Abstract
Livestock is an essential life commodity in modern agriculture involving breeding and maintenance. The farming practices have evolved mainly over the last century for commercial outputs, animal welfare, environment friendliness, and public health. Modifying genetic makeup of livestock has been proposed as an effective tool to create farmed animals with characteristics meeting modern farming system goals. The first technique used to produce transgenic farmed animals resulted in random transgene insertion and a low gene transfection rate. Therefore, genome manipulation technologies have been developed to enable efficient gene targeting with a higher accuracy and gene stability. Genome editing (GE) with engineered nucleases-Zinc finger nucleases (ZFNs) and transcription activator-like effector nucleases (TALENs) regulates the targeted genetic alterations to facilitate multiple genomic modifications through protein-DNA binding. The application of genome editors indicates usefulness in reproduction, animal models, transgenic animals, and cell lines. Recently, CRISPR/Cas system, an RNA-dependent genome editing tool (GET), is considered one of the most advanced and precise GE techniques for on-target modifications in the mammalian genome by mediating knock-in (KI) and knock-out (KO) of several genes. Lately, CRISPR/Cas9 tool has become the method of choice for genome alterations in livestock species due to its efficiency and specificity. The aim of this review is to discuss the evolution of engineered nucleases and GETs as a powerful tool for genome manipulation with special emphasis on its applications in improving economic traits and conferring resistance to infectious diseases of animals used for food production, by highlighting the recent trends for maintaining sustainable livestock production.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
Data availability
No new data were created or analyzed in this study. Data sharing is not applicable to this article.
References
Aida T, Chiyo K, Usami T et al (2015) Cloning-free CRISPR/Cas system facilitates functional cassette knock-in in mice. Genome Biol 16:87. https://doi.org/10.1186/s13059-015-0653-x
Antunes MS, Smith JJ, Jantz D, Medford JI (2012) Targeted DNA excision in Arabidopsis by a re-engineered homing endonuclease. BMC Biotechnol 12:86. https://doi.org/10.1186/1472-6750-12-86
Arnould S, Perez C, Cabaniols J-P et al (2007) Engineered I-CreI Derivatives Cleaving Sequences from the Human XPC Gene can Induce Highly Efficient Gene Correction in Mammalian Cells. J Mol Biol 371:49–65. https://doi.org/10.1016/j.jmb.2007.04.079
Bao J, Xie Q (2022) Artificial intelligence in animal farming: A systematic literature review. J Clean Prod 331:129956. https://doi.org/10.1016/j.jclepro.2021.129956
Bashir S, Dang T, Rossius J et al (2020) Enhancement of CRISPR-Cas9 induced precise gene editing by targeting histone H2A–K15 ubiquitination. BMC Biotechnol 20:57. https://doi.org/10.1186/s12896-020-00650-x
Bevacqua RJ, Fernandez-Martín R, Savy V et al (2016) Efficient edition of the bovine PRNP prion gene in somatic cells and IVF embryos using the CRISPR/Cas9 system. Theriogenology 86:1886-1896.e1. https://doi.org/10.1016/j.theriogenology.2016.06.010
Bhat SA, Malik AA, Ahmad SM et al (2017) Advances in genome editing for improved animal breeding: A review. Vet World 10:1361–1366. https://doi.org/10.14202/vetworld.2017.1361-1366
Bi H, Xie S, Cai C et al (2020) Frameshift mutation in myostatin gene by zinc-finger nucleases results in a significant increase in muscle mass in Meishan sows. Czech J Anim Sci 65(2020):182–191. https://doi.org/10.17221/265/2019-CJAS
Blix TB, Dalmo RA, Wargelius A, Myhr AI (2021) Genome editing on finfish: Current status and implications for sustainability. Rev Aquac 13:2344–2363. https://doi.org/10.1111/raq.12571
Capecchi MR (1989) Altering the genome by homologous recombination. Science 244:1288–1292. https://doi.org/10.1126/science.2660260
Carey K, Ryu J, Uh K et al (2019) Frequency of off-targeting in genome edited pigs produced via direct injection of the CRISPR/Cas9 system into developing embryos. BMC Biotechnol 19:25. https://doi.org/10.1186/s12896-019-0517-7
Carlson DF, Tan W, Lillico SG et al (2012) Efficient TALEN-mediated gene knockout in livestock. Proc Natl Acad Sci USA 109:17382–17387. https://doi.org/10.1073/pnas.1211446109
Carlson DF, Lancto CA, Zang B et al (2016) Production of hornless dairy cattle from genome-edited cell lines. Nat Biotechnol 34:479–481. https://doi.org/10.1038/nbt.3560
Carroll D (2017) Genome editing: Past, present, and future. Yale J Biol Med 90:653–659
Cavalu S, Damian G (2003) Rotational correlation times of 3-carbamoyl-2,2,5,5-tetramethyl-3-pyrrolin-1-yloxy spin label with respect to heme and nonheme proteins. Biomacromol 4:1630–1635. https://doi.org/10.1021/bm034093z
Chae C (2016) Porcine respiratory disease complex: Interaction of vaccination and porcine circovirus type 2, porcine reproductive and respiratory syndrome virus, and Mycoplasma hyopneumoniae. Vet J Lond Engl 212:1–6. https://doi.org/10.1016/j.tvjl.2015.10.030
Chakrapani V, Patra SK, Panda RP et al (2016) Establishing targeted carp TLR22 gene disruption via homologous recombination using CRISPR/Cas9. Dev Comp Immunol 61:242–247. https://doi.org/10.1016/j.dci.2016.04.009
Chapdelaine P, Pichavant C, Rousseau J et al (2010) Meganucleases can restore the reading frame of a mutated dystrophin. Gene Ther 17:846–858. https://doi.org/10.1038/gt.2010.26
Chen J, Wang H, Bai J et al (2019) Generation of pigs resistant to highly pathogenic-porcine reproductive and respiratory syndrome virus through gene editing of CD163. Int J Biol Sci 15:481–492. https://doi.org/10.7150/ijbs.25862
Chen D, Mechlowitz K, Li X et al (2021) Benefits and Risks of Smallholder Livestock Production on Child Nutrition in Low- and Middle-Income Countries. Front Nutr 8:751686
Cheng W, Zhao H, Yu H et al (2016) Efficient generation of GGTA1-null Diannan miniature pigs using TALENs combined with somatic cell nuclear transfer. Reprod Biol Endocrinol RBE 14:77. https://doi.org/10.1186/s12958-016-0212-7
Cho SW, Kim S, Kim Y et al (2014) Analysis of off-target effects of CRISPR/Cas-derived RNA-guided endonucleases and nickases. Genome Res 24:132–141. https://doi.org/10.1101/gr.162339.113
Choi W, Yum S, Lee S et al (2015) Disruption of exogenous eGFP gene using RNA-guided endonuclease in bovine transgenic somatic cells. Zygote Camb Engl 23:916–923. https://doi.org/10.1017/S096719941400063X
Chu VT, Weber T, Graf R et al (2016) Efficient generation of Rosa26 knock-in mice using CRISPR/Cas9 in C57BL/6 zygotes. BMC Biotechnol 16:4. https://doi.org/10.1186/s12896-016-0234-4
Cı̂ntã-Pı̂nzaru S, Cavalu S, Leopold N et al (2001) Raman and surface-enhanced Raman spectroscopy of tempyo spin labelled ovalbumin. J Mol Struct 565–566:225–229. https://doi.org/10.1016/S0022-2860(00)00930-3
Crispo M, Mulet AP, Tesson L et al (2015) Efficient generation of Myostatin knock-out sheep using CRISPR/Cas9 technology and microinjection into zygotes. PLoS ONE 10:e0136690. https://doi.org/10.1371/journal.pone.0136690
Datsomor AK, Olsen RE, Zic N et al (2019) CRISPR/Cas9-mediated editing of Δ5 and Δ6 desaturases impairs Δ8-desaturation and docosahexaenoic acid synthesis in Atlantic salmon (Salmo salar L.). Sci Rep 9:16888. https://doi.org/10.1038/s41598-019-53316-w
de Graeff N, Jongsma KR, Johnston J et al (2019) The ethics of genome editing in non-human animals: a systematic review of reasons reported in the academic literature. Philos Trans R Soc Lond B Biol Sci 374:20180106. https://doi.org/10.1098/rstb.2018.0106
Doench JG, Fusi N, Sullender M et al (2016) Optimized sgRNA design to maximize activity and minimize off-target effects of CRISPR-Cas9. Nat Biotechnol 34:184–191. https://doi.org/10.1038/nbt.3437
Dong Z, Ge J, Xu Z et al (2014) Generation of myostatin B knockout yellow catfish (Tachysurus fulvidraco) using transcription activator-like effector nucleases. Zebrafish 11:265–274. https://doi.org/10.1089/zeb.2014.0974
Dong J, Zhang N, Zhao P et al (2021) Disruption of dense granular Protein 2 (GRA2) decreases the Virulence of Neospora caninum. Front Vet Sci 8:634612. https://doi.org/10.3389/fvets.2021.634612
Doudna JA, Charpentier E (2014) Genome editing. The new frontier of genome engineering with CRISPR-Cas9. Science 346:1258096. https://doi.org/10.1126/science.1258096
Doyon Y, McCammon JM, Miller JC et al (2008) Heritable targeted gene disruption in Zebrafish using designed zinc finger nucleases. Nat Biotechnol 26:702–708. https://doi.org/10.1038/nbt1409
Elaswad A, Khalil K, Cline D et al (2018) Microinjection of CRISPR/Cas9 Protein into Channel Catfish, Ictalurus punctatus, Embryos for Gene Editing. J Vis Exp JoVE 56275. https://doi.org/10.3791/56275
Epinat J-C, Arnould S, Chames P et al (2003) A novel engineered meganuclease induces homologous recombination in yeast and mammalian cells. Nucleic Acids Res 31:2952–2962
Fan B, Huang P, Zheng S et al (2011) Assembly and in vitro functional analysis of zinc finger nuclease specific to the 3’ untranslated region of chicken ovalbumin gene. Anim Biotechnol 22:211–222. https://doi.org/10.1080/10495398.2011.626885
Fan J, Wang Y, Chen YE (2021) Genetically modified rabbits for cardiovascular research. Front Genet 12:14. https://doi.org/10.3389/fgene.2021.614379
Fu Y, Foden JA, Khayter C et al (2013) High frequency off-target mutagenesis induced by CRISPR-Cas nucleases in human cells. Nat Biotechnol 31:822–826. https://doi.org/10.1038/nbt.2623
Fu Y, Sander JD, Reyon D et al (2014) Improving CRISPR-Cas nuclease specificity using truncated guide RNAs. Nat Biotechnol 32:279–284. https://doi.org/10.1038/nbt.2808
Gaj T, Gersbach CA, Barbas CF (2013) ZFN, TALEN, and CRISPR/Cas-based methods for genome engineering. Trends Biotechnol 31:397–405. https://doi.org/10.1016/j.tibtech.2013.04.004
Gao Y, Wu H, Wang Y et al (2017) Single Cas9 nickase induced generation of NRAMP1 knockin cattle with reduced off-target effects. Genome Biol 18:13. https://doi.org/10.1186/s13059-016-1144-4
Garrood WT, Kranjc N, Petri K et al (2021) Analysis of off-target effects in CRISPR-based gene drives in the human malaria mosquito. Proc Natl Acad Sci 118. https://doi.org/10.1073/pnas.2004838117
Ge L, Kang J, Dong X et al (2021) Myostatin site-directed mutation and simultaneous PPARγ site-directed knockin in bovine genome. J Cell Physiol 236:2592–2605. https://doi.org/10.1002/jcp.30017
Gim G-M, Kwon D-H, Eom K-H et al (2021) Production of MSTN-mutated cattle without exogenous gene integration using CRISPR-Cas9. Biotechnol J e2100198. https://doi.org/10.1002/biot.202100198
Gratacap RL, Regan T, Dehler CE et al (2020) Efficient CRISPR/Cas9 genome editing in a salmonid fish cell line using a lentivirus delivery system. BMC Biotechnol 20:35. https://doi.org/10.1186/s12896-020-00626-x
Güralp H, Skaftnesmo KO, Kjærner-Semb E et al (2020) Rescue of germ cells in dnd crispant embryos opens the possibility to produce inherited sterility in Atlantic salmon. Sci Rep 10:18042. https://doi.org/10.1038/s41598-020-74876-2
Hai T, Teng F, Guo R et al (2014) One-step generation of knockout pigs by zygote injection of CRISPR/Cas system. Cell Res 24:372–375. https://doi.org/10.1038/cr.2014.11
Hallerman EM, Bredlau JP, Camargo LSA et al (2022) Towards progressive regulatory approaches for agricultural applications of animal biotechnology. Transgenic Res 31:167–199. https://doi.org/10.1007/s11248-021-00294-3
Han X, Gao Y, Li G et al (2020) Enhancing the antibacterial activities of sow milk via site-specific knock-in of a lactoferrin gene in pigs using CRISPR/Cas9 technology. Cell Biosci 10:133. https://doi.org/10.1186/s13578-020-00496-y
Hashem NM, González-Bulnes A, Rodriguez-Morales AJ (2020) Animal Welfare and livestock supply chain sustainability under the COVID-19 outbreak: An overview. Front Vet Sci 7:582528. https://doi.org/10.3389/fvets.2020.582528
Hauschild J, Petersen B, Santiago Y et al (2011) Efficient generation of a biallelic knockout in pigs using zinc-finger nucleases. Proc Natl Acad Sci USA 108:12013–12017. https://doi.org/10.1073/pnas.1106422108
Hennig SL, Owen JR, Lin JC et al (2020) Evaluation of mutation rates, mosaicism and off target mutations when injecting Cas9 mRNA or protein for genome editing of bovine embryos. Sci Rep 10:22309. https://doi.org/10.1038/s41598-020-78264-8
Heo YT, Quan X, Xu YN et al (2015) CRISPR/Cas9 nuclease-mediated gene knock-in in bovine-induced pluripotent cells. Stem Cells Dev 24:393–402. https://doi.org/10.1089/scd.2014.0278
Hiruta C, Ogino Y, Sakuma T et al (2014) Targeted gene disruption by use of transcription activator-like effector nuclease (TALEN) in the water flea Daphnia pulex. BMC Biotechnol 14:95. https://doi.org/10.1186/s12896-014-0095-7
Hsu PD, Lander ES, Zhang F (2014) Development and applications of CRISPR-Cas9 for genome engineering. Cell 157:1262–1278. https://doi.org/10.1016/j.cell.2014.05.010
Ikeda M, Matsuyama S, Akagi S et al (2017) Correction of a disease mutation using CRISPR/Cas9-assisted genome editing in Japanese Black Cattle. Sci Rep 7:17827. https://doi.org/10.1038/s41598-017-17968-w
Islam MdA, Rony SA, Rahman MB et al (2020) Improvement of disease resistance in livestock: Application of immunogenomics and CRISPR/Cas9 technology. Anim Open Access J MDPI 10:2236. https://doi.org/10.3390/ani10122236
Jeong Y-H, Kim YJ, Kim EY et al (2016) Knock-in fibroblasts and transgenic blastocysts for expression of human FGF2 in the bovine β-casein gene locus using CRISPR/Cas9 nuclease-mediated homologous recombination. Zygote Camb Engl 24:442–456. https://doi.org/10.1017/S0967199415000374
Jin YH, Liao B, Migaud H, Davie A (2020) Physiological impact and comparison of mutant screening methods in piwil2 KO founder Nile tilapia produced by CRISPR/Cas9 system. Sci Rep 10:12600. https://doi.org/10.1038/s41598-020-69421-0
Kadam US, Shelake RM, Chavhan RL, Suprasanna P (2018) Concerns regarding ‘off-target’ activity of genome editing endonucleases. Plant Physiol Biochem 131:22–30. https://doi.org/10.1016/j.plaphy.2018.03.027
Kaneko T, Sakuma T, Yamamoto T, Mashimo T (2014) Simple knockout by electroporation of engineered endonucleases into intact rat embryos. Sci Rep 4:6382. https://doi.org/10.1038/srep06382
Karavolias NG, Horner W, Abugu MN, Evanega SN (2021) Application of gene editing for climate change in agriculture. Front Sustain Food Syst 5:296. https://doi.org/10.3389/fsufs.2021.685801
Kc M, Steer CJ (2019) A new era of gene editing for the treatment of human diseases. Swiss Med Wkly 149:w20021. https://doi.org/10.4414/smw.2019.20021
Kim D, Bae S, Park J et al (2015) Digenome-seq: genome-wide profiling of CRISPR-Cas9 off-target effects in human cells. Nat Methods 12:237–243. https://doi.org/10.1038/nmeth.3284 (1 p following 243)
Kim GA, Lee EM, Jin J-X et al (2017) Generation of CMAHKO/GTKO/shTNFRI-Fc/HO-1 quadruple gene modified pigs. Transgenic Res 26:435–445. https://doi.org/10.1007/s11248-017-0021-6
Kiyonari H, Kaneko M, Abe T et al (2021) Targeted gene disruption in a marsupial, Monodelphis domestica, by CRISPR/Cas9 genome editing. Curr Biol 31:3956-3963.e4. https://doi.org/10.1016/j.cub.2021.06.056
Kosicki M, Tomberg K, Bradley A (2018) Repair of double-strand breaks induced by CRISPR–Cas9 leads to large deletions and complex rearrangements. Nat Biotechnol 36:765–771. https://doi.org/10.1038/nbt.4192
Koslová A, Trefil P, Mucksová J et al (2020) Precise CRISPR/Cas9 editing of the NHE1 gene renders chickens resistant to the J subgroup of avian leukosis virus. Proc Natl Acad Sci USA 117:2108–2112. https://doi.org/10.1073/pnas.1913827117
Kurtz S, Lucas-Hahn A, Schlegelberger B et al (2021) Knockout of the HMG domain of the porcine SRY gene causes sex reversal in gene-edited pigs. Proc Natl Acad Sci USA 118:e2008743118. https://doi.org/10.1073/pnas.2008743118
Landaeta-Hernández AJ, Zambrano-Nava S, Verde O et al (2021) Heat stress response in slick vs normal-haired Criollo Limonero heifers in a tropical environment. Trop Anim Health Prod 53:445. https://doi.org/10.1007/s11250-021-02856-3
Larson MH, Gilbert LA, Wang X et al (2013) CRISPR interference (CRISPRi) for sequence-specific control of gene expression. Nat Protoc 8:2180–2196. https://doi.org/10.1038/nprot.2013.132
Lei Y, Guo X, Liu Y et al (2012) Efficient targeted gene disruption in Xenopus embryos using engineered transcription activator-like effector nucleases (TALENs). Proc Natl Acad Sci USA 109:17484–17489. https://doi.org/10.1073/pnas.1215421109
Lewis CE, Pickering B (2022) Livestock and Risk Group 4 Pathogens: Researching Zoonotic Threats to Public Health and Agriculture in Maximum Containment. ILAR J 61:86–102. https://doi.org/10.1093/ilar/ilab029
Li M, Yang H, Zhao J et al (2014) Efficient and heritable gene targeting in tilapia by CRISPR/Cas9. Genetics 197:591–599. https://doi.org/10.1534/genetics.114.163667
Li HL, Fujimoto N, Sasakawa N et al (2015) Precise correction of the dystrophin gene in duchenne muscular dystrophy patient induced pluripotent stem cells by TALEN and CRISPR-Cas9. Stem Cell Rep 4:143–154. https://doi.org/10.1016/j.stemcr.2014.10.013
Li H, Yang Y, Hong W et al (2020) Applications of genome editing technology in the targeted therapy of human diseases: mechanisms, advances and prospects. Signal Transduct Target Ther 5:1. https://doi.org/10.1038/s41392-019-0089-y
Liang F, Han M, Romanienko PJ, Jasin M (1998) Homology-directed repair is a major double-strand break repair pathway in mammalian cells. Proc Natl Acad Sci USA 95:5172–5177
Lillico SG, Proudfoot C, King TJ et al (2016) Mammalian interspecies substitution of immune modulatory alleles by genome editing. Sci Rep 6:21645. https://doi.org/10.1038/srep21645
Liu X, Wang Y, Guo W et al (2013) Zinc-finger nickase-mediated insertion of the lysostaphin gene into the beta-casein locus in cloned cows. Nat Commun 4:2565. https://doi.org/10.1038/ncomms3565
Liu X, Wang Y, Tian Y et al (2014) Generation of mastitis resistance in cows by targeting human lysozyme gene to β-casein locus using zinc-finger nucleases. Proc Biol Sci 281:20133368. https://doi.org/10.1098/rspb.2013.3368
Liu X, Liu H, Wang M et al (2019) Disruption of the ZBED6 binding site in intron 3 of IGF2 by CRISPR/Cas9 leads to enhanced muscle development in Liang Guang Small Spotted pigs. Transgenic Res 28:141–150. https://doi.org/10.1007/s11248-018-0107-9
Looi FY, Baker ML, Townson T et al (2018) Creating disease resistant chickens: A viable solution to avian influenza? Viruses 10:E561. https://doi.org/10.3390/v10100561
Loureiro A, da Silva GJ (2019) CRISPR-Cas: Converting a bacterial defence mechanism into a state-of-the-art genetic manipulation tool. Antibiotics 8:18. https://doi.org/10.3390/antibiotics8010018
Luo J, Song Z, Yu S et al (2014) Efficient generation of myostatin (MSTN) biallelic mutations in cattle using zinc finger nucleases. PLoS ONE 9:e95225. https://doi.org/10.1371/journal.pone.0095225
Ma J, Fan Y, Zhou Y et al (2018) Efficient resistance to grass carp reovirus infection in JAM-A knockout cells using CRISPR/Cas9. Fish Shellfish Immunol 76:206–215. https://doi.org/10.1016/j.fsi.2018.02.039
Mashimo T, Kaneko T, Sakuma T et al (2013) Efficient gene targeting by TAL effector nucleases coinjected with exonucleases in zygotes. Sci Rep 3:1253. https://doi.org/10.1038/srep01253
Menchaca A, dos Santos-Neto PC, Souza-Neves M et al (2020) Otoferlin gene editing in sheep via CRISPR-assisted ssODN-mediated Homology Directed Repair. Sci Rep 10:5995. https://doi.org/10.1038/s41598-020-62879-y
Miao D, Giassetti MI, Ciccarelli M et al (2019) Simplified pipelines for genetic engineering of mammalian embryos by CRISPR-Cas9 electroporation†. Biol Reprod 101:177–187. https://doi.org/10.1093/biolre/ioz075
Mir TUG, Wani AK, Akhtar N, Shukla S (2022) CRISPR/Cas9: Regulations and challenges for law enforcement to combat its dual-use. Forensic Sci Int 334:111274. https://doi.org/10.1016/j.forsciint.2022.111274
Modrzejewski D, Hartung F, Lehnert H et al (2020) Which factors affect the occurrence of off-target effects caused by the use of CRISPR/Cas: A systematic review in plants. Front Plant Sci 11:1838. https://doi.org/10.3389/fpls.2020.574959
Moghaddassi S, Eyestone W, Bishop CE (2014) TALEN-Mediated modification of the bovine genome for large-scale production of human serum albumin. PLoS ONE 9:e89631. https://doi.org/10.1371/journal.pone.0089631
Morton J, Davis MW, Jorgensen EM, Carroll D (2006) Induction and repair of zinc-finger nuclease-targeted double-strand breaks in Caenorhabditis elegans somatic cells. Proc Natl Acad Sci USA 103:16370–16375. https://doi.org/10.1073/pnas.0605633103
Nagy A, Perrimon N, Sandmeyer S, Plasterk R (2003) Tailoring the genome: the power of genetic approaches. Nat Genet 33(Suppl):276–284. https://doi.org/10.1038/ng1115
Nakanishi T, Kato Y, Matsuura T, Watanabe H (2016) TALEN-mediated knock-in via non-homologous end joining in the crustacean Daphnia magna. Sci Rep 6:36252. https://doi.org/10.1038/srep36252
Nemudryi AA, Valetdinova KR, Medvedev SP, Zakian SM (2014) TALEN and CRISPR/Cas genome editing systems: Tools of discovery. Acta Naturae 6:19–40
Ni W, Qiao J, Hu S et al (2014) Efficient gene knockout in goats using CRISPR/Cas9 system. PLoS ONE 9:e106718. https://doi.org/10.1371/journal.pone.0106718
Niu Y, Shen B, Cui Y et al (2014) Generation of gene-modified cynomolgus monkey via Cas9/RNA-mediated gene targeting in one-cell embryos. Cell 156:836–843. https://doi.org/10.1016/j.cell.2014.01.027
Onasanya GO, Msalya GM, Thiruvenkadan AK et al (2020) Single nucleotide polymorphisms at heat shock protein 90 gene and their association with thermo-tolerance potential in selected indigenous Nigerian cattle. Trop Anim Health Prod 52:1961–1970. https://doi.org/10.1007/s11250-020-02222-9
Ou Z, Sun X (2016) Application of CRISPR-Cas9 genome editing for constructing animal models of human diseases. Zhonghua Yi Xue Yi Chuan Xue Za Zhi Zhonghua Yixue Yichuanxue Zazhi Chin J Med Genet 33:559–563. https://doi.org/10.3760/cma.j.issn.1003-9406.2016.04.030
Park K-E, Kaucher AV, Powell A et al (2017) Generation of germline ablated male pigs by CRISPR/Cas9 editing of the NANOS2 gene. Sci Rep 7:40176. https://doi.org/10.1038/srep40176
Pinzon-Arteaga C, Snyder MD, Lazzarotto CR et al (2020) Efficient correction of a deleterious point mutation in primary horse fibroblasts with CRISPR-Cas9. Sci Rep 10:7411. https://doi.org/10.1038/s41598-020-62723-3
Qi LS, Larson MH, Gilbert LA et al (2013) Repurposing CRISPR as an RNA-Guided platform for sequence-specific control of gene expression. Cell 152:1173–1183. https://doi.org/10.1016/j.cell.2013.02.022
Qian L, Tang M, Yang J et al (2015) Targeted mutations in myostatin by zinc-finger nucleases result in double-muscled phenotype in Meishan pigs. Sci Rep 5:14435. https://doi.org/10.1038/srep14435
Qin Z, Li Y, Su B et al (2016) Editing of the Luteinizing Hormone Gene to Sterilize Channel Catfish, Ictalurus punctatus, Using a Modified Zinc Finger Nuclease Technology with Electroporation. Mar Biotechnol N Y N 18:255–263. https://doi.org/10.1007/s10126-016-9687-7
Riordan SM, Heruth DP, Zhang LQ, Ye SQ (2015) Application of CRISPR/Cas9 for biomedical discoveries. Cell Biosci 5:33. https://doi.org/10.1186/s13578-015-0027-9
Rocha-Martins M, Cavalheiro GR, Matos-Rodrigues GE, Martins RAP (2015) From Gene Targeting to Genome Editing: Transgenic animals applications and beyond. An Acad Bras Cienc 87:1323–1348. https://doi.org/10.1590/0001-3765201520140710
Rouet P, Smih F, Jasin M (1994) Introduction of double-strand breaks into the genome of mouse cells by expression of a rare-cutting endonuclease. Mol Cell Biol 14:8096–8106. https://doi.org/10.1128/mcb.14.12.8096-8106.1994
Sakuma T, Ochiai H, Kaneko T et al (2013) Repeating pattern of non-RVD variations in DNA-binding modules enhances TALEN activity. Sci Rep 3:3379. https://doi.org/10.1038/srep03379
Sakuma T, Nakade S, Sakane Y et al (2016) MMEJ-assisted gene knock-in using TALENs and CRISPR-Cas9 with the PITCh systems. Nat Protoc 11:118–133. https://doi.org/10.1038/nprot.2015.140
Saleh-Gohari N, Helleday T (2004) Conservative homologous recombination preferentially repairs DNA double-strand breaks in the S phase of the cell cycle in human cells. Nucleic Acids Res 32:3683–3688. https://doi.org/10.1093/nar/gkh703
Sano A, Matsushita H, Wu H et al (2013) Physiological level production of antigen-specific human immunoglobulin in cloned transchromosomic cattle. PLoS ONE 8:e78119. https://doi.org/10.1371/journal.pone.0078119
Sato M, Miyoshi K, Nagao Y et al (2014) The combinational use of CRISPR/Cas9-based gene editing and targeted toxin technology enables efficient biallelic knockout of the α-1,3-galactosyltransferase gene in porcine embryonic fibroblasts. Xenotransplantation 21:291–300. https://doi.org/10.1111/xen.12089
Segev-Hadar A, Slosman T, Rozen A et al (2021) Genome editing using the CRISPR-Cas9 System to Generate a Solid-Red Germline of Nile Tilapia (Oreochromis niloticus). CRISPR J 4:583–594. https://doi.org/10.1089/crispr.2020.0115
Shandilya UK, Sharma A, Mallikarjunappa S et al (2021) CRISPR-Cas9-mediated knockout of TLR4 modulates Mycobacterium avium ssp. paratuberculosis cell lysate-induced inflammation in bovine mammary epithelial cells. J Dairy Sci 104:11135–11146. https://doi.org/10.3168/jds.2021-20305
Shanthalingam S, Tibary A, Beever JE et al (2016) Precise gene editing paves the way for derivation of Mannheimia haemolytica leukotoxin-resistant cattle. Proc Natl Acad Sci USA 113:13186–13190. https://doi.org/10.1073/pnas.1613428113
Sheets TP, Park C-H, Park K-E et al (2016) Somatic cell nuclear transfer followed by CRIPSR/Cas9 microinjection results in highly efficient genome editing in cloned pigs. Int J Mol Sci 17:2031. https://doi.org/10.3390/ijms17122031
Shen Y, Xu K, Yuan Z et al (2017) Efficient generation of P53 biallelic knockout Diannan miniature pigs via TALENs and somatic cell nuclear transfer. J Transl Med 15:224. https://doi.org/10.1186/s12967-017-1327-0
Silva G, Poirot L, Galetto R et al (2011) Meganucleases and other tools for targeted genome engineering: Perspectives and challenges for gene therapy. Curr Gene Ther 11:11–27. https://doi.org/10.2174/156652311794520111
Singh P, Ali SA (2021) Impact of CRISPR-Cas9-based genome engineering in farm animals. Vet Sci 8:122. https://doi.org/10.3390/vetsci8070122
Song J, Zhong J, Guo X et al (2013) Generation of RAG 1- and 2-deficient rabbits by embryo microinjection of TALENs. Cell Res 23:1059–1062. https://doi.org/10.1038/cr.2013.85
Straume AH, Kjærner-Semb E, Ove Skaftnesmo K et al (2020) Indel locations are determined by template polarity in highly efficient in vivo CRISPR/Cas9-mediated HDR in Atlantic salmon. Sci Rep 10:409. https://doi.org/10.1038/s41598-019-57295-w
Su X, Cui K, Du S et al (2018a) Efficient genome editing in cultured cells and embryos of Debao pig and swamp buffalo using the CRISPR/Cas9 system. In Vitro Cell Dev Biol Anim 54:375–383. https://doi.org/10.1007/s11626-018-0236-8
Su X, Wang S, Su G et al (2018b) Production of microhomologous-mediated site-specific integrated LacS gene cow using TALENs. Theriogenology 119:282–288. https://doi.org/10.1016/j.theriogenology.2018.07.011
Sun Z, Wang M, Han S et al (2018) Production of hypoallergenic milk from DNA-free beta-lactoglobulin (BLG) gene knockout cow using zinc-finger nucleases mRNA. Sci Rep 8:15430. https://doi.org/10.1038/s41598-018-32024-x
Sun Y, Zheng G-D, Nissa M et al (2020) Disruption of mstna and mstnb gene through CRISPR/Cas9 leads to elevated muscle mass in blunt snout bream (Megalobrama amblycephala). Aquaculture 528:735597. https://doi.org/10.1016/j.aquaculture.2020.735597
Sung YH, Baek I-J, Kim DH et al (2013) Knockout mice created by TALEN-mediated gene targeting. Nat Biotechnol 31:23–24. https://doi.org/10.1038/nbt.2477
Swarthout JT, Raisinghani M, Cui X (2011) Zinc Finger Nucleases: A new era for transgenic animals. Ann Neurosci 18:25–28. https://doi.org/10.5214/ans.0972.7531.1118109
Tait-Burkard C, Doeschl-Wilson A, McGrew MJ et al (2018) Livestock 2.0 - genome editing for fitter, healthier, and more productive farmed animals. Genome Biol 19:204. https://doi.org/10.1186/s13059-018-1583-1
Tang C, Zhang Q, Li X et al (2014) Targeted modification of CCR5 gene in rabbits by TALEN. Yi Chuan Hered 36:360–368
Tanihara F, Hirata M, Nguyen NT et al (2020) Efficient generation of GGTA1-deficient pigs by electroporation of the CRISPR/Cas9 system into in vitro-fertilized zygotes. BMC Biotechnol 20:40. https://doi.org/10.1186/s12896-020-00638-7
Tanihara F, Hirata M, Otoi T (2021) Current status of the application of gene editing in pigs. J Reprod Dev 67:177–187. https://doi.org/10.1262/jrd.2021-025
Taylor L, Carlson DF, Nandi S et al (2017) Efficient TALEN-mediated gene targeting of chicken primordial germ cells. Dev Camb Engl 144:928–934. https://doi.org/10.1242/dev.145367
United Nations World Population Prospects - Population Division - United Nations. https://population.un.org/wpp/. Accessed 15 Dec 2021
Van Eenennaam AL (2019) Application of genome editing in farm animals: cattle. Transgenic Res 28:93–100. https://doi.org/10.1007/s11248-019-00141-6
Vats P, Kaushik R, Rawat N et al (2021) Production of Transgenic Handmade Cloned Goat (Capra hircus) Embryos by Targeted Integration into Rosa 26 Locus Using Transcription Activator-like Effector Nucleases. Cell Reprogramming 23:250–262. https://doi.org/10.1089/cell.2021.0011
Veres A, Gosis BS, Ding Q et al (2014) Low incidence of off-target mutations in individual CRISPR-Cas9 and TALEN targeted human stem cell clones detected by whole-genome sequencing. Cell Stem Cell 15:27–30. https://doi.org/10.1016/j.stem.2014.04.020
Wang H, Yang H, Shivalila CS et al (2013) One-step generation of mice carrying mutations in multiple genes by CRISPR/Cas-mediated genome engineering. Cell 153:910–918. https://doi.org/10.1016/j.cell.2013.04.025
Wang X, Yu H, Lei A et al (2015) Generation of gene-modified goats targeting MSTN and FGF5 via zygote injection of CRISPR/Cas9 system. Sci Rep 5:13878. https://doi.org/10.1038/srep13878
Wang X, Cai B, Zhou J et al (2016) Disruption of FGF5 in Cashmere Goats Using CRISPR/Cas9 Results in More Secondary Hair Follicles and Longer Fibers. PLoS ONE 11:e0164640. https://doi.org/10.1371/journal.pone.0164640
Wang X, Liu J, Niu Y et al (2018) Low incidence of SNVs and indels in trio genomes of Cas9-mediated multiplex edited sheep. BMC Genomics 19:397. https://doi.org/10.1186/s12864-018-4712-z
Wang M, Sun Z, Ding F et al (2021) Efficient TALEN-mediated gene knockin at the bovine Y chromosome and generation of a sex-reversal bovine. Cell Mol Life Sci 78:5415–5425. https://doi.org/10.1007/s00018-021-03855-1
Wani AK, Akhtar N, Sher F et al (2022a) Microbial adaptation to different environmental conditions: molecular perspective of evolved genetic and cellular systems. Arch Microbiol 204:144. https://doi.org/10.1007/s00203-022-02757-5
Wani AK, Roy P, Kumar V, ul Gani Mir T (2022c) Metagenomics and artificial intelligence in the context of human health. Infect Genet Evol 100:105267. https://doi.org/10.1016/j.meegid.2022.105267
Wani AK, Hashem NM, Akhtar N et al (2022b) Understanding microbial networks of farm animals through genomics, metagenomics and other meta-omic approaches for livestock wellness and sustainability. Ann Anim Sci {"content-type":"ahead-of-print","content":0}: https://doi.org/10.2478/aoas-2022-0002
Wei Y-Y, Zhan Q-M, Zhu X-X et al (2020) Efficient CRISPR/Cas9-mediated gene editing in Guangdong small-ear spotted pig cells using an optimized electrotransfection method. Biotechnol Lett 42:2091–2109. https://doi.org/10.1007/s10529-020-02930-0
Weissmann A, Reitemeier S, Hahn A et al (2013) Sexing domestic chicken before hatch: A new method for in ovo gender identification. Theriogenology 80:199–205. https://doi.org/10.1016/j.theriogenology.2013.04.014
Wells KD, Bardot R, Whitworth KM et al (2017) Replacement of Porcine CD163 Scavenger Receptor Cysteine-Rich Domain 5 with a CD163-Like Homolog Confers Resistance of Pigs to Genotype 1 but Not Genotype 2 Porcine Reproductive and Respiratory Syndrome Virus. J Virol 91:e01521-e1616. https://doi.org/10.1128/JVI.01521-16
Whitworth KM, Lee K, Benne JA et al (2014) Use of the CRISPR/Cas9 system to produce genetically engineered pigs from in vitro-derived oocytes and embryos. Biol Reprod 91:78. https://doi.org/10.1095/biolreprod.114.121723
Whitworth KM, Rowland RRR, Ewen CL et al (2016) Gene-edited pigs are protected from porcine reproductive and respiratory syndrome virus. Nat Biotechnol 34:20–22. https://doi.org/10.1038/nbt.3434
Wiggans GR, Cole JB, Hubbard SM, Sonstegard TS (2017) Genomic Selection in Dairy Cattle: The USDA Experience. Annu Rev Anim Biosci 5:309–327. https://doi.org/10.1146/annurev-animal-021815-111422
Wu H, Wang Y, Zhang Y et al (2015) TALE nickase-mediated SP110 knockin endows cattle with increased resistance to tuberculosis. Proc Natl Acad Sci USA 112:E1530-1539. https://doi.org/10.1073/pnas.1421587112
Xie S, Zhang Y, Zhang L et al (2015) sgRNA design for the CRISPR/Cas9 system and evaluation of its off-target effects. Yi Chuan Hered 37:1125–1136. https://doi.org/10.16288/j.yczz.15-093
Xie Z, Jiao H, Xiao H et al (2020) Generation of pRSAD2 gene knock-in pig via CRISPR/Cas9 technology. Antiviral Res 174:104696. https://doi.org/10.1016/j.antiviral.2019.104696
Xiong K, Li S, Zhang H et al (2013) Targeted editing of goat genome with modular-assembly zinc finger nucleases based on activity prediction by computational molecular modeling. Mol Biol Rep 40:4251–4256. https://doi.org/10.1007/s11033-013-2507-5
Xu X, Cao X, Gao J (2019) Production of a mutant of large-scale loach Paramisgurnus dabryanus with skin pigmentation loss by genome editing with CRISPR/Cas9 system. Transgenic Res 28:341–356. https://doi.org/10.1007/s11248-019-00125-6
Xu K, Zhou Y, Mu Y et al (2020a) CD163 and pAPN double-knockout pigs are resistant to PRRSV and TGEV and exhibit decreased susceptibility to PDCoV while maintaining normal production performance. Elife 9:e57132. https://doi.org/10.7554/eLife.57132
Xu Y, Liu H, Pan H et al (2020b) CRISPR/Cas9-mediated Disruption of Fibroblast Growth Factor 5 in Rabbits Results in a Systemic Long Hair Phenotype by Prolonging Anagen. Genes 11:E297. https://doi.org/10.3390/genes11030297
Xu J, Zhang J, Yang D et al (2021) Gene editing in rabbits: Unique opportunities for translational biomedical research. Front Genet 12:1. https://doi.org/10.3389/fgene.2021.642444
Yang D, Zhang J, Xu J et al (2013) Production of Apolipoprotein C-III Knockout Rabbits using Zinc Finger Nucleases. J Vis Exp JoVE 50957. https://doi.org/10.3791/50957
Yang H, Wu Z (2018) Genome editing of pigs for agriculture and biomedicine. Front Genet 9:360. https://doi.org/10.3389/fgene.2018.00360
Yao J, Huang J, Hai T et al (2014) Efficient bi-allelic gene knockout and site-specific knock-in mediated by TALENs in pigs. Sci Rep 4:6926. https://doi.org/10.1038/srep06926
Yoon Y, Wang D, Tai PWL et al (2018) Streamlined ex vivo and in vivo genome editing in mouse embryos using recombinant adeno-associated viruses. Nat Commun 9:412. https://doi.org/10.1038/s41467-017-02706-7
Young SA, Aitken RJ, Ikawa M (2015) Advantages of using the CRISPR/Cas9 system of genome editing to investigate male reproductive mechanisms using mouse models. Asian J Androl 17:623–627. https://doi.org/10.4103/1008-682X.153851
Young AE, Mansour TA, McNabb BR et al (2020) Genomic and phenotypic analyses of six offspring of a genome-edited hornless bull. Nat Biotechnol 38:225–232. https://doi.org/10.1038/s41587-019-0266-0
Yu B, Lu R, Yuan Y et al (2016) Efficient TALEN-mediated myostatin gene editing in goats. BMC Dev Biol 16:26. https://doi.org/10.1186/s12861-016-0126-9
Zhang X, Wang L, Wu Y et al (2016) Knockout of Myostatin by Zinc-finger Nuclease in Sheep Fibroblasts and Embryos. Asian-Australas J Anim Sci 29:1500–1507. https://doi.org/10.5713/ajas.16.0130
Zhang X, Li W, Liu C et al (2017) Alteration of sheep coat color pattern by disruption of ASIP gene via CRISPR Cas9. Sci Rep 7:8149. https://doi.org/10.1038/s41598-017-08636-0
Zhang J, Cui M-L, Nie Y-W et al (2018) CRISPR/Cas9-mediated specific integration of fat-1 at the goat MSTN locus. FEBS J 285:2828–2839. https://doi.org/10.1111/febs.14520
Zhang H-X, Zhang Y, Yin H (2019) Genome editing with mRNA Encoding ZFN, TALEN, and Cas9. Mol Ther 27:735–746. https://doi.org/10.1016/j.ymthe.2019.01.014
Zhang L, Lu Q, Chang C (2020) Epigenetics in Health and Disease. Adv Exp Med Biol 1253:3–55. https://doi.org/10.1007/978-981-15-3449-2_1
Zhao X, Ni W, Chen C et al (2016) Targeted Editing of Myostatin Gene in Sheep by Transcription Activator-like Effector Nucleases. Asian-Australas J Anim Sci 29:413–418. https://doi.org/10.5713/ajas.15.0041
Zhao J, Lai L, Ji W, Zhou Q (2019) Genome editing in large animals: current status and future prospects. Natl Sci Rev 6:402–420. https://doi.org/10.1093/nsr/nwz013
Zhu B, Ge W (2018) Genome editing in fishes and their applications. Gen Comp Endocrinol 257:3–12. https://doi.org/10.1016/j.ygcen.2017.09.011
Zoppo M, Okoniewski N, Pantelyushin S et al (2021) A ribonucleoprotein transfection strategy for CRISPR/Cas9-mediated gene editing and single cell cloning in rainbow trout cells. Cell Biosci 11:103. https://doi.org/10.1186/s13578-021-00618-0
Zou Q, Wang X, Liu Y et al (2015) Generation of gene-target dogs using CRISPR/Cas9 system. J Mol Cell Biol 7:580–583. https://doi.org/10.1093/jmcb/mjv061
Acknowledgements
The authors are grateful to Mr. Tahir ul Gani Mir, Department of Forensic Science, Lovely Professional University, India for his help in the making of Figure 1 & 2. All figures were adapted or created using Biorender.com
Author information
Authors and Affiliations
Contributions
Conceptualization, A.K.W.and N.M.H; writing-original draft preparation, A.K.W., N.A., R.S., A.P., S.C., C.C., and N.M.H.; writing-review and editing. A.K.W., N.A., S.H.A.R, M.M., A.E. and N.M.H. All authors have read and agreed to the published version of the manuscript.
Corresponding author
Ethics declarations
Institutional review board statement
Not applicable.
Animal ethics
Not applicable.
Informed consent
Not applicable.
Conflicts of interest
The authors declare no conflict of interest.
Additional information
Publisher's note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Rights and permissions
About this article
Cite this article
Wani, A.K., Akhtar, N., Singh, R. et al. Genome centric engineering using ZFNs, TALENs and CRISPR-Cas9 systems for trait improvement and disease control in Animals. Vet Res Commun 47, 1–16 (2023). https://doi.org/10.1007/s11259-022-09967-8
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s11259-022-09967-8