Abstract
We examined A- and B-chromosome pairing and recombination in 12 males from the farm-bred population of the silver fox (2n = 34 + 0–10 Bs) by means of electron and immunofluorescent microscopy. To detect recombination at A and B chromosomes, we used immunolocalisation of MLH1, a mismatch repair protein of mature recombination nodules, at synaptonemal complexes. The mean total number of MLH1 foci at A-autosomes was 29.6 foci per cell. The XY bivalent had one MLH1 focus at the pairing region. Total recombination length of the male fox genome map was estimated as 1,530 centimorgans. We detected single MLH1 foci at 61% of linear synaptic configurations involving B chromosomes. The distribution of the foci along B- and A-bivalents was the same. This may be considered as a first molecular evidence that meiotic recombination does occur in mammalian B chromosomes. There was no correlation between the number of synaptic configurations involving B chromosomes per cell and the recombination rate of the A-genome.
Similar content being viewed by others
Abbreviations
- ACA:
-
Anti-centromere antibody
- BSA:
-
Bovine serum albumin
- cM:
-
Centimorgan
- DAPI:
-
4′-6-diamidino-2-phenylindole
- Cy3:
-
Orange fluorescing cyanine
- FITC:
-
Fluorescein isothiocyanate
- MLH1:
-
Homolog of prokaryotic mutL 1 mismatch repair protein
- PBS:
-
Phosphate buffered saline
- SC:
-
Synaptonemal complex
- SCP3:
-
Synaptonemal complex protein 3
- S.D.:
-
Standard deviation
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(4):1569–1579
Banaszek A, Jadwiszczak K (2006) B-chromosomes behavior during meiosis of yellow-necked mouse, Apodemus flavicollis. Folia Zool 55:113–122
Basheva EA, Bidau CJ, Borodin PM (2008) General pattern of meiotic recombination in male dogs estimated by MLH1 and RAD51 immunolocalization. Chromosome Res 16(5):709–719
Beliaev DK, Volobuev VT, Radzhabli SI, Trut LN (1974a) Investigation of the nature and the role of additional chromosomes in silver fox. II. Additional chromosomes and breeding of animals for behaviour. Genetika 10(8):83–97
Beliaev DK, Volobuev VT, Radzhabli SI, Trut LN (1974b) Polymorphism and mosaicism for additional chromosomes in silver foxes. Genetika 10(2):58–67
Bell G, Burt A (1990) B-chromosomes: germ-line parasites which induced changes in host recombination. Parasitology 100(Suppl):S19–S26
Bidau CJ (1987) Influence of a rare unstable B-chromosome on chiasma frequency and non-haploid sperm production in Dichroplus pratensis (Melanoplinae, Acrididae). Genetica 73:201–210
Bidau CJ, Rosato M, Martн DA (2004) FISH detection of ribosomal cistrons and assortment-distortion for X and B chromosomes in Dichroplus pratensis (Acrididae). Cytogenetic and genome research 106(2–4):295–301
Borodin PM, Karamysheva TV, Rubtsov NB (2007) Immunofluorescent analysis of meiotic recombination and interference in the domestic cat. Cell and Tissue Biology 1(6):503–507
Borodin PM, Karamysheva TV, Belonogova NM et al (2008) Recombination map of the common shrew, Sorex araneus (Eulipotyphla, Mammalia). Genetics 178(2):621–632
Borodin PM, Basheva EA, Zhelezova AI (2009) Immunocytological analysis of meiotic recombination in the American mink (Mustela vison). Anim Genet 40(2):235–238
Brandham PE, Bhattarai S (1977) The effect of B chromosome number on chiasma frequency within and between individuals of Gibasis linearis (Commelinaceae). Chromosoma 64(4):343–348
Camacho JP, Shaw MW, Lopez-Leon MD et al (1997) Population dynamics of a selfish B chromosome neutralized by the standard genome in the grasshopper Eyprepocnemis plorans. Am Nat 149(6):1030–1050
Camacho JP, Sharbel TF, Beukeboom LW (2000) B-chromosome evolution. Philos Trans R Soc Lond B Biol Sci 355(1394):163–178
Camacho JP, Bakkali M, Corral JM et al (2002) Host recombination is dependent on the degree of parasitism. Proc Biol Sci 269(1505):2173–2177
Camacho JP, Perfectti F, Teruel M et al (2004) The odd-even effect in mitotically unstable B chromosomes in grasshoppers. Cytogenet Genome Res 106(2–4):325–331
Codina-Pascual M, Campillo M, Kraus J et al (2006) Crossover frequency and synaptonemal complex length: their variability and effects on human male meiosis. Mol Hum Reprod 12(2):123–133
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(6):1353–1368
Graphodatsky AS, Kukekova AV, Yudkin DV et al (2005) The proto-oncogene C-KIT maps to canid B-chromosomes. Chromosome Res 13(2):113–122
Grieco ML, Bidau CJ (2000) The dicentric nature of the metacentric B chromosome of Metaleptea brevicornis adspersa (Acridinae, acrididae). Heredity 84(Pt 6):639–646
Hassold T, Judis L, Chan ER et al (2004) Cytological studies of meiotic recombination in human males. Cytogenet Genome Res 107(3–4):249–255
Howell WM, Black DA (1980) Controlled silver-staining of nucleolus organizer regions with a protective colloidal developer: a 1-step method. Experientia 36(8):1014–1015
Jimenez G, Manzanero S, Puertas MJ (2000) Relationship between pachytene synapsis, metaphase I associations, and transmission of 2B and 4B chromosomes in rye. Genome 43(2):232–239
Jones RN (1991) B-chromosome drive. American Naturalist 137(3):430–442
Jones RN (1995) B chromosomes in plants. New Phytologist 131(4):411–434
Jones R, Rees H (1967) Genotypic control of chromosome behaviour in rye. XI. The influence of B-chromosomes on meiosis. Heredity 22:333–347
Jones RN, Rees H (1982) B chromosomes. Academic, London; New York
Karamysheva TV, Andreenkova OV, Bochkaerev MN et al (2002) B chromosomes of Korean field mouse Apodemus peninsulae (Rodentia, Murinae) analysed by microdissection and FISH. Cytogenet Genome Res 96(1–4):154–160
Kolomiets OL, Borbiev TE, Safronova LD et al (1988) Synaptonemal complex analysis of B-chromosome behavior in meiotic prophase I in the East-Asiatic mouse Apodemus peninsulae (Muridae, Rodentia). Cytogenet Cell Genet 48(3):183–187
Kukekova AV, Trut LN, Oskina IN et al (2007) A meiotic linkage map of the silver fox, aligned and compared to the canine genome. Genome Res 17(3):387–399
Lynn A, Koehler KE, Judis L et al (2002) Covariation of synaptonemal complex length and mammalian meiotic exchange rates. Science 296(5576):2222–2225
Matsubara K, Yamada K, Umemoto S et al (2008) Molecular cloning and characterization of the repetitive DNA sequences that comprise the constitutive heterochromatin of the A and B chromosomes of the Korean field mouse (Apodemus peninsulae, Muridae, Rodentia). Chromosome Res 16(7):1013–1026
Perfectti F, Corral JM, Mesa JA et al (2004) Rapid suppression of drive for a parasitic B chromosome. Cytogenet Genome Res 106(2–4):338–343
Peters AH, Plug AW, van Vugt MJ, de Boer P (1997) A drying-down technique for the spreading of mammalian meiocytes from the male and female germline. Chromosome Res 5(1):66–68
Radzhabli SI, Isaenko AA, Volobuev VT (1978) Nature and role of accessory chromosomes in silver-gray foxes. IV. The behavior of accessory chromosomes in meiosis. Genetika 14(3):438–443
Rees H, Dale PJ (1974) Chiasmata and variability in Lolium and Festuca populations. Chromosoma 47(3):335–351
Reeves A (2001) MicroMeasure: a new computer program for the collection and analysis of cytogenetic data. Genome 44(3):439–443
Rice WR (1994) Degeneration of a nonrecombining chromosome. Science 263(5144):230–232
Rubtsov NB, Karamysheva TV, Andreenkova OV et al (2004) Comparative analysis of micro and macro B chromosomes in the Korean field mouse Apodemus peninsulae (Rodentia, Murinae) performed by chromosome microdissection and FISH. Cytogenet Genome Res 106(2–4):289–294
Santos JL, Del Cerro AL, Fernandez A, Diez M (1993) Meiotic behaviour of B chromosomes in the grasshopper Omocestus burri: A case of drive in females. Hereditas 118(3):139
Shi L, Tang L, Ma K, Ma C (1988) Synaptonemal complex formation among supernumerary B chromosomes: an electron microscopic study on spermatocytes of Chinese raccoon dogs. Chromosoma 97(2):178
Sun F, Oliver-Bonet M, Liehr T et al (2006) Variation in MLH1 distribution in recombination maps for individual chromosomes from human males. Hum Mol Genet 15(15):2376–2391
Switonsky M, Gustavsson I, Hoejer K, Ploeen L (1987) Synaptonemal complex analysis of the B chromosomes in spermatocytes of the silver fox (Vulpes fulvus Desm.). Cytogenet Cell Genet 45:84–92
Tanic N, Dedovic N, Vujosevic M, Dimitrijevic B (2000) DNA profiling of B chromosomes from the yellow-necked mouse Apodemus flavicollis (Rodentia, Mammalia). Genome Res 10(1):55–61
Trifonov VA, Perelman PL, Kawada SI et al (2002) Complex structure of B-chromosomes in two mammalian species: Apodemus peninsulae (Rodentia) and Nyctereutes procyonoides (Carnivora). Chromosome Res 10(2):109–116
Ward EJ (1976) The effect of accessory chromatin on chiasma distribution in maize. Can J Genet Cytol 18(3):479–484
Yang F, O'Brien PCM, Milne BS et al (1999) A complete comparative chromosome map for the dog, red fox, and human and its integration with canine genetic maps. Genomics 62(2):189
Yudkin DV, Trifonov VA, Kukekova AV et al (2007) Mapping of KIT adjacent sequences on canid autosomes and B chromosomes. Cytogenet Genome Res 116(1–2):100–103
Acknowledgements
This work was supported by research grants from the Russian Foundation for Basic Research and Russian Ministry of Science and Education, the Programs of Russian Academy of Sciences “Biosphere Origin and Evolution” and “Biodiversity”. We thank Mrs. Marina Rodionova for her help in SC spreading, Prof. Ludmila Trut for valuable discussion and the Microscopic Center of the Siberian Department of the Russian Academy of Sciences for granting access to microscopic equipment.
Author information
Authors and Affiliations
Corresponding author
Additional information
Responsible Editor: Walther Traut.
Rights and permissions
About this article
Cite this article
Basheva, E.A., Torgasheva, A.A., Sakaeva, G.R. et al. A- and B-chromosome pairing and recombination in male meiosis of the silver fox (Vulpes vulpes L., 1758, Carnivora, Canidae). Chromosome Res 18, 689–696 (2010). https://doi.org/10.1007/s10577-010-9149-4
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10577-010-9149-4