Animal Reproduction (AR)
Animal Reproduction (AR)

Perspectives of gene editing for cattle farming in tropical and subtropical regions

Luiz Sergio Almeida Camargo; Naiara Zoccal Saraiva; Clara Slade Oliveira; Allie Carmickle; Diana Rangel Lemos; Luiz Gustavo Bruno Siqueira; Anna Carolina Denicol

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Cattle productivity in tropical and subtropical regions can be severely affected by the environment. Reproductive performance, milk and meat production are compromised by the heat stress imposed by the elevated temperature and humidity. The resulting low productivity contributes to reduce the farmer’s income and to increase the methane emissions per unit of animal protein produced and the pressure on land usage. The introduction of highly productive European cattle breeds as well as crossbreeding with local breeds have been adopted as strategies to increase productivity but the positive effects have been limited by the low adaptation of European animals to hot climates and by the reduction of the heterosis effect in the following generations. Gene editing tools allow precise modifications in the animal genome and can be an ally to the cattle industry in tropical and subtropical regions. Alleles associated with production or heat tolerance can be shifted between breeds without the need of crossbreeding. Alongside assisted reproductive biotechnologies and genome selection, gene editing can accelerate the genetic gain of indigenous breeds such as zebu cattle. This review focuses on some of the potential applications of gene editing for cattle farming in tropical and subtropical regions, bringing aspects related to heat stress, milk yield, bull reproduction and methane emissions.


genome editing, bovine, livestock, heat stress, CRISPR


Balcombe P, Speirs JF, Brandon NP, Hawkes AD. Methane emissions: choosing the right climate metric and time horizon. Environ Sci Process Impacts. 2018;20(10):1323-39. PMid:30255177.

Banos G, Woolliams JA, Woodward BW, Forbes AB, Coffey MP. Impact of single nucleotide polymorphisms in leptin, leptin receptor, growth hormone receptor, and Diacylglycerol Acyltransferase (DGAT1) gene loci on milk production, feed, and body energy traits of UK dairy cows. J Dairy Sci. 2008;91(8):3190-200. PMid:18650297.

Baruselli PS, Rodrigues CA, Ferreira RM, Sales JNS, Elliff FM, Silva LG, Viziack MP, Factor L, D’Occhio MJ. Impact of oocyte donor age and breed on in vitro embryo production in cattle, and relationship of dairy and beef embryo recipients on pregnancy and the subsequent performance of offspring: a review. Reprod Fertil Dev. 2021;34(2):36-51. PMid:35231233.

Bauman DE. Bovine somatotropin and lactation: from basic science to commercial application. Domest Anim Endocrinol. 1999;17(2-3):101-16. PMid:10527114.

Bharathi M, Senthil Kumar N, Chellapandi P. Functional prediction and assignment of methanobrevibacter ruminantium M1 operome using a combined bioinformatics approach. Front Genet. 2020;11:593990. PMid:33391347.

Bhattacharya A, Banu J, Rahman M, Causey J, Fernandes G. Biological effects of conjugated linoleic acids in health and disease. J Nutr Biochem. 2006;17(12):789-810. PMid:16650752.

Bhatt-Wessel B, Jordan TW, Miller JH, Peng L. Role of DGAT enzymes in triacylglycerol metabolism. Arch Biochem Biophys. 2018;655:1-11. PMid:30077544.

Black JL, Davison TM, Box I. Methane emissions from ruminants in Australia: mitigation potential and applicability of mitigation strategies. Animals. 2021;11(4):951. PMid:33805324.

Blott S, Kim J-J, Moisio S, Schmidt-Küntzel A, Cornet A, Berzi P, Cambisano N, Ford C, Grisart B, Johnson D, Karim L, Simon P, Snell R, Spelman R, Wong J, Vilkki J, Georges M, Farnir F, Coppieters W. Molecular dissection of a quantitative trait locus: a phenylalanine-to-tyrosine substitution in the transmembrane domain of the bovine growth hormone receptor is associated with a major effect on milk yield and composition. Genetics. 2003;163(1):253-66. PMid:12586713.

Bobbo T, Tiezzi F, Penasa M, De Marchi M, Cassandro M. Short communication: association analysis of diacylglycerol acyltransferase (DGAT1) mutation on chromosome 14 for milk yield and composition traits, somatic cell score, and coagulation properties in Holstein bulls. J Dairy Sci. 2018;101(9):8087-91. PMid:30007808.

Bohlouli M, Yin T, Hammami H, Gengler N, König S. Climate sensitivity of milk production traits and milk fatty acids in genotyped Holstein dairy cows. J Dairy Sci. 2021;104(6):6847-60. PMid:33714579.

Bouwman AC, Bovenhuis H, Visker MH, van Arendonk JA. Genome-wide association of milk fatty acids in Dutch dairy cattle. BMC Genet. 2011;12(1):43. PMid:21569316.

Bovenhuis H, Visker MHPW, Poulsen NA, Sehested J, van Valenberg HJF, van Arendonk JAM, Larsen LB, Buitenhuis AJ. Effects of the diacylglycerol o-acyltransferase 1 (DGAT1) K232A polymorphism on fatty acid, protein, and mineral composition of dairy cattle milk. J Dairy Sci. 2016;99(4):3113-23. PMid:26898284.

Bovenhuis H, Visker MHPW, van Valenberg HJF, Buitenhuis AJ, van Arendonk JAM. Effects of the DGAT1 polymorphism on test-day milk production traits throughout lactation. J Dairy Sci. 2015;98(9):6572-82. PMid:26142855.

Carmickle AT, Larson CC, Hernandez FS, Pereira JMV, Ferreira FC, Haimon MLJ, Jensen LM, Hansen PJ, Denicol AC. Physiological responses of Holstein calves and heifers carrying the SLICK1 allele to heat stress in California and Florida dairy farms. J Dairy Sci. 2022;105(11):9216-25. PMid:36114060.

Carroll D. Genome editing: past, present, and future. Yale J Biol Med. 2017;90(4):653-9. PMid:29259529.

Chang J, Peng S, Ciais P, Saunois M, Dangal SRS, Herrero M, Havlík P, Tian H, Bousquet P. Revisiting enteric methane emissions from domestic ruminants and their δ13CCH4 source signature. Nat Commun. 2019;10(1):3420. PMid:31366915.

Ciccarelli M, Giassetti MI, Miao D, Oatley MJ, Robbins C, Lopez-Biladeau B, Waqas MS, Tibary A, Whitelaw B, Lillico S, Park CH, Park KE, Telugu B, Fan Z, Liu Y, Regouski M, Polejaeva IA, Oatley JM. Donor-derived spermatogenesis following stem cell transplantation in sterile NANOS2 knockout males. Proc Natl Acad Sci USA. 2020;117(39):24195-204. PMid:32929012.

Clark LA, Thomson JM, Moore SS, Oba M. The effect of Ala293Val single nucleotide polymorphism in the stearoyl-CoA desaturase gene on conjugated linoleic acid concentration in milk fat of dairy cows. Can J Anim Sci. 2010;90(4):575-84.

Contreras-Correa Z, Peña-Alvarado N, Torres-Ruiz W, Almodóvar-Rivera J, Domenech-Pérez K, Youngblood C, Pagán-Morales M, Mesonero-Morales A, Curbelo-Rodríguez J, Randel-Follin PF, Muñiz-Colón GC, Colón-González V, Jiménez-Arroyo AL, Jiménez-Arroyo GM, Sánchez-Rodríguez HL. Slick-haired Puerto Rican Holstein cows have larger sweat glands than their wild type-haired counterparts. J Dairy Sci. 2017;100:M202.

Cooke RF, Daigle CL, Moriel P, Smith SB, Tedeschi LO, Vendramini JMB. Cattle adapted to tropical and subtropical environments: social, nutritional, and carcass quality considerations. J Anim Sci. 2020;98(2):skaa014. PMid:31955200.

DeFries R, Rosenzweig C. Toward a whole-landscape approach for sustainable land use in the tropics. Proc Natl Acad Sci USA. 2010;107(46):19627-32. PMid:21081701.

Demeter RM, Schopen GC, Lansink AG, Meuwissen MP, van Arendonk JA. Effects of milk fat composition, DGAT1, and SCD1 on fertility traits in Dutch Holstein cattle. J Dairy Sci. 2009;92(11):5720-9. PMid:19841232.

Deppenmeier U. The unique biochemistry of methanogenesis. Prog Nucleic Acid Res Mol Biol. 2002;71:223-83.

Dikmen S, Alava E, Pontes E, Fear JM, Dikmen BY, Olson TA, Hansen PJ. Differences in thermoregulatory ability between slick-haired and wild-type lactating holstein cows in response to acute heat stress. J Dairy Sci. 2008;91(9):3395-402. PMid:18765598.

Dikmen S, Khan FA, Huson HJ, Sonstegard TS, Moss JI, Dahl GE, Hansen PJ. The SLICK hair locus derived from Senepol cattle confers thermotolerance to intensively managed lactating Holstein cows. J Dairy Sci. 2014;97(9):5508-20. PMid:24996281.

Doudna JA, Charpentier E. The new frontier of genome engineering with CRISPR-Cas9. Science. 2014;346(6213):1258096.

Doudna JA. The promise and challenge of therapeutic genome editing. Nature. 2020;578(7794):229-36. PMid:32051598.

El-Nahas A. Variation in the Genetic Effects of ABCG2, Growth Hormone and Growth Hormone Receptor Gene Polymorphisms on Milk Production Traits in Egyptian Native, Holstein and Hybrid Cattle Populations. Pak Vet J. 2018;38(4):371-6.

Ferry JG. Biochemistry of Methanogenesis. Crit Rev Biochem Mol Biol. 1992;27(6):473-503. PMid:1473352.

Ferry JG. Fundamentals of methanogenic pathways that are key to the biomethanation of complex biomass. Curr Opin Biotechnol. 2011;22(3):351-7. PMid:21555213.

Flórez Murillo JM, Landaeta‐Hernández AJ, Kim E, Bostrom JR, Larson SA, Pérez O’Brien AM, Montero-Urdaneta MA, Garcia JF, Sonstegard TS. Three novel nonsense mutations of prolactin receptor found in heat‐tolerant Bos taurus breeds of the Caribbean Basin. Anim Genet. 2021;52(1):132-4. PMid:33259090.

Gaj T, Gersbach CA, Barbas CF 3rd. ZFN, TALEN, and CRISPR/Cas-based methods for genome engineering. Trends Biotechnol. 2013;31(7):397-405. PMid:23664777.

Gerber PJ, Steinfeld H, Henderson B, Mottet A, Opio C, Dijkman J, Falcucci A, Tempio G. Tackling climate change through livestock: a global assessment of emissions and mitigation opportunities. Rome: Food and Agriculture Organization of the United Nations; 2013.

Giassetti MI, Ciccarelli M, Oatley JM. Spermatogonial stem cell transplantation: insights and outlook for domestic animals. Annu Rev Anim Biosci. 2019;7(1):385-401. PMid:30762440.

Grisart B, Coppieters W, Farnir F, Karim L, Ford C, Berzi P, Cambisano N, Mni M, Reid S, Simon P, Spelman R, Georges M, Snell R. Positional candidate cloning of a QTL in dairy cattle: identification of a missense mutation in the bovine DGAT1 gene with major effect on milk yield and composition. Genome Res. 2002;12(2):222-31. PMid:11827942.

Hammond AC, Olson TA, Chase CC Jr, Bowers EJ, Randel RD, Murphy CN, Vogt DW, Tewolde A. Heat tolerance in two tropically adapted Bos taurus breeds, Senepol and Romosinuano, compared with Brahman, Angus, and Hereford cattle in Florida. J Anim Sci. 1996;74(2):295-303. PMid:8690664.

Hansen PJ. Prospects for gene introgression or gene editing as a strategy for reduction of the impact of heat stress on production and reproduction in cattle. Theriogenology. 2020;154:190-202. PMid:32622199.

Henderson G, Cox F, Ganesh S, Jonker A, Young W, Abecia L, Angarita E, Aravena P, Nora Arenas G, Ariza C, Attwood GT, Mauricio Avila J, Avila-Stagno J, Bannink A, Barahona R, Batistotti M, Bertelsen MF, Brown-Kav A, Carvajal AM, Cersosimo L, Vieira Chaves A, Church J, Clipson N, Cobos-Peralta MA, Cookson AL, Cravero S, Cristobal Carballo O, Crosley K, Cruz G, Cerón Cucchi M, de la Barra R, De Menezes AB, Detmann E, Dieho K, Dijkstra J, dos Reis WLS, Dugan MER, Hadi Ebrahimi S, Eythórsdóttir E, Nde Fon F, Fraga M, Franco F, Friedeman C, Fukuma N, Gagić D, Gangnat I, Javier Grilli D, Guan LL, Heidarian Miri V, Hernandez-Sanabria E, Gomez AXI, Isah OA, Ishaq S, Jami E, Jelincic J, Kantanen J, Kelly WJ, Kim S-H, Klieve A, Kobayashi Y, Koike S, Kopecny J, Nygaard Kristensen T, Julie Krizsan S, LaChance H, Lachman M, Lamberson WR, Lambie S, Lassen J, Leahy SC, Lee S-S, Leiber F, Lewis E, Lin B, Lira R, Lund P, Macipe E, Mamuad LL, Cuquetto Mantovani H, Marcoppido GA, Márquez C, Martin C, Martinez G, Eugenia Martinez M, Lucía Mayorga O, McAllister TA, McSweeney C, Mestre L, Minnee E, Mitsumori M, Mizrahi I, Molina I, Muenger A, Muñoz C, Murovec B, Newbold J, Nsereko V, O’Donovan M, Okunade S, O’Neill B, Ospina S, Ouwerkerk D, Parra D, Pereira LGR, Pinares-Patiño C, Pope PB, Poulsen M, Rodehutscord M, Rodriguez T, Saito K, Sales F, Sauer C, Shingfield K, Shoji N, Simunek J, Stojanović-Radić Z, Stres B, Sun X, Swartz J, Liang Tan Z, Tapio I, Taxis TM, Tomkins N, Ungerfeld E, Valizadeh R, van Adrichem P, Van Hamme J, Van Hoven W, Waghorn G, John Wallace R, Wang M, Waters SM, Keogh K, Witzig M, Wright A-DG, Yamano H, Yan T, Yáñez-Ruiz DR, Yeoman CJ, Zambrano R, Zeitz J, Zhou M, Wei Zhou H, Xia Zou C, Zunino P, Janssen PH. Rumen microbial community composition varies with diet and host, but a core microbiome is found across a wide geographical range. Sci Rep. 2015;5(1):14567. PMid:26449758.

Hickey JM, Bruce C, Whitelaw A, Gorjanc G. Promotion of alleles by genome editing in livestock breeding programmes. J Anim Breed Genet. 2016;133(2):83-4. PMid:26995217.

Houaga I, Muigai AWT, Ng’ang’a FM, Ibeagha-Awemu EM, Kyallo M, Youssao IAK, Stomeo F. Milk fatty acid variability and association with polymorphisms in SCD1 and DGAT1 genes in White Fulani and Borgou cattle breeds. Mol Biol Rep. 2018;45(6):1849-62. PMid:30168097.

Jacobs AAA, Dijkstra J, Hendriks WH, van Baal J, van Vuuren AM. Comparison between stearoyl-CoA desaturase expression in milk somatic cells and in mammary tissue of lactating dairy cows. J Anim Physiol Anim Nutr. 2013;97(2):353-62. PMid:22369625.

Jenko J, Gorjanc G, Cleveland MA, Varshney RK, Whitelaw CBA, Woolliams JA, Hickey JM. Potential of promotion of alleles by genome editing to improve quantitative traits in livestock breeding programs. Genet Sel Evol. 2015;47(1):55. PMid:26133579.

Johnson KA, Johnson DE. Methane emissions from cattle. J Anim Sci. 1995;73(8):2483-92. PMid:8567486.

Jonas E, Koning D-J. Genomic selection needs to be carefully assessed to meet specific requirements in livestock breeding programs. Front Genet. 2015;6:49. PMid:25750652.

Jones HD. Future of breeding by genome editing is in the hands of regulators. GM Crops Food. 2015;6(4):223-32. PMid:26930115.

Jones MGK, Fosu-Nyarko J, Iqbal S, Adeel M, Romero-Aldemita R, Arujanan M, Kasai M, Wei X, Prasetya B, Nugroho S, Mewett O, Mansoor S, Awan MJA, Ordonio RL, Rao SR, Poddar A, Hundleby P, Iamsupasit N, Khoo K. Enabling Trade in gene-edited produce in Asia and Australasia: the developing regulatory landscape and future perspectives. Plants. 2022;11(19):2538.

Kęsek-Woźniak MM, Wojtas E, Zielak-Steciwko AE. Impact of SNPs in ACACA, SCD1, and DGAT1 genes on fatty acid profile in bovine milk with regard to lactation phases. Animals. 2020;10(6):997. PMid:32521715.

Kgwatalala PM, Ibeagha-Awemu EM, Hayes JF, Zhao X. Single nucleotide polymorphisms in the open reading frame of the stearoyl-CoA desaturase gene and resulting genetic variants in Canadian Holstein and Jersey cows. DNA Seq. 2007;18(5):357-62. PMid:17654011.

Kim H, Kim J-S. A guide to genome engineering with programmable nucleases. Nat Rev Genet. 2014;15(5):321-34. PMid:24690881.

Lacorte GA, Machado MA, Martinez ML, Campos AL, Maciel RP, Verneque RS, Teodoro RL, Peixoto MG, Carvalho MR, Fonseca CG. DGAT1 K232A polymorphism in Brazilian cattle breeds. Genet Mol Res. 2006;5(3):475-82. PMid:17117362.

Lamas‐Toranzo I, Martínez‐Moro A, O’Callaghan E, Millán‐Blanca G, Sánchez JM, Lonergan P, Bermejo-Álvarez P. RS‐1 enhances CRISPR‐mediated targeted knock‐in in bovine embryos. Mol Reprod Dev. 2020;87(5):542-9. PMid:32227559.

Landaeta-Hernández A, Zambrano-Nava S, Hernández-Fonseca JP, Godoy R, Calles M, Iragorri JL, Añez L, Polanco M, Montero-Urdaneta M, Olson T. Variability of hair coat and skin traits as related to adaptation in Criollo Limonero cattle. Trop Anim Health Prod. 2011;43(3):657-63. PMid:21104126.

Landaeta-Hernández AJ, Zambrano-Nava S, Verde O, Pinto-Santini L, Montero-Urdaneta M, Hernández-Fonseca JP, Fuenmayor-Morales C, Sonstegard TS, Huson HJ, Olson TA. Heat stress response in slick vs normal-haired Criollo Limonero heifers in a tropical environment. Trop Anim Health Prod. 2021;53(4):445. PMid:34427775.

Leahy SC, Kelly WJ, Altermann E, Ronimus RS, Yeoman CJ, Pacheco DM, Li D, Kong Z, McTavish S, Sang C, Lambie SC, Janssen PH, Dey D, Attwood GT. The genome sequence of the rumen methanogen methanobrevibacter ruminantium reveals new possibilities for controlling ruminant methane emissions. PLoS One. 2010;5(1):e8926. PMid:20126622.

Lee H, Park WJ. Unsaturated fatty acids, desaturases, and human health. J Med Food. 2014;17(2):189-97. PMid:24460221.

Li G, Zhang X, Zhong C, Mo J, Quan R, Yang J, Liu D, Li Z, Yang H, Wu Z. Small molecules enhance CRISPR/Cas9-mediated homology-directed genome editing in primary cells. Sci Rep. 2017;7(1):8943. PMid:28827551.

Li Y, Pan S, Zhang Y, Ren M, Feng M, Peng N, Chen L, Liang YX, She Q. Harnessing Type I and Type III CRISPR-Cas systems for genome editing. Nucleic Acids Res. 2016;44(4):e34. PMid:26467477.

Li Y, Peng N. Endogenous CRISPR-Cas system-based genome editing and antimicrobials: review and prospects. Front Microbiol. 2019;10:2471. PMid:31708910.

Littlejohn MD, Henty KM, Tiplady K, Johnson T, Harland C, Lopdell T, Sherlock RG, Li W, Lukefahr SD, Shanks BC, Garrick DJ, Snell RG, Spelman RJ, Davis SR. Functionally reciprocal mutations of the prolactin signalling pathway define hairy and slick cattle. Nat Commun. 2014;5(1):5861. PMid:25519203.

Liu M, Rehman S, Tang X, Gu K, Fan Q, Chen D, Ma W. Methodologies for Improving HDR Efficiency. Front Genet. 2019;9:691. PMid:30687381.

Liu Z, Ezernieks V, Wang J, Arachchillage NW, Garner JB, Wales WJ, Cocks BG, Rochfort S. Heat Stress in Dairy Cattle Alters Lipid Composition of Milk. Sci Rep. 2017;7(1):961. PMid:28424507.

Lu J, Boeren S, van Hooijdonk T, Vervoort J, Hettinga K. Effect of the DGAT1 K232A genotype of dairy cows on the milk metabolome and proteome. J Dairy Sci. 2015;98(5):3460-9. PMid:25771043.

Manteca X, Smith AJ. Effects of poor forage conditions on the behaviour of grazing ruminants. Trop Anim Health Prod. 1994;26(3):129-38. PMid:7809984.

Maruyama T, Dougan SK, Truttmann MC, Bilate AM, Ingram JR, Ploegh HL. Increasing the efficiency of precise genome editing with CRISPR-Cas9 by inhibition of nonhomologous end joining. Nat Biotechnol. 2015;33(5):538-42. PMid:25798939.

Mele M, Conte G, Castiglioni B, Chessa S, Macciotta NPP, Serra A, Buccioni A, Pagnacco G, Secchiari P. Stearoyl-coenzyme A desaturase gene polymorphism and milk fatty acid composition in Italian holsteins. J Dairy Sci. 2007;90(9):4458-65. PMid:17699067.

Miranda J, Freitas A. Raças e tipos de cruzamento para produção de leite. Juiz de Fora: Embrapa; 2009.

Mishra SR. Behavioural, physiological, neuro-endocrine and molecular responses of cattle against heat stress: an updated review. Trop Anim Health Prod. 2021;53(3):400. PMid:34255188.

Molla KA, Sretenovic S, Bansal KC, Qi Y. Precise plant genome editing using base editors and prime editors. Nat Plants. 2021;7(9):1166-87. PMid:34518669.

Morrell JM. Heat stress and bull fertility. Theriogenology. 2020;153:62-7. PMid:32442741.

Mueller ML, Van Eenennaam AL. Synergistic power of genomic selection, assisted reproductive technologies, and gene editing to drive genetic improvement of cattle. CABI Agric Biosci. 2022;3(1):13.

Muñiz-Cruz J, Peña-Alvarado N, Torres-Ruiz W, Almodóvar-Rivera J, Domenech-Pérez K, Contreras-Correa Z, Muñiz-Colón GC, Cortés-Arocho AC, Santiago-Rodríguez JM, Ruiz-Ríos S, Soriano-Varela GA, Cortés-Viruet NN, Jiménez-Arroyo AL, Jiménez-Arroyo GM, Sánchez-Rodríguez HL. Sweat gland cross-sectional cut areas comparisons between slick and wild type-haired Holstein and Senepol cows in Puerto Rico. J Dairy Sci. 2018;101:T162.

Näslund J, Fikse WF, Pielberg GR, Lundén A. Frequency and Effect of the bovine Acyl-CoA:Diacylglycerol Acyltransferase 1 (DGAT1) K232A polymorphism in Swedish dairy cattle. J Dairy Sci. 2008;91(5):2127-34. PMid:18420644.

Nayak DD, Metcalf WW. Cas9-mediated genome editing in the methanogenic archaeon Methanosarcina acetivorans. Proc Natl Acad Sci USA. 2017;114(11):2976-81. PMid:28265068.

Ntambi J, Miyazaki M. Regulation of stearoyl-CoA desaturases and role in metabolism. Prog Lipid Res. 2004;43(2):91-104. PMid:14654089.

Olson TA, Lucena C, Chase CC Jr, Hammond AC. Evidence of a major gene influencing hair length and heat tolerance in Bos taurus cattle. J Anim Sci. 2003;81(1):80-90. PMid:12597376.

Oosting SJ, Udo HMJ, Viets TC. Development of livestock production in the tropics: farm and farmers’ perspectives. Animal. 2014;8(8):1238-48. PMid:24673769.

Paquet D, Kwart D, Chen A, Sproul A, Jacob S, Teo S, Olsen KM, Gregg A, Noggle S, Tessier-Lavigne M. Efficient introduction of specific homozygous and heterozygous mutations using CRISPR/Cas9. Nature. 2016;533(7601):125-9. PMid:27120160.

Park K-E, Kaucher AV, Powell A, Waqas MS, Sandmaier SES, Oatley MJ, Park CH, Tibary A, Donovan DM, Blomberg LA, Lillico SG, Whitelaw CB, Mileham A, Telugu BP, Oatley JM. Generation of germline ablated male pigs by CRISPR/Cas9 editing of the NANOS2 gene. Sci Rep. 2017;7(1):40176. PMid:28071690.

Paton CM, Ntambi JM. Biochemical and physiological function of stearoyl-CoA desaturase. Am J Physiol Endocrinol Metab. 2009;297(1):E28-37. PMid:19066317.

Penev T, Naydenova N, Dimov D, Marinov I. Influence of heat stress and physiological indicators related to it on health lipid indices in milk of holstein-friesian cows. J Oleo Sci. 2021;70(6):745-55. PMid:33967167.

Porto-Neto LR, Bickhart DM, Landaeta-Hernandez AJ, Utsunomiya YT, Pagan M, Jimenez E, Hansen PJ, Dikmen S, Schroeder SG, Kim ES, Sun J, Crespo E, Amati N, Cole JB, Null DJ, Garcia JF, Reverter A, Barendse W, Sonstegard TS. Convergent evolution of slick coat in cattle through truncation mutations in the prolactin receptor. Front Genet. 2018;9:57. PMid:29527221.

Rahman MB, Schellander K, Luceño NL, Van Soom A. Heat stress responses in spermatozoa: mechanisms and consequences for cattle fertility. Theriogenology. 2018;113:102-12. PMid:29477908.

Rahmatalla SA, Müller U, Strucken EM, Reissmann M, Brockmann GA. The F279Y polymorphism of the GHR gene and its relation to milk production and somatic cell score in German Holstein dairy cattle. J Appl Genet. 2011;52(4):459-65. PMid:21660490.

Ramesha K, Rao A, Basavaraju M, Geetha G, Kataktalware M, Jeyakumar S. Genetic variability of bovine GHR, IGF-1 and IGFBP-3 genes in Indian cattle and buffalo. S Afr J Anim Sci. 2016;45(5):485.

Reynolds CM, Roche HM. Conjugated linoleic acid and inflammatory cell signalling. Prostaglandins Leukot Essent Fatty Acids. 2010;82(4-6):199-204. PMid:20207526.

Ryu S-M, Hur JW, Kim K. Evolution of CRISPR towards accurate and efficient mammal genome engineering. BMB Rep. 2019;52(8):475-81. PMid:31234957.

Sada A, Suzuki A, Suzuki H, Saga Y. The RNA-binding protein NANOS2 is required to maintain murine spermatogonial stem cells. Science. 2009;325(5946):1394-8.

Sánchez-Rodríguez HL, Domenech-Pérez K. Light sensors assess solar radiation vs. shade exposure of slick- and wild-type Puerto Rican Holstein cows. J Agric Univ P R. 2021;105(1):39-48.

Santos MM, Souza-Junior JBF, Dantas MRT, de Macedo Costa LL. An updated review on cattle thermoregulation: physiological responses, biophysical mechanisms, and heat stress alleviation pathways. Environ Sci Pollut Res Int. 2021;28(24):30471-85. PMid:33895955.

Schennink A, Heck JML, Bovenhuis H, Visker MHPW, van Valenberg HJF, van Arendonk JAM. Milk fatty acid unsaturation: genetic parameters and effects of Stearoyl-CoA Desaturase (SCD1) and Acyl CoA: Diacylglycerol Acyltransferase 1 (DGAT1). J Dairy Sci. 2008;91(5):2135-43. PMid:18420645.

Schubert MS, Thommandru B, Woodley J, Turk R, Yan S, Kurgan G, McNeill MS, Rettig GR. Optimized design parameters for CRISPR Cas9 and Cas12a homology-directed repair. Sci Rep. 2021;11(1):19482. PMid:34593942.

Shen R, Xie T. NANOS: a germline stem cell’s guardian angel. J Mol Cell Biol. 2010;2(2):76-7. PMid:20008335.

Shi W, Moon CD, Leahy SC, Kang D, Froula J, Kittelmann S, Fan C, Deutsch S, Gagic D, Seedorf H, Kelly WJ, Atua R, Sang C, Soni P, Li D, Pinares-Patiño CS, McEwan JC, Janssen PH, Chen F, Visel A, Wang Z, Attwood GT, Rubin EM. Methane yield phenotypes linked to differential gene expression in the sheep rumen microbiome. Genome Res. 2014;24(9):1517-25. PMid:24907284.

Shima S, Warkentin E, Thauer RK, Ermler U. Structure and function of enzymes involved in the methanogenic pathway utilizing carbon dioxide and molecular hydrogen. J Biosci Bioeng. 2002;93(6):519-30. PMid:16233244.

Shyma KP, Gupta JP, Singh V. Breeding strategies for tick resistance in tropical cattle: a sustainable approach for tick control. J Parasit Dis. 2015;39(1):1-6. PMid:25698850.

Silva MO, Borges MS, Fernandes LG, Rodrigues NN, Watanabe YF, Joaquim DC, Oliveira CS, da Feuchard VLS, Dos Cyrillo JNSG, Mercadante MEZ, Monteiro FM. Effect of Nellore (Bos indicus) donor age on in‐vitro embryo production and pregnancy rate. Reprod Domest Anim. 2022;57(9):980-8. PMid:35612981.

Song J, Yang D, Xu J, Zhu T, Chen YE, Zhang J. RS-1 enhances CRISPR/Cas9- and TALEN-mediated knock-in efficiency. Nat Commun. 2016;7(1):10548. PMid:26817820.

Sprink T, Eriksson D, Schiemann J, Hartung F. Regulatory hurdles for genome editing: process- vs. product-based approaches in different regulatory contexts. Plant Cell Rep. 2016;35(7):1493-506. PMid:27142995.

Summer A, Lora I, Formaggioni P, Gottardo F. Impact of heat stress on milk and meat production. Anim Front. 2018;9(1):39-46. PMid:32002238.

Sun D, Jia J, Ma Y, Zhang Y, Wang Y, Yu Y, Zhang Y. Effects of DGAT1 and GHR on milk yield and milk composition in the Chinese dairy population. Anim Genet. 2009;40(6):997-1000. PMid:19781040.

Svennersten-Sjaunja K, Olsson K. Endocrinology of milk production. Domest Anim Endocrinol. 2005;29(2):241-58. PMid:15876512.

Symington LS, Gautier J. Double-strand break end resection and repair pathway choice. Annu Rev Genet. 2011;45(1):247-71. PMid:21910633.

Syrstad O. Dairy cattle crossbreeding in the tropics: choice of crossbreeding strategy. Trop Anim Health Prod. 1996;28(3):223-9. PMid:8888529.

Syrstad O. Dairy cattle cross-breeding in the tropics: performance of secondary cross-bred populations. Livest Prod Sci. 1989;23(1-2):97-106.

Tăbăran A, Balteanu VA, Gal E, Pusta D, Mihaiu R, Dan SD, Tăbăran AF, Mihaiu M. Influence of DGAT1 K232A Polymorphism on Milk Fat Percentage and Fatty Acid Profiles in Romanian Holstein Cattle. Anim Biotechnol. 2015;26(2):105-11. PMid:25380462.

Takata M, Sasaki MS, Sonoda E, Morrison C, Hashimoto M, Utsumi H, Yamaguchi-Iwai Y, Shinohara A, Takeda S. Homologous recombination and non-homologous end-joining pathways of DNA double-strand break repair have overlapping roles in the maintenance of chromosomal integrity in vertebrate cells. EMBO J. 1998;17(18):5497-508. PMid:9736627.

Tani C. EU agriculture ministers move closer to consensus on gene editing of crops. Sci Bussiness; 20 sep 2022.

U.S. Food and Drug Administration. FDA makes low-risk determination for marketing of products from genome-edited beef cattle after safety review. Silver Spring: FDA; 2022.

UF/IFA Range Cattle Research and Education. The SLICK gene in Holstein cattle improves thermotolerance - Colleen Larson [Internet]. YouTube; 2022 [cited 2022 Oct 25]. Available from:

United NationsDepartment of Economic and Social Affairs Population Division. World population prospects 2022: summary of results. UN DESA/POP/2022/TR/NO 3 2022. New York; 2022.

van Eenennaam AL, Silva FF, Trott JF, Zilberman D. Genetic engineering of livestock: the opportunity cost of regulatory delay. Annu Rev Anim Biosci. 2021;9(1):453-78. PMid:33186503.

Vieira LR, Freitas NC, Justen F, Miranda VDJ, Garcia BDO, Nepomuceno AL, Fuganti-Pagliarini R, Felipe M, Molinari H, Velini E, Pinto E, Dagli M, Andrade G, Fernandes P, Mertz-Henning L, Kobayashi A. Regulatory framework of genome editing in Brazil and worldwide. In: Molinari HBC, Vieira LR, Silva NV, Prado GS, Lopes JF Fo, editors. CRISPR technology in plant genome editing: biotechnology applied to agriculture. Brasilia: Embrapa; 2021. p. 169-95.

Viitala S, Szyda J, Blott S, Schulman N, Lidauer M, Mäki-Tanila A, Georges M, Vilkki J. The role of the bovine growth hormone receptor and prolactin receptor genes in milk, fat and protein production in finnish ayrshire dairy cattle. Genetics. 2006;173(4):2151-64. PMid:16751675.

Weindl I, Popp A, Bodirsky BL, Rolinski S, Lotze-Campen H, Biewald A, Humpenöder F, Dietrich JP, Stevanović M. Livestock and human use of land: productivity trends and dietary choices as drivers of future land and carbon dynamics. Global Planet Change. 2017;159:1-10.

Whelan AI, Lema MA. Regulatory framework for gene editing and other new breeding techniques (NBTs) in Argentina. GM Crops Food. 2015;6(4):253-65. PMid:26552666.

Winter A, Krämer W, Werner FAO, Kollers S, Kata S, Durstewitz G, Buitkamp J, Womack JE, Thaller G, Fries R. Association of a lysine-232/alanine polymorphism in a bovine gene encoding acyl-CoA:diacylglycerol acyltransferase (DGAT1) with variation at a quantitative trait locus for milk fat content. Proc Natl Acad Sci USA. 2002;99(14):9300-5. PMid:12077321.

Wulandari AS, Rahayu H, Volkandari S, Herlina N, Anwar S, Irnidayanti Y. Genetic polymorphism of SCD1 gene of Holstein-Friesian cows in Indonesia. J Ilmu Ternak Vet. 2019;24(2):56.

Zhao D, Zhu X, Zhou H, Sun N, Wang T, Bi C, Zhang X. CRISPR-based metabolic pathway engineering. Metab Eng. 2021;63:148-59. PMid:33152516.

Zhu Y. Advances in CRISPR/Cas9. BioMed Res Int. 2022;2022:9978571. PMid:36193328.

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