Abstract
Aquaculture is one of the fastest developing agricultural industries worldwide. One of the most important factors for sustainable aquaculture is the development of high performing culture strains. Genome manipulation offers a powerful method to achieve rapid and directional breeding in fish. We review the history of fish breeding methods based on classical genome manipulation, including polyploidy breeding and nuclear transfer. Then, we discuss the advances and applications of fish directional breeding based on transgenic technology and recently developed genome editing technologies. These methods offer increased efficiency, precision and predictability in genetic improvement over traditional methods.
Article PDF
Similar content being viewed by others
Avoid common mistakes on your manuscript.
References
Cressey D. Aquaculture: Future fish. Nature, 2009, 458: 398–400
Gui JF, Zhu ZY. Molecular basis and genetic improvement of economically important traits in aquaculture animals. Chin Sci Bull, 2012, 57: 1751–1760
Bakos J, Gorda S. Genetic-improvement of common carp strains using intraspecific hybridization. Aquaculture, 1995, 129: 183–186
Bartley DM, Rana K, Immink AJ. The use of inter-specific hybrids in aquaculture and fisheries. Rev Fish Biol Fisher, 2000, 10: 325–337
Wu CJ, Ye YZ, Chen RD. Genome manipulation in carp (cyprinuscarpio l). Aquaculture, 1986, 54: 57–61
Zhu ZY, Sun YH. Embryonic and genetic manipulation in fish. Cell Res, 2000, 10: 17–27
Nagy A, Rajki K, Horvath L, Csanyi V. Investigation on carp, cyprinuscarpio l gynogenesis. J Fish Bio, 1978, 13: 215–224
Sajiro Makino YO. Formation of the diploid egg nucleus due to suppression of the second maturation division, induced by refrigeration of fertilized eggs of the carp, cyprinus carpio. Cytologia, 1943, 13: 55–60
Komen H, Thorgaard GH. Androgenesis, gynogenesis and the production of clones in fishes: a review. Aquaculture, 2007, 269: 150–173
Streisinger G, Walker C, Dower N, Knauber D, Singer F. Production of clones of homozygous diploid zebra fish (brachydanio rerio). Nature, 1981, 291: 293–296
Chen SL, Ji XS, Shao CW, Li WL, Yang JF, Liang Z, Liao XL, Xu GB, Xu Y, Song WT. Induction of mitogynogenetic diploids and identification of ww super-female using sex-specific ssr markers in half-smooth tongue sole (Cynoglossus semilaevis). Mar Biotechnol, 2012, 14: 120–128
Chen SL, Tian YS, Yang JF, Shao CW, Ji XS, Zhai JM, Liao XL, Zhuang ZM, Su PZ, Xu JY, Sha ZX, Wu PF, Wang N. Artificial gynogenesis and sex determination in half-smooth tongue sole (Cynoglossus semilaevis). Mar Biotechnol, 2009, 11: 243–251
Wang D, Mao HL, Chen HX, Liu HQ, Gui JF. Isolation of y- and x-linked scar markers in yellow catfish and application in the production of all-male populations. Anim Genet, 2009, 40: 978–981
Horvath L, Orban L. Genome and gene manipulation in the common carp. Aquaculture, 1995, 129: 157–181
Guo XH, Liu SJ, Liu Y. Evidence for recombination of mitochondrial DNA in triploid crucian carp. Genetics, 2006, 172: 1745–1749
Liu SJ, Liu Y, Zhou GJ, Zhang XJ, Luo C, Feng H, He XX, Zhu GH, Yang H. The formation of tetraploid stocks of red crucian carp×common carp hybrids as an effect of interspecific hybridization. Aquaculture, 2001, 192: 171–186
Liu SJ, Qin QB, Xiao J, Lu WT, Shen JM, Li W, Liu JF, Duan W, Zhang C, Tao M, Zhao RR, Yan JP, Liu Y. The formation of the polyploid hybrids from different subfamily fish crossings and its evolutionary significance. Genetics, 2007, 176: 1023–1034
Qin QB, He WG, Liu SJ, Wang J, Xiao J, Liu Y. Analysis of 5S rDNA organization and variation in polyploid hybrids from crosses of different fish subfamilies. J Exp Zool Part B, 2010, 314B: 403–411
Gurdon JB, Wilmut I. Nuclear transfer to eggs and oocytes. CSH Perspect in Biol, 2011, 3: a002659
Wilmut I, Schnieke AE, McWhir J, Kind AJ, Campbell KH. Viable offspring derived from fetal and adult mammalian cells. Nature, 1997, 385: 810–813
Tung TC, Wu SC, Tung YYF, Yan SY, Tu M, Lu TY. Nuclear trans plantation in fish. Chinese Sci Bull, 1963, 7: 60–61
Chen HX, Yi YL, Chen MR, Yang X. Studies on the developmental potentiality of cultured cell nuclei of fish. Acta Hydrobiol Sin, 1986, 10: 1–7
Chen H, Yi Y, Chen M, Yang X. Studies on the developmental potentiality of cultured cell nuclei of fish. Int J Biol Sci, 2010, 6: 192–198
Lee KY, Huang H, Ju B, Yang Z, Lin S. Cloned zebrafish by nuclear transfer from long-term-cultured cells. Nat Biotechnol, 2002, 20: 795–799
Yi M, Hong N, Hong Y. Generation of medaka fish haploid embryonic stem cells. Science, 2009, 326: 430–433
Tung TC, Tung YYF. Nuclear transplantation in teleosts. I. Hybrid fish from the nucleus of carp and the cytoplasm of crucian. Sci Sin, 1980, 14: 1244–1245
Gurdon JB. The transplantation of nuclei between two species of xenopus. Dev Biol, 1962, 5: 68–83
Moore JA. Serial back-transfers of nuclei in experiments involving two species of frogs. Dev Biol, 1960, 2: 535–550
Sun YH, Zhu ZY. Cross-species cloning: Influence of cytoplasmic factors on development. J Physiol, 2014, 592: 2375–2379
Yan S, Lu D, Du M, Li G, Lin L, Jin G, Wang H, Yang Y, Xia D, Liu A. Nuclear transplantation in teleosts. Hybrid fish from the nucleus of crucian and the cytoplasm of carp. Sci Sin Series B, 1984, 27: 1029
Sun YH, Chen SP, Wang YP, Hu W, Zhu ZY. Cytoplasmic impact on cross-genus cloned fish derived from transgenic common carp (Cyprinus carpio) nuclei and goldfish (Carassius auratus) enucleated eggs. Biol Reprod, 2005, 72: 510–515
Yan SY, Mao ZR, Yang HY, Tu MA, Li SH, Huang GP, Li GS, Guo L, Jin GQ, He RF, et al. Further investigation on nuclear transplantation in different orders of teleost: the combination of the nucleus of tilapia (Oreochromis nilotica) and the cytoplasm of loach (Paramisgurnus dabryanus). Int J Dev Biol, 1991, 35: 429–435
Yan SY, Tu M, Yang HY, Mao ZG, Zhao ZY, Fu LJ, Li GS, Huang GP, Li SH, Jin GQ, et al. Developmental incompatibility between cell nucleus and cytoplasm as revealed by nuclear transplantation experiments in teleost of different families and orders. Int J Dev Biol, 1990, 34: 255–266
Yi YL, Liu PL, Liu HQ, Chen HX. Electric fusion between blastula cells and unfertilized eggs in fish. Acta Hydrobiol Sin, 1988, 12: 189–192
Yu LL, Zuo WG, Fang YL, Zheng WD. Cell-engineering grass carp produced by the combination of electric fusion and nuclear transplantation. J Fish China, 1996, 20: 314–318
Inoue K, Yamashita S, Hata J, Kabeno S, Asada S, Nagahisa E, Fujita T. Electroporation as a new technique for producing transgenic fish. Cell Diff Dev, 1990, 29: 123–128
Powers DA, Hereford L, Cole T, Chen TT, Lin CM, Kight K, Creech K, Dunham R. Electroporation: a method for transferring genes into the gametes of zebrafish (Brachydanio rerio), channel catfish (Ictalurus punctatus), and common carp (Cyprinus carpio). Mol Mar Biol Biotechnol, 1992, 1: 301–308
Xie YD, Liu J, Zou GL, Zhu Z. Gene transfer via electroporation in fish. Aquaculture, 1993, 111: 207–213
Khoo HW, Ang LH, Lim HB, Wong KY. Sperm cells as vectors for introducing foreign DNA into zebrafish. Aquaculture, 1992, 107: 1–19
Lavitrano M, Camaioni A, Fazio VM, Dolci S, Farace MG, Spadafora C. Sperm cells as vectors for introducing foreign DNA into eggs—genetic-transformation of mice. Cell, 1989, 57: 717–723
Tsai HJ. Electroporated sperm mediation of a gene transfer system for finfish and shellfish. Mol Reprod Dev, 2000, 56: 281–284
Zhong JY, Wang YP, Zhu ZY. Introduction of the human lactoferrin gene into grass carp (Ctenopharyngodon idellus) to increase resistance against GCH virus. Aquaculture, 2002, 214: 93–101
Lin S, Gaiano N, Culp P, Burns JC, Friedmann T, Yee JK, Hopkins N. Integration and germ-line transmission of a pseudotyped retroviral vector in zebrafish. Science, 1994, 265: 666–669
Linney E, Hardison NL, Lonze BE, Lyons S, DiNapoli L. Transgene expression in zebrafish: a comparison of retroviral-vector and DNA-injection approaches. Dev Biol, 1999, 213: 207–216
Lu JK, Burns JC, Chen TT. Pantropic retroviral vector integration, expression, and germline transmission in medaka (Oryzias latipes). Mol Mar Biol Biotechnol, 1997, 6: 289–295
Lu JK, Fu BH, Wu JL, Chen TT. Production of transgenic silver sea bream (Sparus sarba) by different gene transfer methods. Mar Biotechnol, 2002, 4: 328–337
Zhu ZY, Li GH, He L, Chen S. Novel gene transfer into the fertilized eggs of goldfish (Carassius auratus L. 1758). J Appl Ichthyol, 1985, 1: 31–34
Zhu Z, Xu K, Li G, Xie Y, He L. Biological effects of human growth hormone gene microinjected into the fertilized eggs of loach, misgurus anguillicaudatus (cantor). Chinese Sci Bull, 1986, 31: 988–990
Zhang PJ, Hayat M, Joyce C, Gonzalez-Villasenor LI, Lin CM, Dunham RA, Chen TT, Powers DA. Gene transfer, expression and inheritance of pRSV-rainbow trout-GH cDNA in the common carp, cyprinus carpio (Linnaeus). Mol Reprod Dev, 1990, 25: 3–13
Feng H, Fu YM, Luo J, Wu H, Liu Y, Liu S. Black carp growth hormone gene transgenic allotetraploid hybrids of Carassius auratus red var. (female symbol)×Cyprinus carpio (male symbol). Sci China Life Sci, 2011, 54: 822–827
Zhu Z, Xu K, Xie Y, Li G, He L. A model of transgenic fish. Sci Sin B, 1989, (2): 147–155
Wang Y, Hu W, Wu G, Sun Y, Chen S, Zhang F, Zhu Z, Feng J, Zhang X. Genetic analysis of “all-fish” growth hormone gene transferred carp (Cyprinus carpio L.) and its F1 generation. Chinese Sci Bull, 2001, 46: 1174–1177
Zhu Z, He L, Chen TT. Primary-structural and evolutionary analyses of the growth-hormone gene from grass carp (Ctenopharyngodon idellus). Eur J Biochem, 1992, 207: 643–648
Du SJ, Gong ZY, Fletcher GL, Shears MA, King MJ, Idler DR, Hew CL. Growth enhancement in transgenic atlantic salmon by the use of an “all fish” chimeric growth hormone gene construct. Biotechnology (NY), 1992, 10: 176–181
Martinez R, Estrada MP, Berlanga J, Guillen I, Hernandez O, Cabrera E, Pimentel R, Morales R, Herrera F, Morales A, Pina JC, Abad Z, Sanchez V, Melamed P, Lleonart R, de la Fuente J. Growth enhancement in transgenic tilapia by ectopic expression of tilapia growth hormone. Mol Mar Biol Biotechnol, 1996, 5: 62–70
Rahman MA, Mak R, Ayad H, Smith A, Maclean N. Expression of a novel piscine growth hormone gene results in growth enhancement in transgenic tilapia (Oreochromis niloticus). Transgenic Res, 1998, 7: 357–369
Wang R, Zhang P, Gong Z, Hew CL. Expression of the antifreeze protein gene in transgenic goldfish (Carassius auratus) and its implication in cold adaptation. Mol Mar Biol Biotechnol, 1995, 4: 20–26
Fletcher GL, Hobbs RS, Evans RP, Shears MA, Hahn AL, Hew CL. Lysozyme transgenic atlantic salmon (Salmo salar L.). Aquac Res, 2011, 42: 427–440
Hew CL, Fletcher GL, Davies PL. Transgenic salmon: tailoring the genome for food production. J Fish Biol, 1995, 47: 1–19
Dunham RA, Warr GW, Nichols A, Duncan PL, Argue B, Middleton D, Kucuktas H. Enhanced bacterial disease resistance of transgenic channel catfish ictalurus punctatus possessing cecropin genes. Mar Biotechnol, 2002, 4: 338–344
Sun CF, Tao Y, Jiang XY, Zou SM. IGF binding protein 1 is correlated with hypoxia-induced growth reduce and developmental defects in grass carp (ctenopharyngodon idellus) embryos. Gen Comp Endocrinol, 2011, 172: 409–415
Ishtiaq Ahmed AS, Xiong F, Pang SC, He MD, Waters MJ, Zhu ZY, Sun YH. Activation of gh signaling and gh-independent stimulation of growth in zebrafish by introduction of a constitutively activated ghr construct. Transgenic Res, 2011, 20: 557–567
Marszalek JR, Lodish HF. Docosahexaenoic acid, fatty acid-interacting proteins, and neuronal function: Breastmilk and fish are good for you. Annu Rev Cell Dev Biol, 2005, 21: 633–657
Alimuddin, Kiron V, Satoh S, Takeuchi T, Yoshizaki G. Cloning and over-expression of a masu salmon (Oncorhynchus masou) fatty acid elongase-like gene in zebrafish. Aquaculture, 2008, 282: 13–18
Alimuddin, Yoshizaki G, Kiron V, Satoh S, Takeuchi T. Expression of masu salmon delta5-desaturase-like gene elevated EPA and DHA biosynthesis in zebrafish. Mar Biotechnol, 2007, 9: 92–100
Alimuddin, Yoshizaki G, Kiron V, Satoh S, Takeuchi T. Enhancement of EPA and DHA biosynthesis by over-expression of masu salmon delta6-desaturase-like gene in zebrafish. Transgenic Res, 2005, 14: 159–165
Pang SC, Wang HP, Li KY, Zhu ZY, Kang JX, Sun YH. Double transgenesis of humanized fat1 and fat2 genes promotes omega-3 polyunsaturated fatty acids synthesis in a zebrafish model. Mar Biotechnol, 2014, 16: 580–593
Hwang GL, Muller F, Rahman MA, Williams DW, Murdock PJ, Pasi KJ, Goldspink G, Farahmand H, Maclean N. Fish as bioreactors: transgene expression of human coagulation factor VII in fish embryos. Mar Biotechnol, 2004, 6: 485–492
Morita T, Yoshizaki G, Kobayashi M, Watabe S, Takeuchi T. Fish eggs as bioreactors: the production of bioactive luteinizing hormone in transgenic trout embryos. Transgenic Res, 2004, 13: 551–557
Hu SY, Liao CH, Lin YP, Li YH, Gong HY, Lin GH, Kawakami K, Yang TH, Wu JL. Zebrafish eggs used as bioreactors for the production of bioactive tilapia insulin-like growth factors. Transgenic Res, 2011, 20: 73–83
Provost E, Rhee J, Leach SD. Viral 2A peptides allow expression of multiple proteins from a single ORF in transgenic zebrafish embryos. Genesis, 2007, 45: 625–629
Trichas G, Begbie J, Srinivas S. Use of the viral 2A peptide for bicistronic expression in transgenic mice. BMC Biol, 2008, 6: 40
Deng W, Yang D, Zhao B, Ouyang Z, Song J, Fan N, Liu Z, Zhao Y, Wu Q, Nashun B, Tang J, Wu Z, Gu W, Lai L. Use of the 2A peptide for generation of multi-transgenic pigs through a single round of nuclear transfer. PLoS One, 2011, 6: e19986
Devlin RH, Sundstrom LF, Muir WM. Interface of biotechnology and ecology for environmental risk assessments of transgenic fish. Trends Biotechnol, 2006, 24: 89–97
Sundstrom LF, Vandersteen WE, Lohmus M, Devlin RH. Growth-enhanced coho salmon invading other salmon species populations: effects on early survival and growth. J Appl Ecol, 2014, 51: 82–89
Hu W, Wang Y, Zhu Z. Progress in the evaluation of transgenic fish for possible ecological risk and its containment strategies. Sci China Ser C-Life Sci, 2007, 50: 573–579
Yu F, Xiao J, Liang XY, Liu SJ, Zhou GJ, Luo KK, Liu Y, Hu W, Wang YP, Zhu ZY. Rapid growth and sterility of growth hormone gene transgenic triploid carp. Chin Sci Bull, 2011, 56: 1679–1684
McCammon JM, Amacher SL. Using zinc finger nucleases for efficient and heritable gene disruption in zebrafish. Methods Mol Biol, 2010, 649: 281–298
Bedell VM, Wang Y, Campbell JM, Poshusta TL, Starker CG, Krug RG 2nd, Tan W, Penheiter SG, Ma AC, Leung AY, Fahrenkrug SC, Carlson DF, Voytas DF, Clark KJ, Essner JJ, Ekker SC. In vivo genome editing using a high-efficiency talen system. Nature, 2012, 491: 114–118
Huang P, Xiao A, Zhou M, Zhu Z, Lin S, Zhang B. Heritable gene targeting in zebrafish using customized talens. Nat Biotechnol, 2011, 29: 699–700
Chang N, Sun C, Gao L, Zhu D, Xu X, Zhu X, Xiong JW, Xi JJ. Genome editing with RNA-guided Cas9 nuclease in zebrafish embryos. Cell Res, 2013, 23: 465–472
Hwang WY, Fu Y, Reyon D, Maeder ML, Tsai SQ, Sander JD, Peterson RT, Yeh JR, Joung JK. Efficient genome editing in zebrafish using a CRISPR-cas system. Nat Biotechnol, 2013, 31: 227–229
Zhang LL, Zhou Q. CRISPR/cas technology: a revolutionary approach for genome engineering. Sci China Life Sci, 2014, 57: 639–64
Hsu PD, Lander ES, Zhang F. Development and applications of CRISPR-cas9 for genome engineering. Cell, 2014, 157: 1262–1278
Tan W, Carlson DF, Lancto CA, Garbe JR, Webster DA, Hackett PB, Fahrenkrug SC. Efficient nonmeiotic allele introgression in livestock using custom endonucleases. Proc Natl Acad Sci USA, 2013, 110: 16526–16531
Lillico SG, Proudfoot C, Carlson DF, Stverakova D, Neil C, Blain C, King TJ, Ritchie WA, Tan W, Mileham AJ, McLaren DG, Fahrenkrug SC, Whitelaw CB. Live pigs produced from genome edited zygotes. Sci Rep, 2013, 3: 2847
Proudfoot C, Carlson DF, Huddart R, Long CR, Pryor JH, King TJ, Lillico SG, Mileham AJ, McLaren DG, Whitelaw CB, Fahrenkrug SC. Genome edited sheep and cattle. Transgenic Res, 2015, 24: 147–153
Wang HL, Zhu ZY, Sun YH. TALEN-mediated knock out of zebrafish SOCS2 and the growth performance of SOCS2 mutants. Acta Hydrobiol Sin, 2015, in press
Xiao A, Wang Z, Hu Y, Wu Y, Luo Z, Yang Z, Zu Y, Li W, Huang P, Tong X, Zhu Z, Lin S, Zhang B. Chromosomal deletions and inversions mediated by talens and CRISPR/cas in zebrafish. Nucleic Acids Res, 2013, 41: e141
Hruscha A, Krawitz P, Rechenberg A, Heinrich V, Hecht J, Haass C, Schmid B. Efficient CRISPR/cas9 genome editing with low off-target effects in zebrafish. Development, 2013, 140: 4982–4987
Gasiunas G, Barrangou R, Horvath P, Siksnys V. Cas9-crRNA ribonucleoprotein complex mediates specific DNA cleavage for adaptive immunity in bacteria. Proc Natl Acad Sci USA, 2012, 109: E2579–2586
Jinek M, Chylinski K, Fonfara I, Hauer M, Doudna JA, Charpentier E. A programmable dual-RNA-guided DNA endonuclease in adaptive bacterial immunity. Science, 2012, 337: 816–821
Sapranauskas R, Gasiunas G, Fremaux C, Barrangou R, Horvath P, Siksnys V. The streptococcus thermophilus CRISPR/cas system provides immunity in escherichia coli. Nucleic Acids Res, 2011, 39: 9275–9282
Mali P, Aach J, Stranges PB, Esvelt KM, Moosburner M, Kosuri S, Yang L, Church GM. Cas9 transcriptional activators for target specificity screening and paired nickases for cooperative genome engineering. Nat Biotechnol, 2013, 31: 833–838
Ran FA, Hsu PD, Lin CY, Gootenberg JS, Konermann S, Trevino AE, Scott DA, Inoue A, Matoba S, Zhang Y, Zhang F. Double nicking by RNA-guided CRISPR cas9 for enhanced genome editing specificity. Cell, 2013, 154: 1380–1389
Zu Y, Tong X, Wang Z, Liu D, Pan R, Li Z, Hu Y, Luo Z, Huang P, Wu Q, Zhu Z, Zhang B, Lin S. Talen-mediated precise genome modification by homologous recombination in zebrafish. Nat Methods, 2013, 10: 329–331
Dickinson DJ, Ward JD, Reiner DJ, Goldstein B. Engineering the caenorhabditis elegans genome using Cas9-triggered homologous recombination. Nat Methods, 2013, 10: 1028–1034
Bassett AR, Tibbit C, Ponting CP, Liu JL. Mutagenesis and homologous recombination in drosophila cell lines using CRISPR/cas9. Biol Open, 2014, 3: 42–49
Bottcher R, Hollmann M, Merk K, Nitschko V, Obermaier C, Philippou-Massier J, Wieland I, Gaul U, Forstemann K. Efficient chromosomal gene modification with CRISPR/cas9 and PCR-based homologous recombination donors in cultured drosophila cells. Nucleic Acids Res, 2014, 42: e89
Yu Z, Chen H, Liu J, Zhang H, Yan Y, Zhu N, Guo Y, Yang B, Chang Y, Dai F, Liang X, Chen Y, Shen Y, Deng WM, Chen J, Zhang B, Li C, Jiao R. Various applications of talen- and CRISPR/cas9-mediated homologous recombination to modify the drosophila genome. Biol Open, 2014, 3: 271–280
Rong Z, Zhu S, Xu Y, Fu X. Homologous recombination in human embryonic stem cells using CRISPR/cas9 nickase and a long DNA donor template. Protein Cell, 2014, 5: 258–260
Xue H, Wu J, Li S, Rao MS, Liu Y. Genetic modification in human pluripotent stem cells by homologous recombination and CRISPR/cas9 system. Methods Mol Biol, 2014, 1114: 37–55
Kretzschmar A, Otto C, Holz M, Werner S, Hubner L, Barth G. Increased homologous integration frequency in Yarrowia lipolytica strains defective in non-homologous end-joining. Curr Genet, 2013, 59: 63–72
Ninomiya Y, Suzuki K, Ishii C, Inoue H. Highly efficient gene replacements in neurospora strains deficient for nonhomologous end-joining. Proc Natl Acad Sci USA, 2004, 101: 12248–12253
Nishizawa-Yokoi A, Nonaka S, Saika H, Kwon YI, Osakabe K, Toki S. Suppression of Ku70/80 or Lig4 leads to decreased stable transformation and enhanced homologous recombination in rice. New Phytol, 2012, 196: 1048–1059
Verbeke J, Beopoulos A, Nicaud JM. Efficient homologous recombination with short length flanking fragments in Ku70 deficient Yarrowia lipolytica strains. Biotechnol Lett, 2013, 35: 571–576
Wei ZQ, Xiong F, He MD, Wang HP, Zhu ZY, Sun YH. Suppression of ligase 4 or XRCC6 activities enhances the DNA homologous recombination efficiency in zebrafish primordial germ cells. Acta Hydrobiol Sin, 2015, in press
Xiong F, Wei ZQ, Zhu ZY, Sun YH. Targeted expression in zebrafish primordial germ cells by cre/loxP and Gal4/UAS systems. Mar Biotechnol, 2013, 15: 526–539
Wang H, Yang H, Shivalila CS, Dawlaty MM, Cheng AW, Zhang F, Jaenisch R. One-step generation of mice carrying mutations in multiple genes by CRISPR/cas-mediated genome engineering. Cell, 2013, 153: 910–918
Author information
Authors and Affiliations
Corresponding author
Additional information
This article is published with open access at springerlink.bibliotecabuap.elogim.com
Rights and permissions
Open Access This article is distributed under the terms of the Creative Commons Attribution 4.0 International License (https://creativecommons.org/licenses/by/4.0), which permits use, duplication, adaptation, distribution, and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made.
About this article
Cite this article
Ye, D., Zhu, Z. & Sun, Y. Fish genome manipulation and directional breeding. Sci. China Life Sci. 58, 170–177 (2015). https://doi.org/10.1007/s11427-015-4806-7
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s11427-015-4806-7