Skip to main content
SpringerLink
Log in

Recombination correlates with synaptonemal complex length and chromatin loop size in bovids—insights into mammalian meiotic chromosomal organization

  • Original Article
  • Published:
Chromosoma Aims and scope Submit manuscript

Abstract

Homologous chromosomes exchange genetic information through recombination during meiosis, a process that increases genetic diversity, and is fundamental to sexual reproduction. In an attempt to shed light on the dynamics of mammalian recombination and its implications for genome organization, we have studied the recombination characteristics of 112 individuals belonging to 28 different species in the family Bovidae. In particular, we analyzed the distribution of RAD51 and MLH1 foci during the meiotic prophase I that serve, respectively, as proxies for double-strand breaks (DSBs) which form in early stages of meiosis and for crossovers. In addition, synaptonemal complex length and meiotic DNA loop size were estimated to explore how genome organization determines DSBs and crossover patterns. We show that although the number of meiotic DSBs per cell and recombination rates observed vary between individuals of the same species, these are correlated with diploid number as well as with synaptonemal complex and DNA loop sizes. Our results illustrate that genome packaging, DSB frequencies, and crossover rates tend to be correlated, while meiotic chromosomal axis length and DNA loop size are inversely correlated in mammals. Moreover, axis length, DSB frequency, and crossover frequencies all covary, suggesting that these correlations are established in the early stages of meiosis.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

Similar content being viewed by others

References

  • Anderson LK, Reeves A, Webb LM, Ashley T (1999) Distribution of crossing over on mouse synaptonemal complexes using immunofluorescent localization of MLH1 protein. Genetics 151:1569–1579

    CAS  PubMed  PubMed Central  Google Scholar 

  • Auton A, Fledel-Alon A, Pfeifer S, Venn O, Ségurel L, Street T, Leffler EM, Bowden R, Aneas I, Broxholme J, Humburg P, Iqbal Z, Lunter G, Maller J, Hernandez RD, Melton C, Venkat A, Nobrega MA, Bontrop R, Myers S, Donnelly P, Przeworski M, McVean G (2012) A fine-scale chimpanzee genetic map from population sequencing. Science 336:193–198

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Baker SM, Plug AW, Prolla TA, Bronner CE, Harris AC, Yao X, Christie DM, Monell C, Arnheim N, Bradley A, Ashley T, Liskay RM (1996) Involvement of mouse Mlh1 in DNA mismatch repair and meiotic crossing over. Nat Genet 13:336–342

    Article  CAS  PubMed  Google Scholar 

  • Baudat F, de Massy B (2007) Regulating double-stranded DNA break repair towards crossover or non-crossover during mammalian meiosis. Chromosom Res 15:565–577

    Article  CAS  Google Scholar 

  • Baudat F, Imai Y, de Massy B (2013) Meiotic recombination in mammals: localization and regulation. Nat Rev Genet 14:794–806

    Article  CAS  PubMed  Google Scholar 

  • Bishop DK (1994) RecA homologs Dmc1 and Rad51 interact to form multiple nuclear complexes prior to meiotic chromosome synapsis. Cell 79:1081–1092

    Article  CAS  PubMed  Google Scholar 

  • Butlin RK (2005) Recombination and speciation. Mol Ecol 14:2621–2635

    Article  CAS  PubMed  Google Scholar 

  • Capilla L, Medarde N, Alemany-Schmidt A, Oliver-Bonet M, Ventura J, Ruiz-Herrera A (2014) Genetic recombination variation in wild Robertsonian mice: on the role of chromosomal fusions and Prdm9 allelic background. Proc Biol Sci 281:1786

    Article  Google Scholar 

  • Capilla L, Garcia-Caldes M, Ruiz-Herrera A (2016) Mammalian meiotic recombination: a toolbox for genome evolution. Cytogenet Genome Res. doi:10.1159/000452822

  • Carson HL (1957) The species as a field for gene recombination. Pages 23–38. In: Mayr E (ed) The species problem. Amer Assoc Adv Sci Pub 50, Washington

    Google Scholar 

  • Cernohorska H, Kubickova S, Vahala J, Robinson TJ, Rubes J (2011) Cytotypes of Kirk’s dik-dik (Madoqua kirkii, Bovidae) show multiple tandem fusions. Cytogenet Genome Res 132:255–263

    Article  CAS  PubMed  Google Scholar 

  • Cernohorska H, Kubickova S, Vahala J, Rubes J (2012) Molecular insights into X;BTA5 chromosome rearrangements in the tribe Antilopini (Bovidae). Cytogenet Genome Res 136:188–198

    Article  CAS  PubMed  Google Scholar 

  • Clark AG, Wang X, Matise T (2010) Contrasting methods of quantifying fine structure of human recombination. Annu Rev Genomics Hum Genet 11:45–64

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Codina-Pascual M, Campillo M, Kraus J, Speicher MR, Egozcue J, Navarro J, Benet J (2006) Crossover frequency and synaptonemal complex length: their variability and effects on human male meiosis. Mol Hum Reprod 12:123–133

    Article  CAS  PubMed  Google Scholar 

  • Cole F, Kauppi L, Lange J, Roig I, Wang R, Keeney S, Jasin M (2012) Homeostatic control of recombination is implemented progressively in mouse meiosis. Nat Cell Biol 14:424–430

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • de Boer E, Heyting C (2006) The diverse roles of transverse filaments of synaptonemal complexes in meiosis. Chromosoma 115:220–234

    Article  PubMed  Google Scholar 

  • de Boer E, Stam P, Dietrich AJJ, Pastink A, Heyting C (2006) Two levels of interference in mouse meiotic recombination. Proc Nat Ac Sci 103:9607–9612

    Article  Google Scholar 

  • de Massy B (2013) Initiation of meiotic recombination: how and where? Conservation and specificities among eukaryotes. Annu Rev Genet 47:563–599

    Article  PubMed  Google Scholar 

  • de Villena P-M, Sapienza (2001) Recombination is proportional to the number of chromosome arms in mammals. Mamm Genome 12:318–322

    Article  Google Scholar 

  • Dumont BL, Payseur BA (2011) Evolution of the genomic recombination rate in murid rodents. Genetics 187:643–657

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Farré M, Micheletti D, Ruiz-Herrera A (2013) Recombination rates and genomic shuffling in human and chimpanzee-a new twist in the chromosomal speciation theory. Mol Biol Evol 30:853–864

    Article  PubMed  Google Scholar 

  • Froenicke L, Anderson LK, Wienberg J, Ashley T (2002) Male mouse recombination maps for each autosome identified by chromosome painting. Am J Hum Genet 71:1353–1368

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Frohlich J, Vozdova M, Kubickova S, Cernohorska H, Sebestova H, Rubes J (2015) Variation of meiotic recombination rates and MLH1 foci distribution in spermatocytes of cattle, sheep and goats. Cytogenet Genome Res 146:211–221

    Article  PubMed  Google Scholar 

  • Garcia-Cruz R, Roig I, Garcia-Caldes M (2009) Maternal origin of the human aneuploidies. Are homolog synapsis and recombination to blame? Notes (learned) from the underbelly. Genome Dyn 5:128–136

    Article  CAS  PubMed  Google Scholar 

  • Garcia-Cruz R, Pacheco S, Brieno MA, Steinberg ER, Mudry MD, Ruiz-Herrera A, Garcia-Caldes M (2011) A comparative study of the recombination pattern in three species of Platyrrhini monkeys (primates). Chromosoma 120:521–530

    Article  PubMed  Google Scholar 

  • Gauthier F, Martin OC, Falque M (2011) CODA (crossover distribution analyzer): quantitative characterization of crossover position patterns along chromosomes. BMC Bioinformatics 12:27

    Article  PubMed  PubMed Central  Google Scholar 

  • Gruhn JR, Rubio C, Broman KW, Hunt PA, Hassold T (2013) Cytological studies of human meiosis: sex-specific differences in recombination originate at, or prior to, establishment of double-strand breaks. PLoS One 8:e85075

    Article  PubMed  PubMed Central  Google Scholar 

  • Hassanin A, Douzery EJP (1999) The tribal radiation of the family Bovidae (Artiodactyla) and the evolution of the mitochondrial cytochrome b gene. Mol Phylogenet Evol 13:227–243

    Article  CAS  PubMed  Google Scholar 

  • Hassold T, Hunt P (2001) To ERR (meiotically) is human: the genesis of human aneuploidy. Nat Rev Genet 2:280–291

    Article  CAS  PubMed  Google Scholar 

  • Hassold T, Hansen T, Hunt P, VandeVoort C (2009) Cytological studies of recombination in rhesus males. Cytogenet Genome Res 124:132–138

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hayes H, Petit E, Dutrillaux B (1991) Comparison of RBG-banded karyotypes of cattle, sheep, and goats. Cytogenet Cell Genet 57:51–55

    Article  CAS  PubMed  Google Scholar 

  • He Z, Henricksen LA, Wold MS, Ingles CJ (1995) RPA involvement in the damage-recognition and incision steps of nucleotide excision repair. Nature 374:566–569

    Article  CAS  PubMed  Google Scholar 

  • Hunter N (2015) Meiotic recombination: the essence of heredity. Cold Spring Harb Perspect Biol 7(12)

  • Kauppi L, Barchi M, Baudat F, Romanienko PJ, Keeney S, Jasin M (2011) Distinct properties of the XY pseudoautosomal region crucial for male meiosis. Science 331:916–920

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kauppi L, Barchi M, Lange J, Baudat F, Jasin M, Keeney S (2013) Numerical constraints and feedback control of double-strand breaks in mouse meiosis. Genes Dev 27(8):873–886

  • Keeney S, Giroux CN, Kleckner N (1997) Meiosis-specific DNA double-strand breaks are catalyzed by Spo11, a member of a widely conserved protein family. Cell 88:375–384

    Article  CAS  PubMed  Google Scholar 

  • Kleckner N (2006) Chiasma formation: chromatin/axis interplay and the role(s) of the synaptonemal complex. Chromosoma 115:175–194

    Article  PubMed  Google Scholar 

  • Kleckner N, Storlazzi A, Zickler D (2003) Coordinate variation in meiotic pachytene SC length and total crossover/chiasma frequency under conditions of constant DNA length. Trends Genet 19:623–628

    Article  CAS  PubMed  Google Scholar 

  • Kneitz B, Cohen PE, Avdievich E, Zhu L, Kane MF, Hou H Jr, Kolodner RD, Kucherlapati R, Pollard JW, Edelmann W (2000) MutS homolog 4 localization to meiotic chromosomes is required for chromosome pairing during meiosis in male and female mice. Genes Dev 14(9):1085–1097

    CAS  PubMed  PubMed Central  Google Scholar 

  • Koehler KE, Cherry JP, Lynn A, Hunt PA, Hassold TJ (2002) Genetic control of mammalian meiotic recombination. I. Variation in exchange frequencies among males from inbred mouse strains. Genetics 162:297–306

    CAS  PubMed  PubMed Central  Google Scholar 

  • Kong A, Thorleifsson G, Gudbjartsson DF, Masson G, Sigurdsson A, Jonasdottir A, Walters GB, Jonasdottir A, Gylfason A, Kristinsson KT, Gudjonsson SA, Frigge ML, Helgason A, Thorsteinsdottir U, Stefansson K (2010) Fine-scale recombination rate differences between sexes, populations and individuals. Nature 467:1099–1103

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Lam I, Keeney S (2015) Mechanism and regulation of meiotic recombination initiation. Cold Spring Harb Perspect Biol 7:a016634

    Article  PubMed Central  Google Scholar 

  • Lipkin SM, Moens PB, Wang V, Lenzi M, Shanmugarajah D, Gilgeous A, Thomas J, Cheng J, Touchman JW, Green ED, Schwartzberg P, Collins FS, Cohen PE (2002) Meiotic arrest and aneuploidy in MLH3-deficient mice. Nat Genet 31:385–390

    CAS  PubMed  Google Scholar 

  • Lynn A, Koehler KE, Judis L, Chan ER, Cherry JP, Schwartz S, Seftel A, Hunt PA, Hassold TJ (2002) Covariation of synaptonemal complex length and mammalian meiotic exchange rates. Science 296:2222–2225

    Article  CAS  PubMed  Google Scholar 

  • Mary N, Barasc H, Ferchaud S, Billon Y, Meslier F, Robelin D, Calgaro A, Loustau-Dudez AM, Bonnet N, Yerle M, Acloque H, Ducos A, Pinton A (2014) Meiotic recombination analyses of individual chromosomes in male domestic pigs (Sus scrofa domestica). PLoS One 9:e99123

    Article  PubMed  PubMed Central  Google Scholar 

  • Muñoz M, Alves E, Ramayo-Caldas Y, Casellas J, Rodríguez C, Folch JM, Silió L, Fernández AI (2012) Recombination rates across porcine autosomes inferred from high- density linkage maps. Anim Genet 43:620–623

    Article  PubMed  Google Scholar 

  • Murakami H, Keeney S (2008) Regulating the formation of DNA double-strand breaks in meiosis. Genes Dev 22:286–292

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Myers S, Bottolo L, Freeman C, McVean G, Donnelly P (2005) A fine-scale map of recombination rates and hotspots across the human genome. Science 310:321–324

    Article  CAS  PubMed  Google Scholar 

  • Ortiz-Barrientos D, Engelstädter J, Rieseberg LH (2016) Recombination rate evolution and the origin of species. Trends Ecol Evol 31:226–236

    Article  PubMed  Google Scholar 

  • Ottolini CS, Newnham LJ, Capalbo A, Natesan SA, Joshi HA, Cimadomo D, Griffin DK, Sage K, Summers MC, Thornhill AR, Housworth E, Herbert AD, Rienzi L, Ubaldi FM, Handyside AH, Hoffmann ER (2015) Genome-wide maps of recombination and chromosome segregation in human oocytes and embryos show selection for maternal recombination rates. Nat Genet 2047:727–735

    Article  Google Scholar 

  • Pagacova E, Cernohorska H, Kubickova S, Vahala J, Rubes J (2011) Centric fusion polymorphism in captive animals of family Bovidae. Conserv Genet 12:71–77

    Article  Google Scholar 

  • Poissant J, Hogg JT, Davis CS, Miller JM, Maddox JF, Coltman DW (2010) Genetic linkage map of a wild genome: genomic structure, recombination and sexual dimorphism in bighorn sheep. BMC Genomics 11:524

    Article  PubMed  PubMed Central  Google Scholar 

  • Ptak SE, Hinds DA, Koehler K, Nickel B, Patil N, Ballinger DG, Przeworski M, Frazer KA, Pääbo S (2005) Fine-scale recombination patterns differ between chimpanzees and humans. Nat Genet 37:429–434

    Article  CAS  PubMed  Google Scholar 

  • Robinson TJ, Ropiquet A (2011) Examination of hemiplasy, homoplasy and phylogenetic discordance in chromosomal evolution of the Bovidae. Syst Biol 60:439–450

    Article  PubMed  Google Scholar 

  • Rubes J, Kubickova S, Pagacova E, Cernohorska H, Di Berardino D, Antoninova M, Vahala J, Robinson TJ (2008) Phylogenomic study of spiral-horned antelope by cross-species chromosome painting. Chromosom Res 16:935–947

    Article  CAS  Google Scholar 

  • Rubes J, Musilova P, Kopecna O, Kubickova S, Cernohorska H, Kulemsina AI (2012) Comparative molecular cytogenetics in Cetartiodactyla. Cytogenet Genome Res 137:194–207

    Article  CAS  PubMed  Google Scholar 

  • Santucci-Darmanin S, Walpita D, Lespinasse F, Desnuelle C, Ashley T, Paquis-Flucklinger V (2000) MSH4 acts in conjunction with MLH1 during mammalian meiosis. FASEB 14:1539–1547

    Article  CAS  Google Scholar 

  • Sebestova H, Vozdova M, Kubickova S, Cernohorska H, Kotrba R, Rubes J (2016) Effect of species-specific differences in chromosome morphology on chromatin compaction and the frequency and distribution of RAD51 and MLH1 foci in two bovid species: cattle (Bos taurus) and the common eland (Taurotragus oryx). Chromosoma 125:137–149

    Article  CAS  PubMed  Google Scholar 

  • Segura J, Ferretti L, Ramos-Onsins S, Capilla L, Farre M, Reis F, Oliver-Bonet M, Fernandez-Bellon H, Garcia F, Garcia-Caldes M, Robinson TJ, Ruiz-Herrera A (2013) Evolution of recombination in eutherian mammals: insights into mechanisms that affect recombination rates and crossover interference. Proc Royal Soc B 280:20131945

    Article  Google Scholar 

  • Smagulova F, Gregoretti IV, Brick K, Khil P, Camerini-Otero RD, Petukhova GV (2011) Genome-wide analysis reveals novel molecular features of mouse recombination hotspots. Nature 472:375–378

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Smukowski CS, Noor MF (2011) Recombination rate variation in closely related species. Heredity 107:496–508

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Snowden T, Acharya S, Butz C, Berardini M, Fishel R (2004) hMSH4-hMSH5 recognizes Holliday junctions and forms a meiosis-specific sliding clamp that embraces homologous chromosomes. Mol Cell 15:437–451

    Article  CAS  PubMed  Google Scholar 

  • Stevison LS, Woerner AE, Kidd JM, Kelley JL, Veeramah KR, McManus KF, Great Ape Genome Project, Bustamante CD, Hammer MF, Wall JD (2016) The time scale of recombination rate evolution in great apes. Mol Biol Evol 33:928–945

    Article  CAS  PubMed  Google Scholar 

  • Storlazzi A, Gargano S, Ruprich-Robert G, Falque M, David M, Kleckner N, Zickler D (2010) Recombination proteins mediate meiotic spatial chromosome organization and pairing. Cell 141:94–106

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sun F, Trpkov K, Rademaker A, Ko E, Martin RH (2005) Variation in meiotic recombination frequencies among human males. Hum Genet 116:172–178

    Article  CAS  PubMed  Google Scholar 

  • Tease C, Hultén MA (2004) Inter-sex variation in synaptonemal complex lengths largely determine the different recombination rates in male and female germ cells. Cytogenet Genome Res 107:208–215

    Article  CAS  PubMed  Google Scholar 

  • Vozdova M, Sebestova H, Kubícková S, Cernohorska H, Vahala J, Rubes J (2013) A comparative study of meiotic recombination in cattle (Bos taurus) and three wildebeest species (Connochaetes gnou, C. taurinus taurinus and C. t. albojubatus). Cytogenet Genome Res 140:36–45

    Article  CAS  PubMed  Google Scholar 

  • Vozdova M, Sebestova H, Kubickova S, Cernohorska H, Awadova T, Vahala J, Rubes J (2014) Impact of Robertsonian translocation on meiosis and reproduction: an impala (Aepyceros melampus) model. J Appl Genet 55:249–258

    Article  PubMed  Google Scholar 

  • Vozdova M, Ruiz-Herrera A, Fernandez J, Cernohorska H, Frohlich J, Sebestova H, Kubickova S, Rubes J (2016) Meiotic behaviour of evolutionary sex-autosome translocations in Bovidae. Chromosom Res 24:325–338

    Article  CAS  Google Scholar 

  • Wang S, Zickler D, Kleckner N, Zhang L (2015) Meiotic crossover patterns: obligatory crossover, interference and homeostasis in a single process. Cell Cycle 14:305–314

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Youds JL, Mets DG, McIlwraith MJ, Martin JS, Ward JD, ONeil NJ, Rose AM, West SC, Meyer BJ, Boulton SJ (2010) RTEL-1 enforces meiotic crossover interference and homeostasis. Science 327:1254–1258

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zickler D, Kleckner N (1999) Meiotic chromosomes: integrating structure and function. Annu Rev Genet 33:603–754

    Article  CAS  PubMed  Google Scholar 

  • Zickler D, Kleckner N (2015) Recombination, pairing, and synapsis of homologs during meiosis. Cold Spring Harb Perspect Biol 7(6)

Download references

Acknowledgements

The authors are grateful to the Zoo in Dvur Kralove nad Labem, specially to veterinarians J Vahala and L Pavlacik, for providing the samples.

Author information

Authors and Affiliations

  1. Genome Integrity and Instability Group, Institut de Biotecnologia i Biomedicina (IBB), Universitat Autònoma de Barcelona, Barcelona, Spain

    Aurora Ruiz-Herrera, Jonathan Fernández, Laia Capilla, Covadonga Vara & Adrià Hernández-Marsal

  2. Departament de Biologia Cel·lular, Fisiologia i Immunologia, Universitat Autònoma de Barcelona, Barcelona, Spain

    Aurora Ruiz-Herrera & Covadonga Vara

  3. Central European Institute of Technology - Veterinary Research Institute, Brno, Czech Republic

    Miluse Vozdova, Hana Sebestova, Jan Frohlich, Jaroslav Sipek & Jiri Rubes

  4. Evolutionary Genomics Group, Department of Botany and Zoology, University of Stellenbosch, Stellenbosch, South Africa

    Terence J. Robinson

Authors
  1. Aurora Ruiz-Herrera
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Miluse Vozdova
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Jonathan Fernández
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Hana Sebestova
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Laia Capilla
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Jan Frohlich
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Covadonga Vara
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Adrià Hernández-Marsal
    View author publications

    You can also search for this author in PubMed Google Scholar

  9. Jaroslav Sipek
    View author publications

    You can also search for this author in PubMed Google Scholar

  10. Terence J. Robinson
    View author publications

    You can also search for this author in PubMed Google Scholar

  11. Jiri Rubes
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Aurora Ruiz-Herrera.

Ethics declarations

Funding

This work was supported by grants from the Spanish “Ministerio de Economia y Competitividad” (CGL-2010-20170, CGL-2014-54317-P and BFU2015-71786-REDT) to ARH; the Grant Agency of Czech Republic (P502/11/0719) to MV; and the European Regional Development Fund (ED1.1.00/02.0068) and the Ministry of Education, Youth, and Sports of the Czech Republic (CEITEC 2020 project LQ1601) to JR. LC was the beneficiary of a FPI predoctoral fellowship (BES-2011-047722) as well as CV (BES-2015-072924). TJR’s research was funded by the South African National Research Foundation.

Conflict of interest

The authors declare that they have no conflict of interest.

Ethical approval

All applicable international, national, and/or institutional guidelines for the care and use of animals were followed. This article does not contain any studies with human participants performed by any of the authors.

Electronic supplementary material

Supplementary Figure 1

Meiotic recombination patterns in all species included in the study. In the case of the species where more than one individual was analyzed, the mean number of COs is represented. See Fig. 1, Table 1 and Table 2 for further details. Tribal affiliation and species analyzed herein: (i) Bovini—S. C. caffer (SCA), S. C. nanus (SNA), B. taurus (BTA), B. indicus (BIN); (ii) Tragelaphini—T. oryx (TOR), T. imberbis (TIM), T. strepsiceros (TST), T. spekii (TSP); (iii) Aepycerotini—A. melampus (AME); (iv) Antilopini- A. marsupialis (AMA), N. D. ruficollis (NDA), G. leptoceros (GLE), M. kirkii (MKI); (v) Reduncini—K. l. kafuensis (KLE), K. e. ellipsiprymnus (KEL); (vi) Hipotragini—A. nasomaculatus (ANA), H. equinus (HEQ), H. niger (HNI), O. gazela (OGA), O. dammah (ODA), O. leucoryx (OLE); (vii) Alcelaphini—D. P. phillipsi (DPY) , C. gnou (CGN), C. t. taurinus (CTT) , C. t. albojubatus (CTA) and (viii) Caprini—A. lervia (ALE), O.aries (OAR), C. hircus (CHI). Species are color-coded according to their tribal affiliation. (PDF 71 kb).

Supplementary Figure 2

Representative mouse spermatocytes immunostained against SYCP3 (green) and RAD51 (red). In all cases the DNA is counterstained with DAPI (blue). (GIF 153 kb).

High resolution image (TIFF 8194 kb).

Supplementary Figure 3

Covariation between SC length and COs. SC lengths are positively correlated to the number of MLH1 foci detected per cell. The different species analyzed in Table 3 are included. (PDF 24 kb).

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Ruiz-Herrera, A., Vozdova, M., Fernández, J. et al. Recombination correlates with synaptonemal complex length and chromatin loop size in bovids—insights into mammalian meiotic chromosomal organization. Chromosoma 126, 615–631 (2017). https://doi.org/10.1007/s00412-016-0624-3

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00412-016-0624-3

Keywords

Search

Navigation