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- W2964213295 abstract "Aquaculture is an increasingly important component of global food security, and there is major potential for genetic improvement to contribute to sustainable production.The high fecundity and external fertilisation of most aquaculture species are amenable to the application of genetic improvement technologies, including genome editing using CRISPR/Cas9.Disease resistance is a major target trait for improvement, and CRISPR/Cas9 offers new opportunities to fix existing alleles, to perform introgression-by-editing of alleles from wild populations or related species, and to create de novo alleles.Combining in vivo and in vitro screening approaches has the potential to identify functional disease resistance alleles for downstream functional testing and application.Using genome editing to achieve 100% sterility of production animals is a promising avenue to prevent interbreeding of escapees with wild stocks. Aquaculture is the fastest growing food production sector and is rapidly becoming the primary source of seafood for human diets. Selective breeding programs are enabling genetic improvement of production traits, such as disease resistance, but progress is limited by the heritability of the trait and generation interval of the species. New breeding technologies, such as genome editing using CRISPR/Cas9 have the potential to expedite sustainable genetic improvement in aquaculture. Genome editing can rapidly introduce favorable changes to the genome, such as fixing alleles at existing trait loci, creating de novo alleles, or introducing alleles from other strains or species. The high fecundity and external fertilization of most aquaculture species can facilitate genome editing for research and application at a scale that is not possible in farmed terrestrial animals. Aquaculture is the fastest growing food production sector and is rapidly becoming the primary source of seafood for human diets. Selective breeding programs are enabling genetic improvement of production traits, such as disease resistance, but progress is limited by the heritability of the trait and generation interval of the species. New breeding technologies, such as genome editing using CRISPR/Cas9 have the potential to expedite sustainable genetic improvement in aquaculture. Genome editing can rapidly introduce favorable changes to the genome, such as fixing alleles at existing trait loci, creating de novo alleles, or introducing alleles from other strains or species. The high fecundity and external fertilization of most aquaculture species can facilitate genome editing for research and application at a scale that is not possible in farmed terrestrial animals. Food security is a major and increasing global challenge, associated with a rapidly growing demand for high-quality animal protein. Competition for land use will present a serious limitation to the scope for increases in terrestrial crop and animal production [1.Smith P. et al.Competition for land.Philos. Trans. R. Soc. Lond. Ser. B Biol. Sci. 2010; 365: 2941-2957Crossref PubMed Scopus (336) Google Scholar, 2.Organisation for Economic Co-operation and Development OECD Environmental Outlook to 2050. OECD Publishing, 2012Google Scholar]. Therefore, it is likely that aquaculture will have a growing role in meeting this rising food and nutrition demand. Fish production via aquaculture is now approximately equal to capture fishery production for the first time in history, will be the dominant source of seafood within a few decades [3.Food and Agriculture Organization of the United Nations 2018 The State of World Fisheries and Aquaculture: Meeting the Sustainable Development Goals. FAO, 2018Crossref Google Scholar], and is the fastest growing food production sector, predicted to grow by 31% over the next 10 years [4.Organisation for Economic Co-operation and Development OECD-FAO Agricultural Outlook 2018-2027. OECD Publishing, 2018Google Scholar]. Fortunately, development potential is huge, with only ~1% of suitable marine sites currently being used for aquaculture [5.Gentry R.R. et al.Mapping the global potential for marine aquaculture.Nat. Ecol. Evol. 2017; 1: 1317-1324Crossref PubMed Scopus (218) Google Scholar]. Furthermore, aquaculture production is considered efficient in terms of feed conversation and protein retention compared with most terrestrial livestock [6.Fry J.P. et al.Feed conversion efficiency in aquaculture: do we measure it correctly?.Environ. Res. Lett. 2018; 13024017Crossref Scopus (76) Google Scholar], and seafood is the major source of long-chain polyunsaturated fatty acids, which are considered essential for human health [7.Rimm E.B. et al.Seafood long-chain n-3 polyunsaturated fatty acids and cardiovascular disease: a science advisory from the American Heart Association.Circulation. 2018; 138: e35-e47Crossref PubMed Scopus (215) Google Scholar]. However, relative to many crop and livestock production systems, most aquaculture is at a formative stage and is typically a high-risk activity. Sustainability can be hindered by an initial lack of control of the reproduction cycles of species, and periodic collapses due to infectious diseases. Upscaling and improving the reliability of production will require disruptive innovation in engineering, health, nutrition, and genetic improvement technologies, the latter being the focus of this review. Domestication and genetic improvement of terrestrial livestock has occurred for several millennia, with organized breeding programs for most species in place for >50 years. The results have been striking; for example, selective breeding has led to a threefold increase in efficiency of milk production in cows, with similar gains for other target traits [8.Van Eenennaam A.L. Genetic modification of food animals.Curr. Opin. Biotechnol. 2017; 44: 27-34Crossref PubMed Scopus (38) Google Scholar]. By contrast, relatively little aquaculture production is underpinned by modern selective breeding programs [9.Gjedrem T. et al.The importance of selective breeding in aquaculture to meet future demands for animal protein: a review.Aquaculture. 2012; 350–353: 117-129Crossref Scopus (346) Google Scholar, 10.Gjedrem T. Genetic improvement for the development of efficient global aquaculture: a personal opinion review.Aquaculture. 2012; 344–349: 12-22Crossref Scopus (134) Google Scholar]. Most farmed aquatic species are either still sourced from the wild or in the early stages of domestication, suggesting that there is substantial standing genetic variation for traits of economic importance. The reproductive biology of aquatic species can be amenable to the application of genetics and breeding technologies, enabling high selection intensity and, therefore, genetic gain. In part, this is due to the near-universal high fecundity of aquatic species, and the resulting large nuclear families, which can facilitate extensive collection of phenotypic records in close relatives (including full siblings) of selection candidates in breeding programs. The reproductive output from genetically improved broodstock (see Glossary) together with ease of transport of eggs and juveniles, also means widespread dissemination of improved stocks can have a rapid impact on production. Furthermore, with the development of high-density SNP arrays and routine genotyping by sequencing [11.Robledo D. et al.Applications of genotyping by sequencing in aquaculture breeding and genetics.Rev. Aquac. 2018; 10: 670-682Crossref PubMed Scopus (133) Google Scholar], genomic selection has become the state-of-the-art in several globally important aquaculture sectors, offering higher selection accuracies than selection based on phenotypic and pedigree records alone [12.Houston R.D. Future directions in breeding for disease resistance in aquaculture species.R. Bras. Zootec. 2017; 46: 545-551Crossref Google Scholar, 13.Zenger K.R. et al.Genomic selection in aquaculture: application, limitations and opportunities with special reference to marine shrimp and pearl oysters.Front. Genet. 2018; 9: 693Crossref PubMed Scopus (87) Google Scholar]. However, genetic progress in selective breeding is limited by the heritability of the target traits, the generation interval of the species, and the need to target multiple traits in the breeding goal. In addition, advanced breeding programs are typically closed systems, and are limited to the standing genetic variation in the broodstock (typically sourced from a limited sample of wild populations), and new variation that arises from de novo mutations. Genome-editing technologies, such as CRISPR/Cas9 (Box 1), offer new solutions and opportunities in each of these areas.Box 1Advances in Genome-Editing Technologies: CRISPR/Cas9 as the Game-ChangerIn contrast to transgenesis, which involves the transfer of a gene from one organism to another, genome editing allows specific, targeted, and often minor changes to the genome of the species of interest. Initial progress using transcription activator-like effector nucleases (TALENs) and zinc finger nucleases (ZFNs) [68.Zhang F. et al.Efficient construction of sequence-specific TAL effectors for modulating mammalian transcription.Nat. Biotechnol. 2011; 29: 149-153Crossref PubMed Scopus (600) Google Scholar, 70.Beerli R.R. Barbas 3rd, C.F. Engineering polydactyl zinc-finger transcription factors.Nat. Biotechnol. 2002; 20: 135-141Crossref PubMed Scopus (384) Google Scholar] has been largely superseded by the advent of the repurposed CRISPR/Cas9 system [71.Jinek M. et al.A programmable dual-RNA-guided DNA endonuclease in adaptive bacterial immunity.Science. 2012; 337: 816-821Crossref PubMed Scopus (8553) Google Scholar, 72.Mali P. et al.RNA-guided human genome engineering via Cas9.Science. 2013; 339: 823-826Crossref PubMed Scopus (6091) Google Scholar, 73.Cong L. et al.Multiplex genome engineering using CRISPR/Cas systems.Science. 2013; 339: 819-823Crossref PubMed Scopus (9381) Google Scholar]. The CRISPR/Cas9 system was discovered in bacteria, and was engineered to enable easy, cheap, and efficient targeted editing of the genome. The system creates a double-strand break (DSB) at a user-defined locus, enabling imperfect or targeted repair to create alterations to the sequence of the genomic DNA [74.Charpentier E. Doudna J.A. Biotechnology: Rewriting a genome.Nature. 2013; 495: 50-51Crossref PubMed Scopus (127) Google Scholar]. The platform functions by combining an endonuclease, the most commonly used enzyme derived from Streptococcus pyogenes (SpCas9), and an adapter RNA in two parts, the complementary RNA (crRNA) and the transactivating crRNA (tracrRNA). Once annealed, the crRNA recognizes the target DNA sequence, which requires the presence of a protospacer adjacent motif (PAM), and the tracrRNA binds the Cas9 protein to enable targeted endonuclease activity [71.Jinek M. et al.A programmable dual-RNA-guided DNA endonuclease in adaptive bacterial immunity.Science. 2012; 337: 816-821Crossref PubMed Scopus (8553) Google Scholar]. There are then are two primary repair mechanisms, each of which can be used to introduce different types of edit to the target genome. First, the two adjacent strands of DNA can be repaired through a nonhomologous end-joining pathway (NHEJ), which is error prone and induces insertion or deletions of a few nucleotides. Second, if a repair template is present, homology-directed repair (HDR) can be used to insert desired mutations (from a single nucleotide swap to a whole chromosomal region insertion) [72.Mali P. et al.RNA-guided human genome engineering via Cas9.Science. 2013; 339: 823-826Crossref PubMed Scopus (6091) Google Scholar, 75.Doudna J.A. Charpentier E. The new frontier of genome engineering with CRISPR-Cas9.Science. 2014; 346: 1258096Crossref PubMed Scopus (3299) Google Scholar].Over the past few years, technical developments have made genome editing more efficient, and raised new possibilities for biological discovery. Single guide RNA molecules (sgRNA) are routinely used instead of the crRNA and tracrRNA duplex to facilitate synthesis from a polymerase III promoter (U6) [72.Mali P. et al.RNA-guided human genome engineering via Cas9.Science. 2013; 339: 823-826Crossref PubMed Scopus (6091) Google Scholar], which simplifies the process of CRISPR/Cas9 delivery. There have also been numerous innovations that have enabled improved precision of editing, with lower off-target rates, and broadening of the range of target sites accessible via alternative Cas9 proteins (reviewed in [76.Komor A.C. et al.Programmable editing of a target base in genomic DNA without double-stranded DNA cleavage.Nature. 2016; 533: 420-424Crossref PubMed Scopus (2105) Google Scholar]). Novel extensions of the CRISPR/Cas9 editing system now allow researchers to achieve gene activation or inhibition, without DSBs by using a ‘dead’ Cas9 (dCas9) fused to activating (VP64, Rel A, and Rta proteins, known as the VPR system) or inhibiting complex (dCas9-KRAB) [77.Konermann S. et al.Genome-scale transcriptional activation by an engineered CRISPR-Cas9 complex.Nature. 2015; 517: 583-588Crossref PubMed Scopus (1533) Google Scholar, 78.Gilbert L.A. et al.CRISPR-mediated modular RNA-guided regulation of transcription in eukaryotes.Cell. 2013; 154: 442-451Abstract Full Text Full Text PDF PubMed Scopus (2100) Google Scholar, 79.Mali P. et al.CAS9 transcriptional activators for target specificity screening and paired nickases for cooperative genome engineering.Nat. Biotechnol. 2013; 31: 833-838Crossref PubMed Scopus (1244) Google Scholar]. Furthermore, swapping of base pairs (base-editing) from C to T with a cytidine deaminase [76.Komor A.C. et al.Programmable editing of a target base in genomic DNA without double-stranded DNA cleavage.Nature. 2016; 533: 420-424Crossref PubMed Scopus (2105) Google Scholar] and A to G with an adenine deaminase [80.Gaudelli N.M. et al.Programmable base editing of A•T to G•C in genomic DNA without DNA cleavage.Nature. 2017; 551: 464-471Crossref PubMed Scopus (1529) Google Scholar] using the same inactive Cas9 (dCas9) has the potential to target almost two-thirds of human SNPs [81.Koblan L.W. et al.Improving cytidine and adenine base editors by expression optimization and ancestral reconstruction.Nat. Biotechnol. 2018; 36: 843-846Crossref PubMed Scopus (314) Google Scholar]. In contrast to transgenesis, which involves the transfer of a gene from one organism to another, genome editing allows specific, targeted, and often minor changes to the genome of the species of interest. Initial progress using transcription activator-like effector nucleases (TALENs) and zinc finger nucleases (ZFNs) [68.Zhang F. et al.Efficient construction of sequence-specific TAL effectors for modulating mammalian transcription.Nat. Biotechnol. 2011; 29: 149-153Crossref PubMed Scopus (600) Google Scholar, 70.Beerli R.R. Barbas 3rd, C.F. Engineering polydactyl zinc-finger transcription factors.Nat. Biotechnol. 2002; 20: 135-141Crossref PubMed Scopus (384) Google Scholar] has been largely superseded by the advent of the repurposed CRISPR/Cas9 system [71.Jinek M. et al.A programmable dual-RNA-guided DNA endonuclease in adaptive bacterial immunity.Science. 2012; 337: 816-821Crossref PubMed Scopus (8553) Google Scholar, 72.Mali P. et al.RNA-guided human genome engineering via Cas9.Science. 2013; 339: 823-826Crossref PubMed Scopus (6091) Google Scholar, 73.Cong L. et al.Multiplex genome engineering using CRISPR/Cas systems.Science. 2013; 339: 819-823Crossref PubMed Scopus (9381) Google Scholar]. The CRISPR/Cas9 system was discovered in bacteria, and was engineered to enable easy, cheap, and efficient targeted editing of the genome. The system creates a double-strand break (DSB) at a user-defined locus, enabling imperfect or targeted repair to create alterations to the sequence of the genomic DNA [74.Charpentier E. Doudna J.A. Biotechnology: Rewriting a genome.Nature. 2013; 495: 50-51Crossref PubMed Scopus (127) Google Scholar]. The platform functions by combining an endonuclease, the most commonly used enzyme derived from Streptococcus pyogenes (SpCas9), and an adapter RNA in two parts, the complementary RNA (crRNA) and the transactivating crRNA (tracrRNA). Once annealed, the crRNA recognizes the target DNA sequence, which requires the presence of a protospacer adjacent motif (PAM), and the tracrRNA binds the Cas9 protein to enable targeted endonuclease activity [71.Jinek M. et al.A programmable dual-RNA-guided DNA endonuclease in adaptive bacterial immunity.Science. 2012; 337: 816-821Crossref PubMed Scopus (8553) Google Scholar]. There are then are two primary repair mechanisms, each of which can be used to introduce different types of edit to the target genome. First, the two adjacent strands of DNA can be repaired through a nonhomologous end-joining pathway (NHEJ), which is error prone and induces insertion or deletions of a few nucleotides. Second, if a repair template is present, homology-directed repair (HDR) can be used to insert desired mutations (from a single nucleotide swap to a whole chromosomal region insertion) [72.Mali P. et al.RNA-guided human genome engineering via Cas9.Science. 2013; 339: 823-826Crossref PubMed Scopus (6091) Google Scholar, 75.Doudna J.A. Charpentier E. The new frontier of genome engineering with CRISPR-Cas9.Science. 2014; 346: 1258096Crossref PubMed Scopus (3299) Google Scholar]. Over the past few years, technical developments have made genome editing more efficient, and raised new possibilities for biological discovery. Single guide RNA molecules (sgRNA) are routinely used instead of the crRNA and tracrRNA duplex to facilitate synthesis from a polymerase III promoter (U6) [72.Mali P. et al.RNA-guided human genome engineering via Cas9.Science. 2013; 339: 823-826Crossref PubMed Scopus (6091) Google Scholar], which simplifies the process of CRISPR/Cas9 delivery. There have also been numerous innovations that have enabled improved precision of editing, with lower off-target rates, and broadening of the range of target sites accessible via alternative Cas9 proteins (reviewed in [76.Komor A.C. et al.Programmable editing of a target base in genomic DNA without double-stranded DNA cleavage.Nature. 2016; 533: 420-424Crossref PubMed Scopus (2105) Google Scholar]). Novel extensions of the CRISPR/Cas9 editing system now allow researchers to achieve gene activation or inhibition, without DSBs by using a ‘dead’ Cas9 (dCas9) fused to activating (VP64, Rel A, and Rta proteins, known as the VPR system) or inhibiting complex (dCas9-KRAB) [77.Konermann S. et al.Genome-scale transcriptional activation by an engineered CRISPR-Cas9 complex.Nature. 2015; 517: 583-588Crossref PubMed Scopus (1533) Google Scholar, 78.Gilbert L.A. et al.CRISPR-mediated modular RNA-guided regulation of transcription in eukaryotes.Cell. 2013; 154: 442-451Abstract Full Text Full Text PDF PubMed Scopus (2100) Google Scholar, 79.Mali P. et al.CAS9 transcriptional activators for target specificity screening and paired nickases for cooperative genome engineering.Nat. Biotechnol. 2013; 31: 833-838Crossref PubMed Scopus (1244) Google Scholar]. Furthermore, swapping of base pairs (base-editing) from C to T with a cytidine deaminase [76.Komor A.C. et al.Programmable editing of a target base in genomic DNA without double-stranded DNA cleavage.Nature. 2016; 533: 420-424Crossref PubMed Scopus (2105) Google Scholar] and A to G with an adenine deaminase [80.Gaudelli N.M. et al.Programmable base editing of A•T to G•C in genomic DNA without DNA cleavage.Nature. 2017; 551: 464-471Crossref PubMed Scopus (1529) Google Scholar] using the same inactive Cas9 (dCas9) has the potential to target almost two-thirds of human SNPs [81.Koblan L.W. et al.Improving cytidine and adenine base editors by expression optimization and ancestral reconstruction.Nat. Biotechnol. 2018; 36: 843-846Crossref PubMed Scopus (314) Google Scholar]. Genome editing using CRISPR/Cas9 was recently successfully applied in vivo and/or in cell lines of several major aquaculture species of Salmonidae (Atlantic salmon, Salmo salar and rainbow trout, Oncorhynchus mykiss), Cyprinidae (Rohu, grass, and common carp, Labeo rohita, Ctenopharyngodon idella, and Cyprinus carpio, respectively), Siluridae (channel and southern catfish, Ictalurus punctatus), as well as Pacific oyster (Crassostrea gigas), Nile tilapia (Oreochromis niloticus), and gilthead sea bream (Sparus aurata) (Table 1 for details and references). One major group of aquatic species where successful CRISPR/Cas9 editing has not yet been reported is shrimp (Penaeus sp.), which may be partly due to practical limitations, as discussed briefly below. Most studies have a proof-of-principle focus, have typically followed CRISPR/Cas9 protocols developed in model organisms, such as zebrafish (Danio rerio) [35.Jao L.-E. et al.Efficient multiplex biallelic zebrafish genome editing using a CRISPR nuclease system.Proc. Natl. Acad. Sci. U. S. A. 2013; 110: 13904-13909Crossref PubMed Scopus (828) Google Scholar], and have often targeted genes with a clearly observable phenotype to test editing success (e.g., pigmentation). The standard methodology to induce in vivo mutations in aquaculture species is injection of the CRISPR/Cas9 complex into newly fertilized eggs as close as possible to the one-cell stage of development. Typically, mRNA encoding the Cas9 protein is injected together with the guide (g)RNA, leading to the high efficiency of editing demonstrated in various species to date (Table 1); using the Cas9 protein in place of mRNA is also effective [25.Khalil K. et al.Generation of myostatin gene-edited channel catfish (Ictalurus punctatus) via zygote injection of CRISPR/Cas9 system.Sci. Rep. 2017; 7: 7301Crossref PubMed Scopus (57) Google Scholar]. While most studies have used nonhomologous end joining (NHEJ) to induce mutations, homology-directed repair (HDR) has been successfully used to insert a template DNA in Rohu carp [30.Chakrapani V. et al.Establishing targeted carp TLR22 gene disruption via homologous recombination using CRISPR/Cas9.Dev. Comp. Immunol. 2016; 61: 242-247Crossref PubMed Scopus (45) Google Scholar]. Furthermore, successful germline transmission of edits has been reported in several of the studies to date (Table 1). Mosaicism is common in edited animals, implying that the Cas9-induced cutting and editing continues past the one-cell stage; this is an issue to tackle with future research (see Outstanding Questions).Table 1Successful Applications of CRISPR/Cas9 Genome Editing To Date in Aquaculture SpeciesSpeciesTarget geneaFull gene names: aldh1a2, aldehyde dehydrogenase family 1, subfamily A2; amhy, anti-Mullerian hormone; cyp26a1, cytochrome P450, family 26, subfamily a, polypeptide 1; dmrt1, doublesex and mab-3 related transcription factor 1; dmrt6, doublesex and mab-3 related transcription factor 6; dnd, dead end; elovl-2, ELOVL fatty acid elongase 2; foxl2, forkhead box L2; gcjam-a, grass carp junctional adhesion molecule-A; gsdf, gonadal somatic cell derived factor; igfbp-2b1/2b2, IGF binding protein 2b1/2b2; kctd10, potassium channel tetramerisation domain containing 10; LH, luteinizing hormone; mstn, myostatin; nanos2, nanos C2HC-type zinc finger 2; nanos3, nanos C2HC-type zinc finger 3; rbl, rhamnose binding lectin ; sf-1, steroidogenic factor 1; slc45a2, solute carrier family 45 member 2; soxe2 SRY-box transcription factor E2; sp7a/sp7b, transcription factor Sp7-like; ticam1, toll-like receptor adaptor molecule 1; TLR22, toll-like receptor 22; Tyr, tyrosinase; wee1, WEE1 G2 checkpoint kinase; wnt7b, wingless-type MMTV integration site family, member 7B; wt1a/b, Wilms tumor 1 transcription factor a/b.Trait of interestNotable featuresRefsAtlantic salmon, Salmo salartyr/slc45a2Pigmentation14.Edvardsen R.B. et al.Targeted mutagenesis in Atlantic salmon (Salmo salar L.) using the CRISPR/Cas9 system induces complete knockout individuals in the F0 Generation.PLoS One. 2014; 9e108622Crossref PubMed Scopus (109) Google ScholardndSterility15.Wargelius A. et al.Dnd knockout ablates germ cells and demonstrates germ cell independent sex differentiation in Atlantic salmon.Sci. Rep. 2016; 6: 21284Crossref PubMed Scopus (127) Google Scholarelov-2Omega-3 metabolism16.Datsomor A.K. et al.CRISPR/Cas9-mediated ablation of elovl2 in Atlantic salmon (Salmo salar L.) inhibits elongation of polyunsaturated fatty acids and induces Srebp-1 and target genes.Sci. Rep. 2019; 9: 7533Crossref PubMed Scopus (31) Google ScholarTilapia, Oreochromis niloticusdmrt1/nanaos2-3/foxl2ReproductionGermline transmission17.Li M.H. et al.Efficient and heritable gene targeting in tilapia by CRISPR/Cas9.Genetics. 2014; 197: 591-599Crossref PubMed Scopus (157) Google ScholargsdfReproduction18.Jiang D.N. et al.Gsdf is a downstream gene of dmrt1 that functions in the male sex determination pathway of the Nile tilapia.Mol. Reprod. Dev. 2016; 83: 497-508Crossref PubMed Scopus (81) Google Scholaraldh1a2/cyp26a1Reproduction19.Feng R. et al.Retinoic acid homeostasis through aldh1a2 and cyp26a1 mediates meiotic entry in Nile tilapia (Oreochromis niloticus).Sci. Rep. 2015; 5: 1-12Google Scholarsf-1ReproductionGermline transmission20.Xie Q.P. et al.Haploinsufficiency of SF-1 causes female to male sex reversal in Nile tilapia, Oreochromis niloticus.Endocrinology. 2016; 157: 2500-2514Crossref PubMed Scopus (38) Google Scholardmrt6Reproduction21.Zhang X. et al.Isolation of Doublesex- and Mab-3-related transcription factor 6 and its involvement in spermatogenesis in tilapia.Biol. Reprod. 2014; 91: 1-10Crossref Scopus (50) Google ScholaramhyReproduction22.Li M.H. et al.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 Genet. 2015; 11: 1-23Crossref Scopus (150) Google Scholarwt1a/wt1bReproduction23.Jiang D. et al.CRISPR/Cas9-induced disruption of wt1a and wt1b reveals their different roles in kidney and gonad development in Nile tilapia.Dev. Biol. 2017; 428: 63-73Crossref PubMed Scopus (27) Google ScholarSea bream, Sparus auratamstnGrowth24.Kishimoto K. et al.Production of a breed of red sea bream Pagrus major with an increase of skeletal muscle muss and reduced body length by genome editing with CRISPR/Cas9.Aquaculture. 2018; 495: 415-427Crossref Scopus (53) Google ScholarChannel catfish, Ictalarus punctatusmstnGrowthGermline transmission25.Khalil K. et al.Generation of myostatin gene-edited channel catfish (Ictalurus punctatus) via zygote injection of CRISPR/Cas9 system.Sci. Rep. 2017; 7: 7301Crossref PubMed Scopus (57) Google Scholarticam1/rblImmunity26.Elaswad A. et al.Effects of CRISPR/Cas9 dosage on TICAM1 and RBL gene mutation rate, embryonic development, hatchability and fry survival in channel catfish.Sci. Rep. 2018; 8: 16499Crossref PubMed Scopus (18) Google Scholar, 27.Qin Z. et al.Editing of the luteinizing hormone gene to sterilize Channel Catfish, ictalurus punctatus, using a modified zinc finger nuclease technology with electroporation.Mar. Biotechnol. (NY). 2016; 18: 255-263Crossref PubMed Scopus (32) Google ScholarLHSterilitySouthern catfish, Silurus meridionaliscyp26a1Germ cell development28.Li M.H. et al.Retinoic acid triggers meiosis initiation via stra8-dependent pathway in Southern catfish, Silurus meridionalis.Gen. Comp. Endocrinol. 2016; 232: 191-198Crossref PubMed Scopus (36) Google ScholarCommon carp, Cyprinus carpiosp7a/sp7b/mstn(ba)Muscle development29.Zhong Z. et al.Targeted disruption of sp7 and myostatin with CRISPR-Cas9 results in severe bone defects and more muscular cells in common carp.Sci. Rep. 2016; 6: 1-14PubMed Google ScholarRohu carp, Labeo rohitaTLR22ImmunityHomology-directed repair30.Chakrapani V. et al.Establishing targeted carp TLR22 gene disruption via homologous recombination using CRISPR/Cas9.Dev. Comp. Immunol. 2016; 61: 242-247Crossref PubMed Scopus (45) Google ScholarGrass carp, Ctenopharyngodon idellagcjam-aDisease resistanceIn vitro31.Ma J. et al.Efficient resistance to grass carp reovirus infection in JAM-A knockout cells using CRISPR/Cas9.Fish Shellfish Immunol. 2018; 76: 206-215Crossref PubMed Scopus (25) Google ScholarNorthern Chinese lamprey, Lethenteron moriislc24a5/kctd10/wee1/soxe2/wnt7bPigmentation/development32.Zu Y. et al.Biallelic editing of a lamprey genome using the CRISPR/Cas9 system.Sci. Rep. 2016; 6: 1-9Crossref PubMed Scopus (37) Google ScholarRainbow trout, Oncorhynchus mykissigfbp-2b1/2b2Growth33.Cleveland B.M. et al.Editing the duplicated insulin-like growth factor binding protein-2b gene in rainbow trout (Oncorhynchus mykiss).Sci. Rep. 2018; 8: 16054Crossref PubMed Scopus (30) Google ScholarPacific oyster, Crassostrea gigasmstnGrowth34.Yu H. et al.Targeted gene disruption in Pacific oyster based on CRISPR/Cas9 ribonucleoprotein complexes.Mar. Biotechnol. 2019; 23: 494-502Google Scholara Full gene names: aldh1a2, aldehyde dehydrogenase family 1, subfamily A2; amhy, anti-Mullerian hormone; cyp26a1, cytochrome P450, family 26, subfamily a, polypeptide 1; dmrt1, doublesex and mab-3 related transcription factor 1; dmrt6, doublesex and mab-3 related transcription factor 6; dnd, dead end; elovl-2, ELOVL fatty acid elongase 2; foxl2, forkhead box L2; gcjam-a, grass carp junctional adhesion molecule-A; gsdf, gonadal somatic cell derived factor; igfbp-2b1/2b2, IGF binding protein 2b1/2b2; kctd10, potassium channel tetramerisation domain containing 10; LH, luteinizing hormone; mstn, myostatin; nanos2, nanos C2HC-type zinc finger 2; nanos3, nanos C2HC-type zinc finger 3; rbl, rhamnose binding lectin ; sf-1, steroidogenic factor 1; slc45a2, solute carrier family 45 member 2; soxe2 SRY-box transcription factor E2; sp7a/sp7b, transcription factor Sp7-like; ticam1, toll-like receptor adaptor molecule 1; TLR22, toll-like receptor 22; Tyr, tyrosinase; wee1, WEE1 G2 checkpoint kinase; wnt7b, wingless-type MMTV" @default.
- W2964213295 created "2019-07-30" @default.
- W2964213295 creator A5005051455 @default.
- W2964213295 creator A5028235640 @default.
- W2964213295 creator A5060744496 @default.
- W2964213295 creator A5088964182 @default.
- W2964213295 date "2019-09-01" @default.
- W2964213295 modified "2023-10-17" @default.
- W2964213295 title "Potential of Genome Editing to Improve Aquaculture Breeding and Production" @default.
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- W2964213295 doi "https://doi.org/10.1016/j.tig.2019.06.006" @default.
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