期刊论文详细信息
BMC Genetics
Genetics and timing of sex determination in the East African cichlid fish Astatotilapia burtoni
Astrid Böhne1  Walter Salzburger1  Carolin Göppert1  Corina Heule1 
[1] Zoological Institute, University of Basel, Vesalgasse 1, Basel, 4051, Switzerland
关键词: Gene expression profiles;    Speciation;    Adaptive radiation;    Cichlidae;    Sexual development;   
Others  :  1085019
DOI  :  10.1186/s12863-014-0140-5
 received in 2014-11-20, accepted in 2014-12-01,  发布年份 2014
【 摘 要 】

Background

The factors determining sex are diverse in vertebrates and especially so in teleost fishes. Only a handful of master sex-determining genes have been identified, however great efforts have been undertaken to characterize the subsequent genetic network of sex differentiation in various organisms. East African cichlids offer an ideal model system to study the complexity of sexual development, since many different sex-determining mechanisms occur in closely related species of this fish family. Here, we investigated the sex-determining system and gene expression profiles during male development of Astatotilapia burtoni, a member of the rapidly radiating and exceptionally species-rich haplochromine lineage.

Results

Crossing experiments with hormonally sex-reversed fish provided evidence for an XX-XY sex determination system in A. burtoni. Resultant all-male broods were used to assess gene expression patterns throughout development of a set of candidate genes, previously characterized in adult cichlids only.

Conclusions

We could identify the onset of gonad sexual differentiation at 11–12 dpf. The expression profiles identified wnt4B and wt1A as the earliest gonad markers in A. burtoni. Furthermore we identified late testis genes (cyp19a1A, gsdf, dmrt1 and gata4), and brain markers (ctnnb1A, ctnnb1B, dax1A, foxl2, foxl3, nanos1A, nanos1B, rspo1, sf-1, sox9A and sox9B).

【 授权许可】

   
2014 Heule et al.; licensee BioMed Central.

附件列表
Files Size Format View
Fig. 7. 62KB Image download
Figure 5 . 116KB Image download
Figure 4. 121KB Image download
Figure 3. 108KB Image download
Figure 2. 54KB Image download
Figure 1. 9KB Image download
【 图 表 】

Figure 1.

Figure 2.

Figure 3.

Figure 4.

Figure 5 .

Fig. 7.

【 参考文献 】
  • [1]Devlin RH, Nagahama Y: Sex determination and sex differentiation in fish: an overview of genetic, physiological, and environmental influences. Aquaculture 2002, 208(3):191-364.
  • [2]Cutting A, Chue J, Smith CA: Just how conserved is vertebrate sex determination? Dev Dyn 2013, 242(4):380-387.
  • [3]Matsuda M, Nagahama Y, Shinomiya A, Sato T, Matsuda C, Kobayashi T, Morrey CE, Shibata N, Asakawa S, Shimizu N, Hori H, Hamaguchi S, Sakaizuma M: DMY is a Y-specific DM-domain gene required for male development in the medaka fish. Nature 2002, 417:559-563.
  • [4]Nanda I, Kondo M, Hornung U, Asakawa S, Winkler C, Shimizu A, Shan Z, Haaf T, Shimizu N, Shima A, Schmid M, Schartl M: A duplicated copy of DMRT1 in the sex-determining region of the Y chromosome of the medaka, Oryzias latipes. Proc Natl Acad Sci U S A 2002, 99(18):11778-11783.
  • [5]Myosho T, Otake H, Masuyama H, Matsuda M, Kuroki Y, Fujiyama A, Naruse K, Hamaguchi S, Sakaizumi M: Tracing the emergence of a novel sex-determining gene in medaka Oryzias luzonensis. Genetics 2012, 191(1):163-170.
  • [6]Takehana Y, Matsuda M, Myosho T, Suster ML, Kawakami K, Shin-I T, Kohara Y, Kuroki Y, Toyoda A, Fujiyama A, Hamaguchi S, Sakaizumi M, Naruse K: Co-option of Sox3 as the male-determining factor on the Y chromosome in the fish Oryzias dancena. Nat Commun 2014, 5:4157.
  • [7]Hattori RS, Murai Y, Oura M, Masuda S, Majhi SK, Sakamoto T, Fernandino JI, Somoza GM, Yokota M, Strüssmann CA: A Y-linked anti-Müllerian hormone duplication takes over a critical role in sex determination. Proc Natl Acad Sci U S A 2012, 109(8):2955-2959.
  • [8]Kamiya T, Kai W, Tasumi S, Oka A, Matsunaga T, Mizuno N, Fujita M, Suetake H, Suzuki S, Hosoya S, Tohari S, Brenner S, Miyadi T, Venkatesh B, Suzuki Y, Kikuchi K: A trans-species missense SNP in amhr2 is associated with sex determination in the tiger pufferfish, Takifugu rubripes (Fugu). PLoS Genet 2012, 8(7):e1002798.
  • [9]Yano A, Guyomard R, Nicol B, Jouanno E, Quillet E, Klopp C, Cabau C, Bouchez O, Fostier A, Guiguen Y: An immune-related gene evolved into the master sex-determining gene in rainbow trout, Oncorhynchus mykiss. Curr Biol 2012, 22(15):1423-1428.
  • [10]Yano A, Nicol B, Jouanno E, Quillet E, Fostier A, Guyomard R, Guiguen Y: The sexually dimorphic on the Y-chromosome gene (sdY) is a conserved male-specific Y-chromosome sequence in many salmonids. Evol Appl 2013, 6(3):486-496.
  • [11]Böhne A, Heule C, Boileau N, Salzburger W: Expression and sequence evolution of aromatase cyp19a1 and other sexual development genes in East African cichlid fishes. Mol Biol Evol 2013, 30(10):2268-2285.
  • [12]Herpin A, Adolfi MC, Nicol B, Hinzmann M, Schmidt C, Klughammer J, Engel M, Tanaka M, Guiguen Y, Schartl M: Divergent expression regulation of gonad development genes in medaka shows incomplete conservation of the downstream regulatory network of vertebrate sex determination. Mol Biol Evol 2013, 30(10):2328-2346.
  • [13]Hornung U, Herpin A, Schartl M: Expression of the male determining gene dmrt1bY and its autosomal coorthologue dmrt1a in medaka. Sex Dev 2007, 1(3):197-206.
  • [14]Rossi P, Dolci S, Albanesi C, Grimaldi P, Geremia R: Direct evidence that the mouse sex-determining gene Sry is expressed in the somatic cells of male fetal gonads and in the germ cell line in the adult testis. Mol Reprod Dev 1993, 34(4):369-373.
  • [15]Turner ME, Martin C, Martins AS, Dunmire J, Farkas J, Ely DL, Milsted A: Genomic and expression analysis of multiple Sry loci from a single Rattus norvegicus Y chromosome. BMC Genet 2007, 8:11. BioMed Central Full Text
  • [16]Veith AM, Schafer M, Kluver N, Schmidt C, Schultheis C, Schartl M, Winkler C, Volff JN: Tissue-specific expression of dmrt genes in embryos and adults of the platyfish Xiphophorus maculatus. Zebrafish 2006, 3(3):325-337.
  • [17]Ijiri S, Kaneko H, Kobayashi T, Wang D-S, Sakai F, Paul-Prasanth B, Nakamura M, Nagahama Y: Sexual dimorphic expression of genes in gonads during early differentiation of a teleost fish, the Nile tilapia Oreochromis niloticus. Biol Reprod 2008, 78(2):333-341.
  • [18]Herpin A, Schartl M: Dmrt1 genes at the crossroads: a widespread and central class of sexual development factors in fish. FEBS J 2011, 278(7):1010-1019.
  • [19]Lange IG, Hartel A, Meyer HHD: Evolution of oestrogen functions in vertebrates. J Steroid Biochem Mol Biol 2002, 83(1–5):219-226.
  • [20]Nakamura M: The mechanism of sex determination in vertebrates - are sex steroids the key-factor? J Exp Zool A Ecol Genet Physiol 2010, 313(7):381-398.
  • [21]Angelopoulou R, Lavranos G, Manolakou P: Sex determination strategies in 2012: towards a common regulatory model? Reprod Biol Endocrinol 2012, 10(1):13. BioMed Central Full Text
  • [22]Morohashi K, Baba T, Tanaka M: Steroid hormones and the development of reproductive organs. Sex Dev 2013, 7(1–3):61-79.
  • [23]Heule C, Salzburger W, Böhne A: Genetics of sexual development – an evolutionary playground for fish. Genetics 2014, 196(3):579-591.
  • [24]Salzburger W: The interaction of sexually and naturally selected traits in the adaptive radiations of cichlid fishes. Mol Ecol 2009, 18:169-185.
  • [25]Kocher TD: Adaptive evolution and explosive speciation: the cichlid fish model. Nat Rev Genet 2004, 5(4):288-298.
  • [26]Santos ME, Salzburger W: How cichlids diversify. Science 2012, 338(6107):619-621.
  • [27]Salzburger W, Van Bocxlaer B, Cohen AS: The ecology and and evolution of the African Great Lakes and their faunas. Annu Rev Ecol Evol Syst 2014, 5:19-45.
  • [28]Baroiller JF, D’Cotta H, Saillant E: Environmental effects on fish sex determination and differentiation. Sex Dev 2009, 3(2–3):118-135.
  • [29]Reddon AR, Hurd PL: Water pH during early development influences sex ratio and male morph in a West African cichlid fish, Pelvicachromis pulcher. Zoology (Jena) 2013, 116(3):139-143.
  • [30]Roberts RB, Ser JR, Kocher TD: Sexual conflict resolved by invasion of a novel sex determiner in Lake Malawi cichlid fishes. Science 2009, 326(5955):998-1001.
  • [31]Ser JR, Roberts RB, Kocher TD: Multiple interacting loci control sex determination in lake Malawi cichlid fish. Evolution 2010, 64(2):486-501.
  • [32]Parnell NF, Streelman JT: Genetic interactions controlling sex and color establish the potential for sexual conflict in Lake Malawi cichlid fishes. Heredity 2013, 110(3):239-246.
  • [33]Wirtz Ocana S, Meidl P, Bonfils D, Taborsky M: Y-linked Mendelian inheritance of giant and dwarf male morphs in shell-brooding cichlids. 2014, Proc Biol Sci281(1794): 20140253.
  • [34]Baroiller JF, D'Cotta H, Bezault E, Wessels S, Hoerstgen-Schwark G: Tilapia sex determination: Where temperature and genetics meet. Comp Biochem Physiol A Mol Integr Physiol 2009, 153(1):30-38.
  • [35]Theis A, Salzburger W, Egger B: The function of anal fin egg-spots in the cichlid fish Astatotilapia burtoni. PLoS One 2012, 7(1):e29878.
  • [36]Fujimura K, Okada N: Development of the embryo, larva and early juvenile of Nile tilapia Oreochromis niloticus (Pisces: Cichlidae). Dev Staging Sys Dev Growth Differ 2007, 49(4):301-324.
  • [37]Juntti SA, Hu CK, Fernald RD: Tol2-mediated generation of a transgenic haplochromine cichlid. Astatotilapia burtoni. PLoS One 2013, 8(10):e77647.
  • [38]Al Hafedh YS, Siddiqui AQ, Al-Saiady MY: Effects of dietary protein levels on gonad maturation, size and age at first maturity, fecundity and growth of Nile tilapia. Aquac Int 1999, 7(5):319-332.
  • [39]Brawand D, Wagner CE, Li YI, Malinsky M, Keller I, Fan S, Simakov O, Ng AY, Lim ZW, Bezault E, Turner-Maier J, Johnson J, Alcazar R, Noh HJ, Russel P, Aken B, Alfoldi J, Amemiya C, Azzouzi N, Baroiller JF, Barloy-Hubler F, Berlin A, Bloomquist R, Carleton KL, Conte MA, D'Cotta H, Eshel O, Gaffney L, Galibert F, Gante HF, et al.: The genomic substrate for adaptive radiation in African cichlid fish. Nature 2014, 513(7518):375-381.
  • [40]Pandian TJ, Sheela SG: Hormonal induction of sex reversal in fish. Aquaculture 1995, 138:1-22.
  • [41]Mair GC, Abucay JS, Abella TA, Beardmore JA, Skibinski DOF: Genetic manipulation of sex ratio for the large-scale production of all-male tilapia Oreochromis niloticus. Can J Fish Aquat Sci 1997, 54(2):396-404.
  • [42]Poonlaphdecha S, Pepey E, Canonne M, de Verdal H, Baroiller JF, D'Cotta H: Temperature induced-masculinisation in the Nile tilapia causes rapid up-regulation of both dmrt1 and amh expressions. Gen Comp Endocrinol 2013, 193:234-242.
  • [43]Poonlaphdecha S, Pepey E, Huang SH, Canonne M, Soler L, Mortaji S, Morand S, Pfennig F, Mélard C, Baroiller JF, D'Cotta H: Elevated amh gene expression in the brain of male tilapia (Oreochromis niloticus) during testis differentiation. Sex Dev 2011, 5(1):33-47.
  • [44]Fernandino JI, Hattori RS, Kishii A, Strussmann CA, Somoza GM: The cortisol and androgen pathways cross talk in high temperature-induced masculinization: the 11beta-hydroxysteroid dehydrogenase as a key enzyme. Endocrinology 2012, 153(12):6003-6011.
  • [45]Haugen T, Almeida FF, Andersson E, Bogerd J, Male R, Skaar KS, Schulz RW, Sorhus E, Wijgerde T, Taranger GL: Sex differentiation in Atlantic cod (Gadus morhua L.): morphological and gene expression studies. Reprod Biol Endocrinol 2012, 10:47. BioMed Central Full Text
  • [46]Duffy TA, Picha ME, Won ET, Borski RJ, McElroy AE, Conover DO: Ontogenesis of gonadal aromatase gene expression in atlantic silverside (Menidia menidia) populations with genetic and temperature-dependent sex determination. J Exp Zool A Ecol Genet Physiol 2010, 313(7):421-431.
  • [47]Blasco M, Fernandino JI, Guilgur LG, Strussmann CA, Somoza GM, Vizziano-Cantonnet D: Molecular characterization of cyp11a1 and cyp11b1 and their gene expression profile in pejerrey (Odontesthes bonariensis) during early gonadal development. Comp Biochem Physiol A Mol Integr Physiol 2010, 156(1):110-118.
  • [48]Meyer A, Schartl M: Gene and genome duplications in vertebrates: the one-to-four (−to-eight in fish) rule and the evolution of novel gene functions. Curr Opin Cell Biol 1999, 11(6):699-704.
  • [49]D'Cotta H, Fostier A, Guiguen Y, Govoroun M, Baroiller J-F: Aromatase plays a key role during normal and temperature-induced sex differentiation of tilapia Oreochromis niloticus. Mol Reprod Dev 2001, 59(3):265-276.
  • [50]Livak KJ, Schmittgen TD: Analysis of relative gene expression data using real-time quantitative PCR and the 2(−Delta Delta C(T)) method. Methods 2001, 25:402-408.
  • [51]Matson CK, Zarkower D: Sex and the singular DM domain: insights into sexual regulation, evolution and plasticity. Nat Rev Genet 2012, 13(3):163-174.
  • [52]Gautier A, Le Gac F, Lareyre J-J: The gsdf gene locus harbors evolutionary conserved and clustered genes preferentially expressed in fish previtellogenic oocytes. Gene 2011, 472(1–2):7-17.
  • [53]Rondeau E, Messmer A, Sanderson D, Jantzen S, von Schalburg K, Minkley D, Leong J, Macdonald G, Davidsen A, Parker W, Mazzola R, Campell B, Koop B: Genomics of sablefish (Anoplopoma fimbria): expressed genes, mitochondrial phylogeny, linkage map and identification of a putative sex gene. BMC Genomics 2013, 14(1):452. BioMed Central Full Text
  • [54]Shibata Y, Paul-Prasanth B, Suzuki A, Usami T, Nakamoto M, Matsuda M, Nagahama Y: Expression of gonadal soma derived factor (GSDF) is spatially and temporally correlated with early testicular differentiation in medaka. Gene Expr Patterns 2010, 10(6):283-289.
  • [55]Morrish B, Sinclair A: Vertebrate sex determination: many means to an end. Reproduction 2002, 124(4):447-457.
  • [56]Rodriguez-Mari A, Yan YL, Bremiller RA, Wilson C, Canestro C, Postlethwait JH: Characterization and expression pattern of zebrafish Anti-Mullerian hormone (Amh) relative to sox9a, sox9b, and cyp19a1a, during gonad development. Gene Expr Patterns 2005, 5(5):655-667.
  • [57]Mayor C, Brudno M, Schwartz JR, Poliakov A, Rubin EM, Frazer KA, Pachter LS, Dubchak I: VISTA: Visualizing global DNA sequence alignments of arbitrary length. Bioinformatics 2000, 16:1046.
  • [58]Frazer KA, Pachter L, Poliakov A, Rubin EM, Dubchak I: VISTA: computational tools for comparative genomics. Nucleic Acids Res 2004, 1(32):W273-W279.
  • [59]Mohapatra S, Liu ZH, Zhou LY, Zhang YG, Wang DS: Molecular cloning of wt1a and wt1b and their possible involvement in fish sex determination and differentiation. Ind J Sci Technol 2011, 4(S8):85-86.
  • [60]Hale MC, Xu P, Scardina J, Wheeler PA, Thorgaard GH, Nichols KM: Differential gene expression in male and female rainbow trout embryos prior to the onset of gross morphological differentiation of the gonads. BMC Genomics 2011, 12:404. BioMed Central Full Text
  • [61]Han F, Wang Z, Wu F, Liu Z, Huang B, Wang D: Characterization, phylogeny, alternative splicing and expression of Sox30 gene. BMC Mol Biol 2010, 11:98. BioMed Central Full Text
  • [62]Baroiller JF, Guiguen Y, Fostier A: Endocrine and environmental aspects of sex differentiation in fish. Cell Mol Life Sci 1999, 55:910-931.
  • [63]Burmeister SS, Kailasanath V, Fernald RD: Social dominance regulates androgen and estrogen receptor gene expression. Horm Behav 2007, 51(1):164-170.
  • [64]Böhne A, Sengstag T, Salzburger W: Comparative transcriptomics in East African cichlids reveals sex- and species-specific expression and new candidates for sex differentiation in fishes. Genome Biol Evol 2014, 6(9):2567-2585.
  • [65]Bezault E, Clota F, Derivaz M, Chevassus B, Baroiller J-F: Sex determination and temperature-induced sex differentiation in three natural populations of Nile tilapia (Oreochromis niloticus) adapted to extreme temperature conditions. Aquaculture 2007, 272, Supplement(0):S3-S16.
  • [66]Jameson SA, Lin Y-T, Capel B: Testis development requires the repression of Wnt4 by Fgf signaling. Dev Biol 2012, 370(1):24-32.
  • [67]Yu H, Pask A, Shaw G, Renfree M: Differential expression of WNT4 in testicular and ovarian development in a marsupial. BMC Dev Biol 2006, 6(1):44. BioMed Central Full Text
  • [68]Kim Y, Kobayashi A, Sekido R, DiNapoli L, Brennan J, Chaboissier M-C, Poulat F, Behringer RR, Lovell-Badge R, Capel B: Fgf9 and Wnt4 act as antagonistic signals to regulate mammalian sex determination. PLoS Biol 2006, 4(6):e187.
  • [69]Jeays-Ward K, Dandonneau M, Swain A: Wnt4 is required for proper male as well as female sexual development. Dev Biol 2004, 276(2):431-440.
  • [70]Barrionuevo FJ, Burgos M, Scherer G, Jiménez R: Genes promoting and disturbing testis development. Histol Histopathol 2012, 27(11):1361-1383.
  • [71]Miyamoto Y, Taniguchi H, Hamel F, Silversides DW, Viger RS: A GATA4/WT1 cooperation regulates transcription of genes required for mammalian sex determination and differentiation. BMC Mol Biol 2008, 9:44. BioMed Central Full Text
  • [72]Klüver N, Herpin A, Braasch I, Driessle J, Schartl M: Regulatory back-up circuit of medaka Wt1 co-orthologs ensures PGC maintenance. Dev Biol 2009, 325(1):179-188.
  • [73]Wang R-S, Yeh S, Tzeng C-R, Chang C: Androgen receptor roles in spermatogenesis and fertility: Lessons from testicular cell-specific androgen receptor knockout mice. Endocr Rev 2009, 30(2):119-132.
  • [74]Colombo M, Diepeveen ET, Muschick M, Santos ME, Indermaur A, Boileau N, Barluenga M, Salzburger W: The ecological and genetic basis of convergent thick-lipped phenotypes in cichlid fishes. Mol Ecol 2013, 22(3):670-684.
  • [75]Laird PW, Zijderveld A, Linders K, Rudnicki MA, Jaenisch R, Berns A: Simplified mammalian DNA isolation procedure. Nucleic Acids Res 1991, 19(15):4293.
  文献评价指标  
  下载次数:34次 浏览次数:25次