Chromosomal aberrations and their mechanisms have been studied for many years in livestock. In cattle, chromosomal abnormalities are often associated with serious reproduction-related problems, such as infertility of carriers and early mortality of embryos. In the present work, we review the mechanisms and consequences of the most important bovine chromosomal aberrations: Robertsonian translocations and reciprocal translocations. We also discuss the application of bovine cell cultures in genotoxicity studies.

1st Faculty of Medicine Charles University Prague Salmovská 1 121 08 Prague Czech Republic

Department of Biology and Physiology University of Veterinary Medicine and Pharmacy Komenského 73 041 81 Košice Slovakia

Department of Chemistry Biochemistry and Biophysics University of Veterinary Medicine and Pharmacy Komenského 73 041 81 Košice Slovakia

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Philips C.J.C. Principles of Cattle Production. 2nd ed. CABI Publishing; Cambridge, UK: 2010.

Scheu A., Powell A., Bollongino R., Vigne J.D., Tresset A., Cakirlar C., Benecke N., Burger J. The genetic prehistory of domesticated cattle from their origin to the spread across Europe. BMC Genet. 2015;16:54. doi: 10.1186/s12863-015-0203-2. PubMed DOI PMC

Deb R., Singh U., Kumar S., Sharma A. Analysis of Cattle Genome. A Tool Manual. 1st ed. Satish Serial Publishing House; Delhi, India: 2013.

Elsik C.G., Tellam R.L., Worley K.C. The genome sequence of Taurine cattle. A window to ruminant biology and evolution. Science. 2009;324:522–528. PubMed PMC

Childers A., Reese J.T., Sundaram J.P., Vile D.C., Dickens C.M., Childs K.L., Salih H., Bennett A.K., Hagen D.E., Adelson D.L., et al. Bovine genome database: Integrated tools for genome annotation and discovery. Nucleic Acid Res. 2011;39:D830–D834. doi: 10.1093/nar/gkq1235. PubMed DOI PMC

Stothard P., Liao X., Arantes A.S., De Pauw M., Coros C., Plastow G.S., Sargolzaei M., Crowley J.J., Basarab J.A., Schenkel F., et al. A large and diverse collection of bovine sequences from Canadian Cattle Genome Project. Gigascience. 2015;4:1–3. doi: 10.1186/s13742-015-0090-5. PubMed DOI PMC

Hagen D.E., Unni D.R., Tayal A., Burns G.W., Elsik C.G. Bovine Genome Database: Tools for mining the Bos taurus genome. Methods Mol. Biol. 2018;1757:211–249. PubMed

Gustavsson I. From Giessen to Toulouse: 20 years in domestic animal cytogenetics. Genet. Sel. Evol. 1991;23((Suppl. S1)):9–17. doi: 10.1186/1297-9686-23-S1-S9. DOI

Basrur P.K., Stranzinger G. Veterinary cytogenetics: Past and perspective. Cytogenet. Genome Res. 2008;120:11–25. doi: 10.1159/000118737. PubMed DOI

Iannuzzi L., Di Berardino D. Tools of the trade: Diagnostics and research in domestic animal cytogenetics. J. Appl. Genet. 2008;49:357–366. doi: 10.1007/BF03195634. PubMed DOI

Cribiu E.P., Di Berardino D., Di Meo G.P., Eggen A., Gallagher D.S., Gustavsson I., Hayes H., Iannuzzi L., Popescu C.P., Rubes J., et al. International System for Chromosomal Nomenclature of Domestic Bovids (ISCNDB, 2000) Cytogenet. Cell Genet. 2001;92:283–299. doi: 10.1159/000056917. PubMed DOI

Rubes J., Kubickova S., Pagacova E., Cernohorska H., Di Berardino D., Antoninova M., Vahala J., Robinson T.J. Phylogenomic study of spiral horned antelope by cross species chromosome painting. Chromosome Res. 2008;16:935–947. doi: 10.1007/s10577-008-1250-6. PubMed DOI

Iannuzzi L., King W.A., Di Berardino D. Chromosome evolution in domestic bovids as revealed by chromosome banding and FISH-mapping techniques. Cytogenet. Genome Res. 2009;126:49–62. doi: 10.1159/000245906. PubMed DOI

Amancio A.P., Duarte S.S.M., Silva R.C., da Cruz A.S., Silva D.C., da Silva C.C., da Cruz A.D. Banded karyotype of Nelore cattle (Bos taurus indicus Linnaeus, 1758) Comp. Cytogen. 2019;13:265–275. doi: 10.3897/CompCytogen.v13i3.36449. PubMed DOI PMC

Raudsepp T., Chowdhary B.P. Chromosome aberrations and fertility disorders in domestic animals. Annu. Rev. Anim. Biosci. 2016;4:15–43. doi: 10.1146/annurev-animal-021815-111239. PubMed DOI

Szczerbal I., Switonski M. Chromosome Abnormalities in Domestic Animals as Causes of Disorders of Sexual Development or Impaired Fertility. 2016. [(accessed on 23 May 2021)]. Available online: https://.intechopen.com/chapters/49736.

King W. Chromosome variation in the embryos of domestic animals. Cytogenet. Genome Res. 2008;120:81–90. doi: 10.1159/000118743. PubMed DOI

Garrick D., Ruvinsky A. The Genetics of Cattle. 2nd ed. CABI Publishing; Cambridge, UK: 2015.

Griffiths A.J.F., Miller J.H., Suzuki D.T., Lewontin R.C., Gelbart W.M. An Introduction to Genetic Analysis. 7th ed. W. H. Freeman; New York, NY, USA: 2000. [(accessed on 8 March 2021)]. Mechanisms of gene imbalance. Available online: https://www.ncbi.nlm.nih.gov/books/NBK21967.

Iannuzzi L., Di Meo G.P., Leifsson P.S., Eggen A., Christensen K. A case of trisomy 28 in cattle revealed by both banding and FISH-mapping techniques. Hereditas. 2001;134:147–151. doi: 10.1111/j.1601-5223.2001.00147.x. PubMed DOI

Nicholas F.W. Introduction to Veterinary Genetics. 3rd ed. Wiley-Blackwell; Oxford, UK: 2010.

Häfliger I.M., Seefried F., Drögemüller C. Trisomy 29 in a stillborn Swiss Original Braunvieh calf. Anim. Genet. 2020;51:483–484. doi: 10.1111/age.12929. PubMed DOI

Iannuzzi A., Parma P., Iannuzzi L. Chromosome Abnormalities and Fertility in Domestic Bovids: A Review. Animals. 2021;11:802. doi: 10.3390/ani11030802. PubMed DOI PMC

Iannuzzi A.S., Genualdo V., Perucatti A., Pauciullo A., Varricchio G., Incarnato D. Fatal outcome in a newborn calf associated with partial trisomy 25q and partial monosomy 11q, 60, XX, der (11)t(11;25)(q11;q14 similar to 21) Cytogenet. Genome Res. 2015;146:222–229. doi: 10.1159/000438973. PubMed DOI

Larkin D.M., Farré M. Cytogenetics and Chromosome Maps. In: Garrick D., Ruvinsky A., editors. The Genetics of Cattle. 2nd ed. CABI Publishing; Cambridge, UK: 2015. pp. 103–123.

Ducos A., Revay T., Kovacs A., Hidas A., Pinton A., Bonnet-Garnier A., Molteni L., Slota E., Switonski M., Arruga M.V., et al. Cytogenetic screening of livestock populations in Europe: An overview. Cytogenet. Genome Res. 2008;120:26–41. doi: 10.1159/000118738. PubMed DOI

Citek J., Rubes J., Hajkova J. Robertsonian translocations, chimerism, and aneuploidy in cattle. J. Dairy Sci. 2009;92:3481–3483. doi: 10.3168/jds.2009-2099. PubMed DOI

Uzar T., Szczerbal I., Serwanska-Leja K., Nowacka-Woszuk J., Gogulski M., Bugaj S., Switonski M., Komosa M. Congenital Malformations in a Holstein-Fresian Calf with a Unique Mosaic Karyotype: A Case Report. Animals. 2020;10:1615. doi: 10.3390/ani10091615. PubMed DOI PMC

Harewood L., Fraser P. The impact of chromosoal rearrangements on regulation of gene expression. Human Molec. Genet. 2014;23:R76–R82. doi: 10.1093/hmg/ddu278. PubMed DOI

Wilch E.S., Morton C.C. Historical and Clinical Perspectives on Chromosomal Translocations. In: Zhang Y., editor. Chromosome Translocation. Advances in Experimental Medicine and Biology. Volume 1044 Springer; Singapore: 2018. PubMed

Switonski M. 50 years of studies on bovine 1/29 Robertsonian translocation-from Giemsa staining to genomic analysis. Chromosome Res. 2014;22:395.

Popescu C.P., Pech A. Une bibliographie sur la translocation 1/29 de bovins dans le monde (1964–1990) Ann. Zootech. 1991;40:271–305. doi: 10.1051/animres:19910405. DOI

Eldridge F.E. High frequency of a Robertsonian translocation in a herd of British White cattle. Vet. Res. 1975;97:71–73. doi: 10.1136/vr.97.4.71. PubMed DOI

Hari J.J., Franceschi P., Casabianca F., Bosher J., Popescu C.P. Etude cytogénétique d’une population de bovins corses. Compte Rendu de l’Academie d’Agriculture de France. 1984;70:8.

Gustavsson I., Rockborn G. Chromosome abnormality in three cases of lymphatic leukaemia in cattle. Nature. 1964;203:990. doi: 10.1038/203990a0. PubMed DOI

Gustavsson I. Cytogenetics, distribution and phenotypic effects of a translocation in Swedish cattle. Hereditas. 1969;63:68–169. doi: 10.1111/j.1601-5223.1969.tb02259.x. PubMed DOI

King A.W. Ingemar Gustavsson (1938-2016) Cytogenet. Genome Res. 2017;152:167–168. PubMed

Barasc H., Mouney-Bonnet N., Peigney C., Calgaro A., Revel C., Mary N., Ducos A., Pinton A. Analysis of meitoc segregation pattern and interchromosomal effects in a bull heterozygous for a 3/16 Robertsonian translocation. Cytogenet. Genome Res. 2018;4:197–203. doi: 10.1159/000494289. PubMed DOI

De Lorenzi L., Genualdo V., Gimelli S., Rossi E., Perucatti A., Iannuzzi A., Zannotti M., Malagutti L., Molteni L., Iannuzzi L., et al. Genomic analysis of cattle rob (1;29) Chromosome Res. 2012;20:815–823. doi: 10.1007/s10577-012-9315-y. PubMed DOI

Joerg H., Garner D., Rieder S., Suwattana D., Stransinger G. Molecular genetic characterization of Robertsonian translocations in cattle. J. Anim. Breed. Genet. 2001;118:371–377. doi: 10.1046/j.1439-0388.2001.00303.x. DOI

Arslan K., Ozdemir F., Ilgar E.G., Akyuz B. Cytogenetic and molecular genetic screening in Holstein cattle breed which showing repeat breeding problems. J. Agric. Sci. Tarim Bilimleri Dergisi. 2016;22:370–373.

Iannuzzi A., Di Meo G.P., Caputi Jambrenghi A., Vonghia G., Iannuzzi L., Rangel-Figueiredo F. Frequency and distribution of rob (1;29) in eight Portugese cattle breeds. Cytogenet. Genome Res. 2008;120:147–149. doi: 10.1159/000118755. PubMed DOI

Rodero-Serrano E., Demyda-Peyrás S., González-Martinez A., Rodero-Franganillo A., Moreno-Millán M. The rob (1;29) chromosome translocation in endangered Andalusian cattle breeds. Livest. Sci. 2013;158:32–39. doi: 10.1016/j.livsci.2013.10.001. DOI

Meza-López C., Lozano-Carbajal B., de la Colina-Flores F., Bañuelos-Valenzuela R., López-Carlos M.A., Echavarría-Cháirez F.G., Reveles-Torres L.R. Prevalence of the Robertsonian (1;29) translocation in cattle in the state of Zacatecas, México. Rev. Mex. Cienc. Pecu. 2015;6:295–304. doi: 10.22319/rmcp.v6i3.4092. DOI

Dzitsiuk V.V., Tipilo H.T. Chromosomal anomalies in dairy cattle as reasons of impaired fertility. Agric. Sci. Pract. 2019;6:60. doi: 10.15407/agrisp6.01.060. DOI

Gholap P.N., Kale D.S., Sirothia A.R. Genetic diseases in cattle: A review. Res. J. Anim. Vet. Fish. Sci. 2014;2:24–33.

De Lorenzi L., De Giovanni A., Molteni L., Denis C., Eggen A., Parma P. Characterization of balanced reciprocal translocation, rcp(9;11)(q27;q11) in cattle. Cytogenet. Genome Res. 2007;119:231–234. doi: 10.1159/000112066. PubMed DOI

De Lorenzi L., Morando P., Planas J., Zannotti M., Molteni L., Parma P. Reciprocal translocations in cattle: Frequencies estimation. J. Anim. Breed. Genet. 2012;129:409–416. doi: 10.1111/j.1439-0388.2011.00983.x. PubMed DOI

De Lorenzi L., Kopecna O., Gimelli S., Cernohorska H., Zannotti M., Béna F., Molteni L., Rubes J., Parma P. Reciprocal translocation t(4;7)(q14;q28) in cattle: Molecular characterization. Cytogenet. Genome Res. 2010;129:298–304. doi: 10.1159/000315891. PubMed DOI

De Lorenzi L., Rossi E., Gimelli S., Parma P. De novo reciprocal translocation t(5;6)(q13;q34) in cattle: Cytogenetic and molecular characterization. Cytogenet. Genome Res. 2014;142:95–100. PubMed

De Lorenzi L., Iannuzzi A., Rossi E., Bonacina S., Parma P. Centromere repositioning in cattle (Bos taurus) chromosome 17. Cytogenet. Genome Res. 2017;151:191–197. doi: 10.1159/000473781. PubMed DOI

Jennings R.L., Griffin D.J., O′Connor R.E. A new approach for accurate detection of chromosome rearrangements that affect fertility in cattle. Animals. 2020;10:114. doi: 10.3390/ani10010114. PubMed DOI PMC

Switonski M., Andersson M., Nowacka-Woszuk J., Szczerbal I., Sosnowski J., Kopp C., Cernohorska H., Rubeš J. Identification of a new reciprocal translocation in an AI bull by synaptonemal complex analysis, followed by chromosome painting. Cytogenet. Genome Res. 2008;121:245–248. doi: 10.1159/000138891. PubMed DOI

Rubes J., Pinton A., Bonnet-Garnier A., Fillon V., Musilova P., Michalova K., Kubickova S., Ducos A., Yerle M. Fluorscence in situ hybridization applied to domestic animal cytogenetics. Cytogenet. Genome Res. 2009;126:34–48. PubMed

Yang F., Trifonov V., Ng B.L., Kosyakova N., Carter N.P. Generation of paint probes by flow-sorted and microdissected chromosomes. In: Liehr T., editor. Fluorescence in situ hybridization (FISH). Application Guide. 1st ed. Springer; Berlin/Heidelberg, Germany: 2009. pp. 35–52.

Dixon S.C., Miller N.G., Carter N.P., Tucker E.M. Bivariate flow cytometry of farm animal chromosomes: A potential tool for gene mapping. Anim. Genet. 1992;23:203–210. doi: 10.1111/j.1365-2052.1992.tb00132.x. PubMed DOI

Kubickova S., Cernohorska H., Musilova P., Rubes J. The use of laser microdissection for the preparation of chromosome-specific painting probes in farm animals. Chromosome Res. 2002;10:571–577. PubMed

Fröhlich J., Kubickova S., Musilová P., Cernohorska H., Muskova H., Vodička R., Rubes J. Karyotype relationships among selected deer species and cattle revealed by bovine FISH probes. PLoS ONE. 2017;12:e0187559. doi: 10.1371/journal.pone.0187559. PubMed DOI PMC

Rezacova O., Kubickova S., Cernohorska H., Rubes J. Comparison of spontaneous background genomic aberration frequencies among cattle, pig and humans using dual-coloured FISH. Chromosome Res. 2003;11:715–724. PubMed

Pinton A., Ducos A., Yerle M. Chromosomal rearrangements in cattle and pigs revealed by chromosome microdissection and chromosome painting. Genet. Sel. Evol. 2003;35:685–696. doi: 10.1186/1297-9686-35-7-685. PubMed DOI PMC

De Lorenzi L., Molteni L., De Giovanni A., Parma P. A new case of rob (14, 17) in cattle. Cytogenet. Genome Res. 2008;120:144–146. doi: 10.1159/000118754. PubMed DOI

De Lorenzi L., Molteni L., Denis C., Eggen A., Parma P. A new case of centric fusion in cattle:rob (21;23) Anim. Genet. 2008;39:454–455. doi: 10.1111/j.1365-2052.2008.01731.x. PubMed DOI

Weise A., Mrasek K., Kosyakova N., Mkrtchyan H., Gross M., Klaschka V., Liehr T. ISH probes derived from BACs, including microwave treatment for better FISH results. In: Liehr T., editor. Fluorescence in situ hybridization (FISH). Application Guide. 1st ed. Springer; Berlin/Heidelberg, Germany: 2009. pp. 53–60.

Eggen A., Gautier M., Billaut A., Petit E., Hayes H., Laurent P., Urban C. Construction and characterization of a bovine BAC library with four genome-equivalent coverage. Genet. Sel. Evol. 2001;33:543–548. doi: 10.1186/1297-9686-33-5-543. PubMed DOI PMC

Huang L., Ma F., Chapman A., Lu S., Xie X.S. Single-cell whole genome amplification and sequencing: Methodology and applications. Annu. Rev. Genomics Hum. Genet. 2015;16:79–102. doi: 10.1146/annurev-genom-090413-025352. PubMed DOI

Dimitriadou E., Esteki M.Z., Vermeesch J.R. Copy Number Variation Analysis by Array Analysis of Single Cells Following Whole Genome Amplification. In: Kroneis T., editor. Whole Genome Amplification, Methods and Protocols. Humana Press; Totowa, NJ, USA: 2015. PubMed

Hawken R.J., Cavanagh J.A.L., Meadows J.R.S., Khatkar M.S., Husaini Y., Zenger K.R., McClintock S., McClintock A.E., Raadsma H.W. Technical note: Whole-genome amplification of DNA extracted from cattle semen samples. J. Dairy Sci. 2006;89:2217–2222. doi: 10.3168/jds.S0022-0302(06)72292-5. PubMed DOI

Zhang S., Zhao D., Zhang J., Mao Y., Kong L., Zhang Y., Liang B., Sun X., Xu C. BasePhasing: A highly efficient approach preimplantation genetic haplotyping in clinical application of balanced translocation carriers. BMC Med. Genom. 2019;12:3–10. doi: 10.1186/s12920-019-0495-6. PubMed DOI PMC

Rubeš J., Borkovec L., Hořínová Z., Urbanová J., Proroková I., Kulíková L. Cytogenetic monitoring of farm animals under conditions of environmental pollution. Mutat. Res. 1992;283:199–210. doi: 10.1016/0165-7992(92)90108-T. PubMed DOI

Oruc H.H. Fungicides and their effects on animals. In: Carisse O., editor. Fungicides. InTech; Rijeka, Croatia: 2010.

Guitart R., Croubels S., Caloni F., Sachana M., Davanzo F., Vandenbroucke V., Berny P. Animal Poisoning in Europe Part I: Farm livestock and poultry. Vet. J. 2010;183:249–254. doi: 10.1016/j.tvjl.2009.03.002. PubMed DOI

Hernández A.F., Gil F., Lacasana M. Toxicological interactions of pesticide mixtures: An update. Arch. Toxicol. 2017;91:3211–3223. doi: 10.1007/s00204-017-2043-5. PubMed DOI

Rubes J., Pokorna Z., Borkovec L., Urbanova J., Strnadova V. Dairy cattle as a bioindicator of exposure to genotoxic substances in a heavy polluted area in northern Bohemia. Mutat. Res. 1997;391:57–70. doi: 10.1016/S0165-1218(97)00032-3. PubMed DOI

Favetta L., Villagómez D., Iannuzzi L., Di Meo G., Webb A., Crain S., King W. Disorders of sexual development and abnormal early development in domestic food-producing mammals: The role of chromosome abnormalities, environment and stress factors. Sex Dev. 2012;6:18–32. doi: 10.1159/000332754. PubMed DOI

Nakamura A.J., Suzuki M., Redon C.E., Kuwahara Y., Yamashiro H., Abe Y., Takahashi S., Fukuda T., Isogai E., Bonner W.M., et al. The Causal Relationship between DNA Damage Induction in Bovine Lymphocytes and the Fukushima Nuclear Power Plant Accident. Radiat. Res. 2017;187:630–636. doi: 10.1667/RR14630.1. PubMed DOI PMC

Lioi M., Scarfi M., Santoro A., Barbieri R., Zeni O., Di Berardino D., Ursini M. Genotoxicity and oxidative stress induced by pesticide exposure in bovine lymphocyte cultures in vitro. Mutat. Res. 1998;403:13–20. doi: 10.1016/S0027-5107(98)00010-4. PubMed DOI

Rossi C., Danielli P.P., Ronchi B. In vitro effects of the organochlorine pesticide β-hexachlorocyclohexane on bovine peripheral blood mononuclear cells. Ital. J. Anim. Sci. 2014;13:620–626. doi: 10.4081/ijas.2014.3360. DOI

Chwarzbacherová V., Wnuk M., Lewinska A., Potocki L., Zebrowski J., Koziorowski M., Holečková B., Šiviková K., Dianovský J. Evaluation of cytotoxic and genotoxic activity of fungicide formulation Tango Super in bovine lymphocytes. Environ. Poll. 2017;220:255–263. doi: 10.1016/j.envpol.2016.09.057. PubMed DOI

Sivikova K., Holeckova B., Schwarzbacherova V., Galdikova M., Dianovsky J. Potential chromosome damage, cell-cycle kinetics and apoptosis induced by epoxiconazole in bovine peripheral lymphocytes in vitro. Chemosphere. 2018;193:82–88. doi: 10.1016/j.chemosphere.2017.11.008. PubMed DOI

Ferré D.M., Ludueña H.R., Romano R.R., Gorla N.B.M. Evaluation of the genotoxic potential of cypermetrin, chlorpyrifos and their subsequent mixture, on cultured bovine lymphocytes. Chemosphere. 2020;243:1–9. doi: 10.1016/j.chemosphere.2019.125341. PubMed DOI

Holeckova B., Sivikova K., Dianovsky J., Galdikova M. Efect of triazole pesticide formulation on bovine culture cells. J. Environ. Sci. Health B. 2013;48:1080–1088. doi: 10.1080/03601234.2013.824224. PubMed DOI

Šiviková K., Dianovský J., Holečková B., Galdíková M., Kolesárová V. Assessment of cytogenetic damage in bovine peripheral lymphocytes exposed to in vitro tebuconazole-based fungicide. Chemosphere. 2013;92:555–562. doi: 10.1016/j.chemosphere.2013.04.001. PubMed DOI

Castro C.C., Luoma A.M., Adams E.J. Coevolution of T cell receptors with MHC and non-MHC ligands. Immunol. Rev. 2015;267:30–55. doi: 10.1111/imr.12327. PubMed DOI PMC

Drazovska M., Sivikova K., Holeckova B., Dianovsky J., Galdikova M., Schwarzbacherova V. Evaluation of potential genotoxic/cytotoxic effects induced by epoxiconazole and fenpropimorph-based fungicide in bovine lymphocytes in vitro. J. Environ. Sci. Health B. 2016;51:769–776. doi: 10.1080/03601234.2016.1198643. PubMed DOI

Galdikova M., Sivikova K., Holeckova B., Dianovsky J., Drazovska M., Schwarzbacherova V. The effect of thiacloprid formulation on DNA/chromosome damage and changes in GST activity in bovine peripheral lymphocytes. J. Environ. Sci. Health B. 2016;50:698–707. doi: 10.1080/03601234.2015.1048102. PubMed DOI

Marshall R., Obe G. Application of chromosome painting to clastogenicity testing in vitro. Environ. Mol. Mutagen. 1998;32:212–222. doi: 10.1002/(SICI)1098-2280(1998)32:3<212::AID-EM3>3.0.CO;2-G. PubMed DOI

Baumgartner A. Comparative genomic hybridization (CGH) in genotoxicology. In: Dhawan A., Bajpajee M., editors. Genotoxicity Assessment. Methods and Protocols. Humana Press; Totowa, NJ, USA: 2013. pp. 245–256. PubMed