLoS One, 8(11): e78037. doi: 10.1371/journal.pone.0078037
    Dai SF, Qi SS, Wei XY, Liu XY, Li YB, Zhou X, et al. 2021. Germline sexual fate is determined by the antagonistic action of dmrt1 and foxl3/foxl2 in tilapia. Development, 148(8): dev199380. doi: 10.1242/dev.199380
    Devlin B, Roeder K, Wasserman L. 2003. Analysis of multilocus models of association. Genetic Epidemiology, 25(1): 36−47. doi: 10.1002/gepi.10237
    Dong SS, He WM, Ji JJ, Zhang C, Guo Y, Yang TL. 2021. LDBlockShow: a fast and convenient tool for visualizing linkage disequilibrium and haplotype blocks based on variant call format files. Briefings in Bioinformatics, 22(4): bbaa227. doi: 10.1093/bib/bbaa227
    Eshel O, Shirak A, Weller JI, Hulata G, Ron M. 2012. Linkage and physical mapping of sex region on LG23 of Nile tilapia (Oreochromis niloticus). G3 Genes| Genomes| Genetics, 2(1): 35−42.
    Ezaz MT, Harvey SC, Boonphakdee C, Teale AJ, McAndrew BJ, Penman DJ. 2004. Isolation and physical mapping of sex-linked AFLP markers in Nile tilapia (Oreochromis niloticus L. ). Marine Biotechnology, 6(5): 435−445. doi: 10.1007/s10126-004-3004-6
    FAO. 2020. The State of World Fisheries and Aquaculture 2020. Sustainability in Action. Editon. Rome.
    Feller AF, Ogi V, Seehausen O, Meier JI. 2021. Identification of a novel sex determining chromosome in cichlid fishes that acts as XY or ZW in different lineages. Hydrobiologia, 848(16): 3727−3745. doi: 10.1007/s10750-021-04560-7
    Gammerdinger WJ, Conte MA, Baroiller JF, D'Cotta H, Kocher TD. 2016. Comparative analysis of a sex chromosome from the blackchin tilapia. Sarotherodon melanotheron. BMC Genomics, 17: 808. doi: 10.1186/s12864-016-3163-7
    Geffroy B, Besson M, Sánchez-Baizán N, Clota F, Goikoetxea A, Sadoul B, et al. 2021. Unraveling the genotype by environment interaction in a thermosensitive fish with a polygenic sex determination system. Proceedings of the National Academy of Sciences of the United States of America, 118(50): e2112660118. doi: 10.1073/pnas.2112660118
    Guffanti G, Lievers LS, Bonati MT, Marchi M, Geronazzo L, Nardocci N, et al. 2011. Role of UBE3A and ATP10A genes in autism susceptibility region 15q11-q13 in an italian population: a positive replication for UBE3A. Psychiatry Research, 185(1-2): 33−38. doi: 10.1016/j.psychres.2010.04.057
    Hattori T, Kishino T, Stephen S, Eberspaecher H, Maki S, Takigawa M, et al. 2013. E6-AP/UBE3A protein acts as a ubiquitin ligase toward SOX9 protein. Journal of Biological Chemistry, 288(49): 35138−35148. doi: 10.1074/jbc.M113.486795
    Hogart A, Patzel KA, LaSalle JM. 2008. Gender influences monoallelic expression of ATP10A in human brain. Human Genetics, 124(3): 235−242. doi: 10.1007/s00439-008-0546-0
    Jiang DL, Gu XH, Li BJ, Zhu ZX, Qin H, Meng ZN, et al. 2019. Identifying a long QTL cluster across chrLG18 associated with salt tolerance in tilapia using GWAS and QTL-seq. Marine Biotechnology, 21(2): 250−261. doi: 10.1007/s10126-019-09877-y
    Jie MM, Ma H, Zhou L, Wu JH, Li MH, Liu XY, et al. 2020. Regulation of female folliculogenesis by Tsp1a in Nile tilapia (Oreochromis niloticus). International Journal of Molecular Sciences, 21(16): 5893. doi: 10.3390/ijms21165893
    Kofler R, Pandey RV, Schlötterer C. 2011. PoPoolation2: identifying differentiation between populations using sequencing of pooled DNA samples (pool-seq). Bioinformatics, 27(24): 3435−3436. doi: 10.1093/bioinformatics/btr589
    Koyavski L, Panov J, Simchi L, Rayi PR, Sharvit L, Feuermann Y, et al. 2019. Sex-dependent sensory phenotypes and related transcriptomic expression profiles are differentially affected by angelman syndrome. Molecular Neurobiology, 56(9): 5998−6016. doi: 10.1007/s12035-019-1503-8
    Langmead B, Salzberg SL. 2012. Fast gapped-read alignment with Bowtie 2. Nature Methods, 9(4): 357−359. doi: 10.1038/nmeth.1923
    Leamy LJ, Zhang HY, Li CB, Chen CY, Song BH. 2017. A genome-wide association study of seed composition traits in wild soybean (Glycine soja). BMC Genomics, 18: 18. doi: 10.1186/s12864-016-3397-4
    Lee BY, Hulata G, Kocher TD. 2004. Two unlinked loci controlling the sex of blue tilapia (Oreochromis aureus). Heredity, 92(6): 543−549. doi: 10.1038/sj.hdy.6800453
    Lee BY, Lee WJ, Streelman JT, Carleton KL, Howe AE, Hulata G, et al. 2005. A second-generation genetic linkage map of tilapia (Oreochromis spp. ). Genetics, 170(1): 237−244. doi: 10.1534/genetics.104.035022
    Li BJ, Zhu ZX, Gu XH, Lin HR, Xia JH. 2019. Qtl mapping for red blotches in malaysia red tilapia (Oreochromis spp. ). Marine Biotechnology, 21(3): 384−395. doi: 10.1007/s10126-019-09888-9
    Li H, Handsaker B, Wysoker A, Fennell T, Ruan J, Homer N, et al. 2009. The sequence alignment/map format and SAMtools. Bioinformatics, 25(16): 2078−2079. doi: 10.1093/bioinformatics/btp352
    Li MH, Sun YL, Zhao JE, Shi HJ, Zeng S, Ye K, et al. 2015. A tandem duplicate of anti-mullerian hormone with a missense SNP on the Y chromosome is essential for male sex determination in Nile tilapia. Oreochromis niloticus. PLoS Genetics, 11(11): e1005678. doi: 10.1371/journal.pgen.1005678
    Li MH, Yang HH, Li MR, Sun YL, Jiang XL, Xie QP, et al. 2013. Antagonistic roles of Dmrt1 and Foxl2 in sex differentiation via estrogen production in tilapia as demonstrated by TALENs. Endocrinology, 154(12): 4814−4825. doi: 10.1210/en.2013-1451
    Li XY, Gui JF. 2018. Diverse and variable sex determination mechanisms in vertebrates. Science China Life Sciences, 61(12): 1503−1514. doi: 10.1007/s11427-018-9415-7
    Lin QH, Mei J, Li Z, Zhang XM, Zhou L, Gui JF. 2017. Distinct and cooperative roles of amh and dmrt1 in self-renewal and differentiation of male germ cells in zebrafish. Genetics, 207(3): 1007−1022. doi: 10.1534/genetics.117.300274
    Liu F, Sun F, Li J, Xia JH, Lin G, Tu RJ, et al. 2013. A microsatellite-based linkage map of salt tolerant tilapia (Oreochromis mossambicus x Oreochromis spp. ) and mapping of sex-determining loci. BMC Genomics, 14: 58. doi: 10.1186/1471-2164-14-58
    Mair GC, Scott AG, Penman DJ, Beardmore JA, Skibinski DOF. 1991a. Sex determination in the genus oreochromis: 1. Sex reversal, gynogenesis and triploidy in O. Niloticus (L. ). Theoretical and Applied Genetics, 82(2): 144−152. doi: 10.1007/BF00226205
    Mair GC, Scott AG, Penman DJ, Skibinski DOF, Beardmore JA. 1991b. Sex determination in the genus Oreochromis: 2. Sex reversal, hybridisation, gynogenesis and triploidy in O. Aureus steindachner. Theoretical and Applied Genetics, 82(2): 153−160. doi: 10.1007/BF00226206
    Martinez-Cadenas C, Peña-Chilet M, Ibarrola-Villava M, Ribas G. 2013. Gender is a major factor explaining discrepancies in eye colour prediction based on HERC2/OCA2 genotype and the IrisPlex model. Forensic Science International:Genetics, 7(4): 453−460. doi: 10.1016/j.fsigen.2013.03.007
    Matsuda M, Nagahama Y, Shinomiya A, Sato T, Matsuda C, Kobayashi T, et al. 2002. DMY is a Y-specific DM-domain gene required for male development in the medaka fish. Nature, 417(6888): 559−563. doi: 10.1038/nature751
    Menozzi P, Piazza A, Cavalli-Sforza L. 1978. Synthetic maps of human gene frequencies in Europeans: these maps indicate that early farmers of the Near East spread to all of Europe in the Neolithic. Science, 201(4358): 786−792. doi: 10.1126/science.356262
    Myosho T, Otake H, Masuyama H, Matsuda M, Kuroki Y, Fujiyama A, et al. 2012. Tracing the emergence of a novel sex-determining gene in medaka. Oryzias luzonensis. Genetics, 191(1): 163−170.
    Nagahama Y, Chakraborty T, Paul-Prasanth B, Ohta K, Nakamura M. 2021. Sex determination, gonadal sex differentiation, and plasticity in vertebrate species. Physiological Reviews, 101(3): 1237−1308. doi: 10.1152/physrev.00044.2019
    Nakamura M. 2009. Sex determination in amphibians. Seminars in Cell & Developmental Biology, 20(3): 271−282.
    Nyinondi CS, Mtolera MSP, Mmochi AJ, Pinto FAL, Houston RD, de Koning DJ, et al. 2020. Assessing the genetic diversity of farmed and wild Rufiji tilapia (Oreochromis urolepis urolepis) populations using ddRAD sequencing. Ecology and Evolution, 10(18): 10044−10056. doi: 10.1002/ece3.6664
    Ogawa-Wong AN, Hashimoto AC, Ha H, Pitts MW, Seale LA, Berry MJ. 2018. Sexual dimorphism in the selenocysteine lyase knockout mouse. Nutrients, 10(2): 159. doi: 10.3390/nu10020159
    Palaiokostas C, Bekaert M, Khan MGQ, Taggart JB, Gharbi K, McAndrew BJ, et al. 2013. Mapping and validation of the major sex-determining region in Nile tilapia (Oreochromis niloticus L. ) using RAD sequencing. PLoS One, 8(7): e68389. doi: 10.1371/journal.pone.0068389
    Palaiokostas C, Bekaert M, Khan MGQ, Taggart JB, Gharbi K, McAndrew BJ, et al. 2015. A novel sex-determining QTL in Nile tilapia (Oreochromis niloticus). BMC Genomics, 16(1): 171. doi: 10.1186/s12864-015-1383-x
    Peterson BK, Weber JN, Kay EH, Fisher HS, Hoekstra HE. 2012. Double digest RADseq: an inexpensive method for De novo SNP discovery and genotyping in model and non-model species. PLoS One, 7(5): e37135. doi: 10.1371/journal.pone.0037135
    Pradeep PJ, Srijaya TC, Hassan A, Chatterji AK, Withyachumnarnkul B, Jeffs A. 2014. Optimal conditions for cold-shock induction of triploidy in red tilapia. Aquaculture International, 22(3): 1163−1174. doi: 10.1007/s10499-013-9736-4
    Rajendiran P, Jaafar F, Kar S, Sudhakumari C, Senthilkumaran B, Parhar IS. 2021. Sex determination and differentiation in teleost: roles of genetics, environment, and Brain. Biology, 10(10): 973. doi: 10.3390/biology10100973
    Renn SCP, Hurd PL. 2021. Epigenetic regulation and environmental sex determination in cichlid fishes. Sexual Development, 15(1-3): 93−107. doi: 10.1159/000517197
    Rochette NC, Rivera-Colón AG, Catchen JM. 2019. Stacks 2: analytical methods for paired-end sequencing improve RADseq-based population genomics. Molecular Ecology, 28(21): 4737−4754. doi: 10.1111/mec.15253
    Sandeep M, Sun F, Liu F, Li J, David PB, Yue GH. 2012. Novel polymorphic microsatellites from Florida red tilapia and cross-species amplification in Mozambique and Nile tilapia. Journal of Genetics, 91(3): e97−e99.
    Sarre SD, Ezaz T, Georges A. 2011. Transitions between sex-determining systems in reptiles and amphibians. Annual Review of Genomics and Human Genetics, 12: 391−406. doi: 10.1146/annurev-genom-082410-101518
    Sassi FDMC, Deon GA, Moreira-Filho O, Vicari MR, Bertollo LAC, Liehr T, et al. 2020. Multiple sex chromosomes and evolutionary relationships in amazonian catfishes: the outstanding model of the genus Harttia (Siluriformes: Loricariidae). Genes, 11(10): 1179. doi: 10.3390/genes11101179
    Tao WJ, Xu LH, Zhao L, Zhu ZX, Wu X, Min QW, et al. 2021. High-quality chromosome-level genomes of two tilapia species reveal their evolution of repeat sequences and sex chromosomes. Molecular Ecology Resources, 21(2): 543−560. doi: 10.1111/1755-0998.13273
    Taslima K, Wehner S, Taggart JB, de Verdal H, Benzie JAH, Bekaert M, et al. 2020. Sex determination in the GIFT strain of tilapia is controlled by a locus in linkage group 23. BMC Genetics, 21(1): 49. doi: 10.1186/s12863-020-00853-3
    Toyota K, Miyakawa H, Hiruta C, Sato T, Katayama H, Ohira T, et al. 2021. Sex determination and differentiation in decapod and cladoceran crustaceans: an overview of endocrine regulation. Genes, 12(2): 305. doi: 10.3390/genes12020305
    Triay C, Conte MA, Baroiller JF, Bezault E, Clark FE, Penman DJ, et al. 2020. Structure and sequence of the sex determining locus in two wild populations of Nile tilapia. Genes, 11(9): 1017. doi: 10.3390/genes11091017
    van Ooijen JW. 2011. Multipoint maximum likelihood mapping in a full-sib family of an outbreeding species. Genetics Research, 93(5): 343−349. doi: 10.1017/S0016672311000279
    Wang HY, Misztal I, Aguilar I, Legarra A, Fernando RL, Vitezica Z, et al. 2014. Genome-wide association mapping including phenotypes from relatives without genotypes in a single-step (ssGWAS) for 6-week body weight in broiler chickens. Frontiers in Genetics, 5: 134.
    Webster KA, Schach U, Ordaz A, Steinfeld JS, Draper BW, Siegfried KR. 2017. Dmrt1 is necessary for male sexual development in zebrafish. Developmental Biology, 422(1): 33−46. doi: 10.1016/j.ydbio.2016.12.008
    Wessels S, Krause I, Floren C, Schütz E, Beck J, Knorr C. 2017. ddRADseq reveals determinants for temperature-dependent sex reversal in Nile tilapia on LG23. BMC Genomics, 18(1): 531. doi: 10.1186/s12864-017-3930-0
    Xia JH, Bai ZY, Meng ZN, Zhang Y, Wang L, Liu F, et al. 2015. Signatures of selection in tilapia revealed by whole genome resequencing. Scientific Reports, 5: 14168. doi: 10.1038/srep14168
    Xue LZ, Gao Y, Wu MY, Tian T, Fan HP, Huang YJ, et al. 2021. Telomere-to-telomere assembly of a fish Y chromosome reveals the origin of a young sex chromosome pair. Genome Biology, 22(1): 203. doi: 10.1186/s13059-021-02430-y
    Yang Q, Cui J, Chazaro I, Cupples LA, Demissie S. 2005. Power and type I error rate of false discovery rate approaches in genome-wide association studies. BMC Genetics, 6 Suppl 1 (Suppl 1): S134.
    Yoshida GM, Yáñez JM. 2021. Multi-trait GWAS using imputed high-density genotypes from whole-genome sequencing identifies genes associated with body traits in Nile tilapia. BMC Genomics, 22(1): 57. doi: 10.1186/s12864-020-07341-z
    Zhang B, Zhao H, Li T, Gao X, Gao Q, Tang R, et al. 2012. Association study of gene LPP in women with polycystic ovary syndrome. PLoS One, 7(10): e46370. doi: 10.1371/journal.pone.0046370
    Zhang L, Liu JS, Zhao FP, Ren HX, Xu LY, Lu J, et al. 2013. Genome-wide association studies for growth and meat production traits in sheep. PLoS One, 8(6): e66569. doi: 10.1371/journal.pone.0066569
    Zhang XB, Li MR, Ma H, Liu XY, Shi HJ, Li MH, et al. 2017. Mutation of foxl2 or cyp19a1a results in female to male sex reversal in XX Nile tilapia. Endocrinology, 158(8): 2634–2647.
    Zhu ZX, Lin YL, Qin H, Xiong YY, Jiang DL, Lin HR, et al. 2021. Identifying a genome-wide QTL interval controlling for ammonia-nitrogen tolerance on chrLG1 of Nile tilapia. Aquaculture, 543: 736946.
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