鲟鱼性别分化相关基因研究进展

doi:10.13560/j.cnki.biotech.bull.1985.2015.10.013

摘要/Abstract

摘要： 鲟鱼是目前世界上最古老的鱼类之一, 其肉质鲜美, 营养丰富, 鱼卵加工成的鱼子酱具有极高的经济价值。鲟鱼鱼子酱价格居高不下, 因此养殖雌性鲟鱼比养殖雄鱼具有更高的经济前景。由于鲟鱼外形无法辨别雌雄, 目前, 通常借助超声波、内窥镜等仪器进行早期性别鉴定, 但鉴别准确性无法保证。因此采用现代分子生物学技术探究鲟鱼性别决定及性别分化机制有助于早期鲟鱼性别鉴定技术的开发及实现鲟鱼全雌化苗种培育。总结了鱼类性别决定与性别分化相关基因的研究现状, 综述了目前在鲟鱼上性别决定与性别分化相关基因的研究进展并预测了未来的研究方向及研究趋势。

关键词: 鲟鱼, 性别分化, 基因

Abstract: Sturgeon is one of the oldest fishes in the world. Due to the delicious and nutritious flesh and caviar, sturgeon has extremely high economic value. Because of the price of caviar kept very high, breeding female sturgeon should get higher economic prospect than male. It seems impossible to identify the sex according to the exterior condition because of the similarity of sex characteristic on sturgeon. Currently, sex of immature sturgeon is usually identified through the ultrasonic instrument or with the help of endoscope. Even so, the accuracy of the identification cannot be ensured. Using molecular techniques to investigate sex determination and differentiation of sturgeon is supposed to conducively develop the technology of identifying sex and achieve the full female breeding. In this paper, the research status of genes related to sex determination and differentiation of fish is summarized, then the research progress on genes related to sex determination and differentiation of sturgeon is reviewed, and the feasible future research direction is also predicted.

Key words: sturgeon, sex differentiation, genes

东天,刘凤娇,胡红霞,朱华. 鲟鱼性别分化相关基因研究进展[J]. 生物技术通报, 2015, 31(10): 62-70.

Dong Tian, Liu Fengjiao, Hu Hongxia, Zhu Hua. Research Progress on Sex Differentiation Related Genes on Sturgeon[J]. Biotechnology Bulletin, 2015, 31(10): 62-70.

参考文献

[1]Billard R, Lecointre G. Biology and conservation of sturgeon and paddlefish[J]. Rev Fish Biol Fish, 2000, 10（4）：355-392.
[2]Ludwig A. A sturgeon view on conservation genetics[J]. Eur J Wildl Res, 2006, 52（1）：3-8.
[3]Bemis WE, Findeis EK. The sturgeons’ plight[J]. Nature, 1994, 370（6491）：602.
[4]Caprino F, Moretti VM, Bellagamba F, et al. Fatty acid composition and volatile compounds of caviar from farmed white sturgeon（Acipenser transmontanus）[J]. Anal Chim Acta, 2008, 617（1-2）：139-147.
[5]Mashroofeh A, Bakhtiari AR, Pourkazemi M. Bioaccumulation of Zn, Cu and Mn in the caviar and muscle of Persian sturgeon（Acipenser persicus）from the Caspian Sea, Iran[J]. Bull Environ Contam Toxicol, 2012, 89（6）：1201-1204.
[6]Pikitch EK, Doukakis P, Lauck L, et al. Status, trends and management of sturgeon and paddlefish fisheries[J]. Fish Fisheries, 2005, 6：233-265.
[7]Nelson TC, Doukakis P, Lindley ST, et al. Research tools to investigate movements, migrations, and life history of sturgeons（Acipenseridae）, with an emphasis on marine-oriented populations[J]. PLoS One, 2013, 8（8）：e71552.
[8]刘鉴毅, 危起伟, 杜浩, 等. 中华鲟人工繁殖关键技术的改进效果研究[J]. 经济动物学报, 2006, 10（2）：96-100.
[9]胡红霞, 董颖, 朱华, 等. 应用热休克和冷休克方法诱导俄罗斯鲟雌核发育初试[J]. 中国水产, 2010, 11：82.
[10]Doroshov SI, Moberg GP, Van Eenennaam JP. Observations on the reproductive cycle of cultured white sturgeon, acipenser transomntanus[J]. Environmental Biology of Fisheries, 1997, 48：265-278.
[11]Wildhaber ML, Papoulias DM, Delonay AJ, et al. Gender identification of shovelnose sturgeon using ultrasonic and endoscopic imagery and the application of the method to the pallid sturgeon[J]. J Fish Biol, 2005, 67：114-132.
[12]文爱韵, 尤锋, 徐永立, 等. 鱼类性别决定与分化相关基因研究进展[J]. 海洋科学, 2008, 32（1）：74-80.
[13]Kobayashi Y, Nagahama Y, Nakamura M. Diversity and plasticity of sex determination and differentiation in fishes[J]. Sex Dev, 2013, 7（1-3）：115-125.
[14]Shen ZG, Wang HP. Molecular players involved in temperature-dependent sex determination and sex differentiation in Teleost fish[J]. Genet Sel Evol, 2014, 46（1）：26.
[15]Baroiller JF, Dcotta H. Environment and sex determination in farmed fish[J]. Comp Biochem Physiol C Toxicol Pharmacol, 2001, 130（4）：399-409.
[16]Nakamura M, Takahashi H. Gonadal sex differentiation in Tilapia mossambica with special regard to the time of oestrogen treatment effective in inducing feminization of genetic fishes[J]. Bull Fac Fish Hokkaido Univ, 1973, 24：1-23.
[17]Satoh N, Egami N. Sex differentiation of germ cells in the teleost Oryzias latipes during normal embryonic development[J]. Embryol Exp Morphol, 1972, 28：385-395.
[18]Sinclair AH, Berta P, Palmer MS, et al. A gene from the human sex-determining region encodes a protein with homology to a conserved DNA-binding motif[J]. Nature, 1990, 346：240-244.
[19]Koopman P, Gubbay J, Vivian N, et al. Male development of chromosomally female mice transgenic for Sry[J]. Nature, 1991, 351（6322）：117-121.
[20]Yao HH, Capel B. Disruption of testis cords by cyclopamine or forskolin reveals independent cellular pathways in testis organogenesis[J]. Dev Biol, 2002, 246（2）：356-365.
[21]Smith CA, Roeszler KN, Ohnesorg T, et al. The avian Z-linked gene DMRT1 is required for male sex determination in the chicken[J]. Nature, 2009, 461：267-271.
[22]Matsuda M, Nagaharna Y, Shinomiya A, et al. DMY is a Y-specific DM-domain gene required for male development in the medaka fish[J]. Nature, 2002, 417：559-563.
[23]Hattori RS, Murai Y, Oura M, et al. A Y linked anti-Mullerian hormone duplication takes over a critical role in sex determination[J]. Proc Natl Acad Sci USA, 2012, 109（8）：2955-2959.
[24]Kamiya T, Kai W, Tasumi S, et al. A transspecies missense SNP in Amhr2 is associated with sex determination in the tiger pufferfish, Takifugu rubripes（fugu）[J]. PLoS Genet, 2012, 8：e1002798.
[25]Yano A, Guyomard R, Nicol B, et al. An immune-related gene evolved into the master sex-determining gene in rainbow trout, Oncorhynchus mykiss[J]. Curr Biol, 2012, 22：1423-1428.
[26]Ludwig A, Belfiore NM, Pitra C, et al. Genome duplication events and functional reduction of ploidy levels in sturgeon（Acipenser, Huso and Scaphirhynchus）[J]. Genetics, 2001, 158（3）：1203-1215.
[27]Rajkov J, Shao Z, Berrebi P. Evolution of polyploidy and functional diploidization in sturgeons：microsatellite analysis in 10 sturgeon species[J]. J Hered, 2014, 14：esu027.
[28]Chapman FA, Van Eenennaam JP, Doroshov SI. The reproductive condition of white sturgeon, Acipenser transmontanus, in San Francisco Bay, California[J]. Fish B-Noaa, 1996, 94：628-634.
[29]Van Eenennaam AL, Van Eenennaam JP, Medrano JE, et al. Evidence of female heterogametic genetic sex determination in white sturgeon[J]. J Hered, 1999, 90：231-233.
[30]Omoto N, Maebayashi M, Adachi S, et al. Sex ratios of tniploids and gynogenetic diploids induced in the hybrid sturgeon, the bester（Huso huso female 9 Acipenser ruthenus male）[J]. Aquaculture, 2005, 245：39-47.
[31]Flynn SR, Matsuoka M, Reith M, et al. Gynogenesis and sex determination in shortnose sturgeon, Acipenser brevirostrum Lesuere[J]. Aquaculture, 2006, 253：721-727.
[32]Wuertz S, Gaillard S, Barbisan F, et al. Extensive screening of sturgeon genomes by random screening techniques revealed no sex-specific marker[J]. Aquaculture, 2006, 258：685-688.
[33]Keyvanshokooh S, Pourkazemi M, Kalbassi MR. The RAPD technique failed to identify sex-specific sequences in beluga（Huso huso）[J]. J Appl Ichthyol, 2007, 23：1-2.
[34] McCormick CR, Bos DH, Dewoody JA. Multiple molecular approaches yield no evidence for sex-determining genes in lake sturgeon（Acipenser fulvescens）[J]. J Appl Ichthyol, 2008, 24：643-645.
[35] Yarmohammadi M, Pourkazemi M, Chakmehdouz F, et al. Comparative study of male and female gonads in Persian sturgeon（Acipenser persicus）employing DNA-AFLP and CDNA-AFLP analysis[J]. J Appl Ichthyol, 2011, 27：510-513.
[36] Nakamura M, Kobayashi T, Chang XT, et al. Gonadal sex differentiation in teleost fish[J]. Exp Zoolog, 1998, 281：362-372.
[37] Ying H, Siler W, Buckley JJ. Fuzzy control theory：A nonlinear case[J]. Automatic, 1990, 26（3）：513-520.
[38] Callard GV, Tchoudakova AV, Kishida M, et al. Differential tissue distribution, developmental programming, estrogen regulation and promoter characteristics of cyp19 genes in teleost fish[J]. J Steroid Biochem Mol Biol, 2001, 79（1-5）：305-314.
[39] Dalla VL, Ramina A, Vianello S, et al. Cloning of two mRNA variants of brain aromatase cytochrome P450 in rainbow flout（Oncohynchus mykiss Walbaum）[J]. J Steroid Biochem Mol Biol, 2002, 82：19-32.
[40]Simpson ER, Mahendroo MS, Means GD, et al. Aromatase cytochrome P450, the enzyme responsible for estrogen biosynthesis[J]. Endocrinol Rev, 1994, 15（3）：342-355.
[41]Trant JM, Gavasso S, Ackers J, et al. Developmental expression of cytochrome P450 aromatase genes（CYP19a and CYP19b）in zebrafish fry（Danio rerio）[J]. Exp Zool, 2001, 290（5）：475-483.
[42]Kishida M, Callard GV. Distinct cytochrome P450 aromatase isoforms in zebrafish（Danio rerio）brain and ovary are differentially programmed and estrogen regulated during early development[J]. Endocrinology, 2001, 142（2）：740-750.
[43]Tong SIC, Chiang EF, Hsiao PH, et al. Expression and enzyme activity of zebrafish cyp19（P450 aromatase）genes[J]. J Steroid Biochem Mol Biol, 2001, 79（125）：299-303.
[44]Chiang E, Yan Y, Guiguen Y, et al. Two Cyp19（P450 aromatase）genes on duplicated zebrafish chromosomes are expressed in ovary or brain[J]. Molecular Biology and Evolution, 2001, 18（4）：542-550.
[45]Blazquez M, Gonzalez A, Papadaki M, et al. Sex-related changes in estrogen receptors and aromatase gene expression and enzymatic activity during early development and sex differentia- tion in the European sea bass（Dicentrarchus labrax）[J]. Gen Comp Endocrinol, 2008, 158（1）：95-101.
[46]洪万树, 方永强. 鱼类芳香化酶活性研究的进展[J]. 水产学报, 2000, 24（3）：244-251.
[47]Lephart ED. A review of brain aromatase cytochrome P450[J]. Brain Res Rev, 1996, 22（1）：1-26.
[48]Bjerselius R, Lundstedt-Enkel K, Olsen H, et al. Male goldfish reproductive behaviour and physiology are severely affected by exogenous exposure to 17β-estradiol[J]. Aquat Toxicol, 2001, 53（2）：139-152.
[49] Tanaka M, Telecky TM, Fukada S, et al. Cloning and sequence analysis of the Cdna encod- ing P-450 aromatase（P450arom）from a rainbow trout Oncorhynchus mykiss ovary; relation- ship between the amount of P450arom mRNA and the production of oestradiol-17β in the ovary[J]. Mol Endocrinol, 1992, 8（1）：53-61.
[50]Kitano T, Takamune K, Kobayashi T, et al. Supression of P450 aromatase gene expression in sex reversed males produced by rearing genetically female larvae at a high water temperature during a period of sex differentiation in the Japanese flounder Paralichthys olivaceous[J]. Mol Endocrinol, 1999, 23（2）：167-176.
[51] Valle LD, Lunardi L, Colombo L, et al. European sea bass（Dicentrarchus labrax L. ）cytochrome P450arom：cDNA encoding, expression and genomic organization[J]. J Steriod Biochem Mol Biol, 2002, 80（1）：25-34.
[52] Chang XT, Kobayashi T, Senthilkumaran B, et al. Two types of aromatase with different encoding genes, tissue distribution and developmental expression in Nile tilapia（Oreochromis niloticus）[J]. Gen Comp Endocrinol, 2005, 141（2）：101-115.
[53]Ijiri S, Kazeto Y, Lokman P M, et al. Characterization of a cDNA encoding P450 aromatase（CYP19）from Japanese eel ovary and its expression in ovarian follicles during induced ovarian development[J]. Gen Comp Endocrinol, 2003, 130（2）：193-203.
[54]Tilmann C, Capel B. Cellular and molecular pathways regulating mammalian sex determination[J]. Recent Progress in Hormone Research, 2002, 57：1-18.
[55] Kondo M, Froschauer A, Kitano A, et al. Molecular cloning and characterization of Dmrt genes from the medaka Oryzias latipes and the platifish Xiphophorus maculates[J]. Gene, 2002, 295：213-222.
[56]Guan G, Kobayashi T, Nagahama Y. Sexually dimorphie expression of types of DM（Doublesex/ Mab-3）domain genes in a teleost fish, the tilapia（Oreochromis niloticus）[J]. Biochem Bioph Res Co, 2000, 72：662-666.
[57] Liu XS, Liang B, Zhang SY. cDNA cloning, tissue distribution and mrna transcription of dmrt1 gene in the protandrous black porgy Acanthopagrus schlegeli[J]. Zoological Research, 2004, 25（2）：158-161.
[58] Alam MA, Kobayashi Y, Horiguchi R. Molecular cloning and quantitative expression of sexually dimorphic markers Dmrt1 and Foxl2 during female-to-male sex change in Epinephelus merra[J]. Gen Comp Endocrinol, 2008, 157（1）：75-85.
[59] 邓思平, 陈松林. 半滑舌鳎Dmrt1α 基因的cDNA 克隆及其表达[J]. 中国水产科学, 2008, 15（4）：577-584.
[60] Raghuveer K, Senthilkumaran B. Identification of multiple dmrt1s in catfish：localization, dimorphic expression pattern, changes during testicular cycle and after methyl testosterone treatment[J]. Journal of Molecular Endocrinology, 2009, 42（5）：437-448.
[61] Kobayashi T, Matsuda M, Kajiura-Kobayashi H, et al. Two DM domain genes, DMY and DMRT1, involved in testicular differentiation and development in the medaka, Oryzias latipes[J]. Dev Dyn, 2004, 231（3）：518-526.
[62] Kobayashi T, Kajiura-Kobayashi H, Guan G. Sexual dimorphic expression of DMRT1 and Sox9a during gonadal differentiation and hormone-induced sex reversal in the teleost fish Nile tilapia（Oreochromis niloticus）[J]. Developmental Dynamics, 2008, 237（1）：297-306.
[63]Chen Y, Wang YL, Tian J, et al. Expression analysis of genes which related to sex determinateon of zebrafish[J]. Journal of Hydroecology, 2010, 3（5）：10-16.
[64]Yamaguchi A, Lee KH, Fujimoto H, et al. Expression of the dmrt gene and its roles in early gonadal development of the Japanese puffer fish Takifugu rubripes[J]. Comp Biochem Physiol Part D Genomics Proteomics, 2006, 1（1）：59-68.
[65]Marchand O, Gororoun M, D’Cotta H, et al. DMRTI expression during gonadal differentiate-on and spermatogenesis in the rainbow trout, Oncorchynchus[J]. Biochimica et Biophysica Acta, 2000, 1493：180-187.
[66]Nanda I, Kondo M, Hornung U, et al. A duplicated copy of DMRT1 in the sex-determining region of the Y chromosome of the medaka, Oryzias latipes[J]. PNAS, 2002, 99：11778-11783.
[67]Herpin A, Schartl M. Molecular mechanisms of sex determination and evolution of the Y-chromosome：insights from the medakafish（Oryzias latipes）[J]. Mol Cell Endocrinol, 2009, 306（1-2）：51-58.
[68]Ijiri S, Kaneko H, Kobayashi T, et al. Sexual dimorphic expression of genes in gonads during early differentiation of a teleost fish, the Nile Tilapia Oreochromis niloticus[J]. Biol Reprod, 2008, 78（2）：333-341.
[69]Takamatsu N, Kanda H, Ito M, et al. Rainbow trout SOX9：cDNA cloning, gene structure and expression[J]. Gene, 1997, 202（1-2）：167-170.
[70] Zhou RJ, Cheng HH, Zhang QY, et al. SRY-related genes in the genome of the rice field eel Monopterus albus[J]. Genet Sel Evol, 2002, 34：129-137.
[71]Zhou RJ, Liu L, Guo YQ, et al. Similar gene structure of two SOX9a genes and their expression patterns during gonadal differentiation in a teleost fish, rice field eel Monopterus albus[J]. Mol Reprod Dev, 2003, 66（3）：211-217.
[72]Yokoi H, Kobayashi T, Tanaka M, et al. SOX9 in a teleost fish, medaka Oryzias latipes：Evidence for diversified function of SOX9 in gonad differentiation[J]. Mol Reprod Dev, 2002, 63（1）：5-16.
[73]Dong XL, Chen SL, Ji XS, et al. Molecular cloning, characterization and expression analysis of Sox9a and Foxl2 genes in half-smooth tongue sole（Cynoglossussemilaevis）[J]. Acta Oceanologica Ainica, 2011, 30（1）：68-77.
[74] Amberg JJ, Goforth R, Stefanavage T, et al. Sexually dimorphic gene expression in the gonad and liver of shovelnose sturgeon（Scaphirhynchus platorynchus）[J]. Fish Physiol Biochem, 2010, 36（4）：923-932.
[75]Berbejillo J, Martinez-Bengochea A, Bedo G, et al. Expression and phylogeny of candidate genes for sex differentiation in a primitive fish species, the siberian sturgeon, Acipenser baerii[J]. Molecular Reproduction And Development, 2012（79）：504-516.
[76] Berbejillo J, Martinez-Bengochea A, Bedo G, et al. Expression of dmrt1 and sox9 during gonadal development in the Siberian sturgeon（Acipenser baerii）[J]. Fish Physiol Biochem, 2013, 39：91-94.
[77]Hett AK, Ludwig A. SRY-related（Sox）genes in the genome of European Atlantic sturgeon（Acipenser sturio）[J]. Genome, 2005, 48：181-186.
[78]Hett AK, Pitra C, Jenneckens I, et al. Characterization of Sox9 in European Atlantic sturgeon（Acipenser sturio）[J]. J Hered, 2005, 96（2）：150-154.
[79]陈金平, 袁红梅, 王斌, 等. 史氏鲟Sox9基因cDNA的克隆及在早期发育过程不同组织中的表达[J]. 动物学研究, 2004, 25（6）：527-533.
[80]Wang DS, Kobayashi T, Zhou LY, et al. 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 factor1[J]. Mol Endocrinol, 2007, 21（3）：712-725.
[81] Marongiu M, Deiana M, Meloni A, et al. The forkhead transcription factor Foxl2 is sumoylated in both human and mouse：sumoylation affects its stability, localization, and activity[J]. PLoS One, 2010, 5（3）：9477-9482.
[82]Nakamoto M, Matsuda M, Wang D, et al. Molecular cloning and analysis of gonadal expression of Foxl2 in the medaka, Oryzias latipes[J]. Biochem Biophys Res Commun, 2006, 344（1）：353-361.
[83]Yamaguchi T, Yamaguchi S, Hirai T, et al. Follicle-stimulating hormone signaling and Foxl2 are involved in transcriptional regulation of aromatase gene during gonadal sex differentiation in Japanese flounder, Paralichthys olivaceus[J]. Biochem Biophys Res Commun, 2007, 359（4）：935-940.
[84]Lee BY, Kocher TD. Exclusion of Wilms tumour（WT1b）and ovarian cytochrome P450 aromatase（CYP19A1）as candidates for sex determination genes in Nile tilapia（Oreochromis niloticus）[J]. Animal Genetics, 2007, 38（1）：85-86.
[85]Nakamoto M, Wang DS, Suzuki A, et al. Dax1 suppresses P450arom expression in medaka ovarian follicles[J]. Mol Reprod Dev, 2007, 74（10）：1239-1246.
[86]Hale MC, Jackson JR, Dewoody JA. Discovery and evaluation of candidate sex-determining genes and xenobiotics in the gonads of lak sturgeon（Acipenser fulvescens）[J]. Genetica, 2010, 138（7）：745-756.
[87]Amberg JJ, Goforth RR, Seplveda MS. Antagonists to the wnt cascade exhibit sex-specific expression in gonads of sexually mature shovelnose sturgeon[J]. Sex Dev, 2013, 7：308-315.
[88]Hagihara S, Yamashita R, Yamamoto S, et al. Identification of genes involved in gonadal sex differentiation and the dimorphic expression pattern in undifferentiated gonads of Russian sturgeon Acipenser gueldenstaedtii Brandt & Ratzeburg, 1833[J]. J Appl Ichthyol, 2014, 30：1557-1564.
[89]Vidotto M, Grapputo A, Boscari E, et al. Transcriptome sequencing and de novo annotation of the critically endangered Adriatic sturgeon[J]. BMC Genomics, 2013, 14：407-423.