A Tandem Duplicate of Anti-Müllerian Hormone with a Missense SNP on the Y Chromosome Is Essential for Male Sex Determination in Nile Tilapia, Oreochromis niloticus

PLoS Genetics - Tập 11 Số 11 - Trang e1005678
Minghui Li1, Yun-Lv Sun1, Jiue Zhao1, Hongjuan Shi1, Sheng Zeng1, Kai Ye1, Dongneng Jiang1, Linyan Zhou1, Lina Sun1, Wenjing Tao1, Yoshitaka Nagahama2,3, Thomas D. Kocher4, Deshou Wang1
1Key Laboratory of Freshwater Fish Reproduction and Development (Ministry of Education), Key Laboratory of Aquatic Science of Chongqing, School of Life Science, Southwest University, Chongqing, China
2Solution-Oriented Research for Science and Technology (SORST), Laboratory of Reproductive Biology, National Institute for Basic Biology, Okazaki, Japan
3South Ehime Fisheries Research Center, Ehime University, Matsuyama, Japan
4Department of Biology, University of Maryland, College Park, Maryland, United States of America

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Tài liệu tham khảo

AH Sinclair, 1990, A gene from the human sex-determining region encodes a protein with homology to a conserved DNA-binding motif, Nature, 346, 240, 10.1038/346240a0

P Koopman, 1991, Male development of chromosomally female mice transgenic for Sry, Nature, 351, 117, 10.1038/351117a0

Y Takehana, 2014, Co-option of Sox3 as the male-determining factor on the Y chromosome in the fish <italic>Oryzias dancena</italic>, Nat Commun, 5, 4157, 10.1038/ncomms5157

CA Smith, 2009, The avian Z-linked gene DMRT1 is required for male sex determination in the chicken, Nature, 461, 267, 10.1038/nature08298

S Chen, 2014, Whole-genome sequence of a flatfish provides insights into ZW sex chromosome evolution and adaptation to a benthic lifestyle, Nat Genet, 46, 253, 10.1038/ng.2890

S Yoshimoto, 2008, A W-linked DM-domain gene, DM-W, participates in primary ovary development in Xenopus laevis, Proc Natl Acad Sci USA, 105, 2469, 10.1073/pnas.0712244105

M Matsuda, 2002, DMY is a Y-specific DM-domain gene required for male development in the medaka fish, Nature, 417, 559, 10.1038/nature751

I Nanda, 2002, A duplicated copy of DMRT1 in the sex-determining region of the Y chromosome of the medaka, <italic>Oryzias latipes</italic>, Proc Natl Acad Sci USA, 99, 11778, 10.1073/pnas.182314699

L Boulanger, 2014, FOXL2 is a female sex-determining gene in the goat, Curr Biol, 24, 404, 10.1016/j.cub.2013.12.039

A Yano, 2012, An immune-related gene evolved into the master sex-determining gene in rainbow trout, <italic>Oncorhynchus mykiss</italic>, Curr Biol, 22, 1423, 10.1016/j.cub.2012.05.045

RS Hattori, 2012, A Y-linked anti-Müllerian hormone duplication takes over a critical role in sex determination, Proc Natl Acad Sci USA, 109, 2955, 10.1073/pnas.1018392109

T Kamiya, 2012, A trans-species missense SNP in Amhr2 is associated with sex determination in the tiger pufferfish, <italic>Takifugu rubripes</italic> (fugu), PLoS Genet, 8, e1002798, 10.1371/journal.pgen.1002798

T Myosho, 2012, Tracing the emergence of a novel sex-determining gene in medaka, <italic>Oryzias luzonensis</italic>, Genetics, 191, 163, 10.1534/genetics.111.137497

JE Mank, 2009, Evolutionary diversity and turn-over of sex determination in teleost fishes, Sex Dev, 3, 60, 10.1159/000223071

JA Ross, 2009, Turnover of sex chromosomes in the stickleback fishes (<italic>gasterosteidae</italic>), PLoS Genet, 5, e1000391, 10.1371/journal.pgen.1000391

KM Bradley, 2011, An SNP-Based Linkage Map for Zebrafish Reveals Sex Determination Loci, G3 (Bethesda), 1, 3, 10.1534/g3.111.000190

CA Wilson, 2014, Wild sex in zebrafish: loss of the natural sex determinant in domesticated strains, Genetics, 198, 1291, 10.1534/genetics.114.169284

GC Mair, 1991, Sex determination in the genus <italic>Oreochromis</italic>: 1. Sex reversal, gynogenesis and triploidy in o. niloticus (L.), Theor Appl Genet, 82, 144, 10.1007/BF00226205

JF Baroiller, 2009, Tilapia sex determination: Where temperature and genetics meet, Comp Biochem Physiol A Mol Integr Physiol, 153, 30, 10.1016/j.cbpa.2008.11.018

BY Lee, 2003, Identification of a sex-determining region in Nile tilapia (<italic>Oreochromis niloticus</italic>) using bulked segregant analysis, Anim Genet, 34, 379, 10.1046/j.1365-2052.2003.01035.x

O Eshel, 2011, Fine-mapping of a locus on linkage group 23 for sex determination in Nile tilapia (<italic>Oreochromis niloticus</italic>), Anim Genet, 42, 222, 10.1111/j.1365-2052.2010.02128.x

YL Sun, 2014, Screening and characterization of sex-linked DNA markers and marker-assisted selection in the Nile tilapia (<italic>Oreochromis niloticus</italic>), Aquaculture, 433, 19, 10.1016/j.aquaculture.2014.05.035

O Eshel, 2014, Identification of male-specific amh duplication, sexually differentially expressed genes and microRNAs at early embryonic development of Nile tilapia (<italic>Oreochromis niloticus</italic>), BMC Genomics, 15, 774, 10.1186/1471-2164-15-774

O Eshel, 2012, Linkage and Physical Mapping of Sex Region on LG23 of Nile Tilapia (<italic>Oreochromis niloticus</italic>), G3, 2, 35, 10.1534/g3.111.001545

N Josso, 2001, Anti-Müllerian hormone and its receptors, Mol Cell Endocrinol, 179, 25, 10.1016/S0303-7207(01)00467-1

T Miura, 2002, Spermatogenesis-preventing substance in Japanese eel, Development, 129, 2689, 10.1242/dev.129.11.2689

N Yoshinaga, 2004, Sexually dimorphic expression of a teleost homologue of Müllerian inhibiting substance during gonadal sex differentiation in Japanese flounder, <italic>Paralichthys olivaceus</italic>, Biochem Biophys Res Commun, 322, 508, 10.1016/j.bbrc.2004.07.162

GC Wu, 2010, The expression of amh and amhr2 is associated with the development of gonadal tissue and sex change in the protandrous black porgy, <italic>Acanthopagrus schlegeli</italic>, Biol Reprod, 83, 443, 10.1095/biolreprod.110.084681

C Morinaga, 2007, The hotei mutation of medaka in the anti-Müllerian hormone receptor causes the dysregulation of germ cell and sexual development, Proc Natl Acad Sci USA, 104, 9691, 10.1073/pnas.0611379104

MH Li, 2011, Construction of microarray fosmid library and its application in gene isolation in Nile tilapia, <italic>Oreochromis niloticus</italic> [in Chinese], Journal of Fisheries of China, 35, 28

D Brawand, 2014, The genomic substrate for adaptive radiation in African cichlid fish, Nature, 513, 375, 10.1038/nature13726

W Tao, 2013, Characterization of gonadal transcriptomes from Nile tilapia (<italic>Oreochromis niloticus</italic>) reveals differentially expressed genes, PLoS One, 8, e63604, 10.1371/journal.pone.0063604

MH Li, 2013, Antagonistic roles of Dmrt1 and Foxl2 in sex differentiation via estrogen production in tilapia as demonstrated by TALENs, Endocrinology, 154, 4814, 10.1210/en.2013-1451

M Li, 2014, Efficient and Heritable Gene Targeting in Tilapia by CRISPR/Cas9, Genetics, 197, 591, 10.1534/genetics.114.163667

MT Ezaz, 2004, Isolation and physical mapping of sex-linked AFLP markers in Nile tilapia (<italic>Oreochromis niloticus</italic> L.), Mar Biotechnol, 6, 435, 10.1007/s10126-004-3004-6

A Cnaani, 2008, Sex-linked markers and microsatellite locus duplication in the cichlid species Oreochromis tanganicae, Biol Lett, 4, 700, 10.1098/rsbl.2008.0286

WJ Gammerdinger, 2014, Structure and decay of a proto-Y region in Tilapia, <italic>Oreochromis niloticus</italic>, BMC Genomics, 15, 975, 10.1186/1471-2164-15-975

S Ijiri, 2008, Sexual dimorphic expression of genes in gonads during early differentiation of a teleost fish, the Nile tilapia <italic>Oreochromis niloticus</italic>, Biol Reprod, 78, 333, 10.1095/biolreprod.107.064246

M Matsuda, 2007, DMY gene induces male development in genetically female (XX) medaka fish, Proc Natl Acad Sci USA, 104, 3865, 10.1073/pnas.0611707104

S Wessels, 2014, Allelic variant in the anti-Müllerian hormone gene leads to autosomal and temperature-dependent sex reversal in a selected Nile tilapia line, PLoS One, 9, e104795, 10.1371/journal.pone.0104795

A Böhne, 2014, Comparative transcriptomics in East African cichlids reveals sex and specied specific expression and new candidated for sex differentiation in fishes, Genome Biol Evol, 6, 2567, 10.1093/gbe/evu200

AD Cutting, 2014, Identification, expression, and regulation of anti-Müllerian hormone type-II receptor in the embryonic chicken gonad, Biol Reprod, 90, 106, 10.1095/biolreprod.113.116491

R Horiguchi, 2013, Characterization of gonadal soma-derived factor expression during sex change in the protogynous wrasse, <italic>Halichoeres trimaculatus</italic>, Dev Dyn, 242, 388, 10.1002/dvdy.23929

DS Wang, 2007, Foxl2 up-regulates aromatase gene transcription in a female-specific manner by binding to the promoter as well as interacting with ad4 binding protein/steroidogenic factor 1, Mol Endocrinol, 21, 712, 10.1210/me.2006-0248

Y Guiguen, 2010, Ovarian aromatase and estrogens: a pivotal role for gonadal sex differentiation and sex change in fish, Gen Comp Endocrinol, 165, 352, 10.1016/j.ygcen.2009.03.002

E Okada, 2009, Xenopus W-linked DM-W induces Foxl2 and Cyp19 expression during ovary formation, Sex Dev, 3, 38, 10.1159/000200080

Y Matsumoto, 2013, Epigenetic control of gonadal aromatase (cyp19a1) in temperature-dependent sex determination of red-eared slider turtles, PLoS One, 8, e63599, 10.1371/journal.pone.0063599

LS Lambeth, 2013, Overexpression of aromatase alone is sufficient for ovarian development in genetically male chicken embryos, PLoS One, 8, e68362, 10.1371/journal.pone.0068362

D Coveney, 2001, Estrogen-induced gonadal sex reversal in the tammar wallaby, Biol Reprod, 65, 613, 10.1095/biolreprod65.2.613

D Scheib, 1983, Effects and role of estrogens in avian gonadal differentiation, Differentiation, 23, S87

H Merchant-Larios, 1997, Correlation among thermo sensitive period, estradiol response, and gonad differentiation in the sea turtle <italic>Lepidochelys olivacea</italic>, Gen Comp Endocrinol, 107, 373, 10.1006/gcen.1997.6946

F Piferrer, 2001, Endocrine sex control strategies for the feminization of teleost fish, Aquaculture, 197, 229, 10.1016/S0044-8486(01)00589-0

T Kobayashi, 2003, Induction of XY sex reversal by estrogen involves altered gene expression in a teleost, tilapia, Cytogenet Genome Res, 101, 289, 10.1159/000074351

NH Uhlenhaut, 2009, Somatic sex reprogramming of adult ovaries to testes by FOXL2 ablation, Cell, 139, 1130, 10.1016/j.cell.2009.11.021

M Pannetier, 2006, FOXL2 activates P450 aromatase gene transcription: towards a better characterization of the early steps of mammalian ovarian development, J Mol Endocrino, 36, 399, 10.1677/jme.1.01947

NI Fleming, 2010, Aromatase is a direct target of FOXL2: C134W in granulosa cell tumors via a single highly conserved binding site in the ovarian specific promoter, PLoS One, 5, e14389, 10.1371/journal.pone.0014389

N di Clemente, 1992, A quantitative and interspecific test for biological activity of anti-müllerian hormone: the fetal ovary aromatase assay, Development, 114, 721, 10.1242/dev.114.3.721

H Nishikimi, 2000, Sex differentiation and mRNA expression of P450c17, P450arom and AMH in gonads of the chicken, Mol Reprod Dev, 55, 20, 10.1002/(SICI)1098-2795(200001)55:1<20::AID-MRD4>3.0.CO;2-E

L Cong, 2013, Multiplex genome engineering using CRISPR/Cas systems, Science, 339, 819, 10.1126/science.1231143