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Unequal crossing over and heterochromatin exchange in the X-Y bivalents of the deer mouse,Peromyscus beatae

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Abstract

Differences in length of the heterochromatic short arms of the X and Y chromosomes in individuals ofPeromyscus beatae are hypothesized to result from unequal crossing over. To test this hypothesis, we examined patterns of synapsis, chiasma formation, and segregation for maleP. beatae which were either heterozygous or homozygous for the amount of short-arm sex heterochromatin. Synaptonemal complex analysis demonstrated that mitotic differences in heterochromatic shortarm lengths between the X and Y chromosomes were reflected in early pachynema as corresponding differences in axial element lengths within the pairing region of the sex bivalent. These length differences were subsequently eliminated by synaptic adjustment such that by late pachynema, the synaptonemal complex configurations of the XY bivalent of heterozygotes were not differentiable from those of homozygotes. Crossing over between the heterochromatic short arms of the XY bivalent was documented by the routine appearance of a single chiasma in this region during diakinesis/metaphase I. Sex heterochromatin heterozygotes were characterized by the presence of asymmetrical chiasma between the X and Y short arms at diakinesis/metaphase I and sex chromosomes with unequal chromatid lengths at metaphase II. These data corroborate our hypothesis on the role of unequal crossing over in the production and propagation of X and Y heterochromatin variation and suggest that, in some cases, crossing over can occur during the process of synaptic adjustment.

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References

  • Allen JW (1979) BrdU-dye characterization of late replication and meiotic recombination in Armenian hamster germ cells. Chromosoma 74:189–207

    Google Scholar 

  • Arrighi FE, Hsu TC, Pathak S, Sawada H (1974) The sex chromosomes of the Chinese hamster: Constitutive heterochromatin deficient in repetitive DNA sequences. Cytogenet Cell Genet 13:268–274

    Google Scholar 

  • Baker RJ, Haiduk MW, Robbins LW, Cadena A, Koop BF (1982) Chromosomal studies of South American bats and their systematic implications. In: Mare MA, Genoways HH (eds) Mammalian biology in South America. University of Pittsburgh Press, Pittsburgh, pp 303–327

    Google Scholar 

  • Baverstock PR, Watts CHS, Hogarth JT (1977) Polymorphism of the X-chromosome, Y-chromosome and autosomes in the Australian hopping mice,Notomys alexis, N. cervinus andN. fuscus (Rodentia, Muridae). Chromosoma 61:234–256

    Google Scholar 

  • Buckle V, Mondello C, Darling S, Craig IW, Goodfellow PN (1985) Homologous expressed genes in the human sex chromosome pairing region. Nature 317:739–741

    Google Scholar 

  • Burgos M, Jiménez R, Olmos DM, Diaz de la Guardia R (1988) Heterogeneous heterochromatin and size variation in the sex chromosomes ofMicrotus cabrerae. Cytogenet Cell Genet 47:75–79

    Google Scholar 

  • Burgoyne PS (1982) Genetic homology and crossing over in the X and Y chromosomes of mammals. Hum Genet 61:85–90

    Google Scholar 

  • Chandley AC, Goetz P, Hargreave TB, Joseph AM, Speed RM (1984) On the nature and extent of XY pairing at meiotic prophase in man. Cytogenet Cell Genet 38:241–247

    Google Scholar 

  • Coen ES, Dover GA (1983) Unequal exchanges and the coevolution of X and Y rDNA arrays inDrosophila melanogaster. Cell 33:849–855

    Google Scholar 

  • Committee for the Standardization of Chromosomes of Peromyscus (1977) Standardized karyotype of deer mice,Peromyscus (Rodentia). Cytogenet Cell Genet 19:38–43

    Google Scholar 

  • Cooke HJ, Brown WR, Rappold GA (1985) Hypervariable telomeric sequences from the human sex chromosomes are pseudoautosomal. Nature 317:687–692

    Google Scholar 

  • Counce SJ, Meyer GF (1973) Differentiation of the synaptonemal complex and the kinetochore inLocusta spermatocytes studied by whole mount electron microscopy. Chromosoma 44:231–253

    Google Scholar 

  • Davis KM, Smith SA, Greenbaum IF (1986) Evolutionary implications of chromosomal polymorphisms in populations ofPeromyscus boylii from southwestern Mexico. Evolution 40:645–649

    Google Scholar 

  • Evans EP, Breckon G, Ford CE (1964) An air-drying method of meiotic preparations from mammalian testes. Cytogenetics 3:289–294

    Google Scholar 

  • Evans EP, Burtenshaw MD, Cattanach BM (1982) Meitoic crossing-over between the X and Y chromosomes of male mice carrying the sex-reversing (Sxr) factor. Nature 300:443–445

    Google Scholar 

  • Goodfellow PJ, Darling SM, Thomas NS, Goodfellow PN (1986) A pseudoautosomal gene in man. Science 234:740–743

    Google Scholar 

  • Greenbaum IF, Baker RJ (1978) Determination of the primative karyotype forPeromyscus. J Mammal 59:820–834

    Google Scholar 

  • Greenbaum IF, Hale DW, Fuxa KP (1986) The mechanism of autosomal synapsis and the substaging of zygonema and pachynema from deer mouse spermatocytes. Chromosoma 93:203–212

    Google Scholar 

  • Gunn SJ, Greenbaum IF (1986) Systematic implications of karyotypic variation in mainlandPeromyscus from the Pacific Northwest. J Mammal 67:294–304

    Google Scholar 

  • Hale DW (1988) Cytogenetic analysis of chromosomal heterozygosity in thePeromyscus maniculatus species group. PhD Dissertation, Texas A&M University, College Station, p xi + 114

    Google Scholar 

  • Hale DW, Greenbaum IF (1986) The behavior and morphology of the X and Y chromosomes during prophase I in the Sitka deer mouse (Peromyscus sitkensis). Chromosoma 94:235–242

    Google Scholar 

  • Harbers K, Soriano P, Müller U, Jaenisch R (1986) High frequency of unequal recombination in pseudoautosomal region shown by proviral insertion in transgenic mouse. Nature 324:682–685

    Google Scholar 

  • Hilwig I, Gropp A (1972) Staining of constitutive heterochromatin in mammalian chromosomes with a new fluorochrome. Expl Cell Res 75:122–126

    Google Scholar 

  • Houseal TW, Greenbaum IF, Schmidly DJ, Smith SA, Davis KM (1987) Karyotypic variation inPeromyscus boylii from Mexico. J Mammal 68:281–296

    Google Scholar 

  • Howell WM, Black DA (1980) Controlled silver staining of nucleolus organizer regions with a protective colloidal developer: A 1-step method. Experientia 36:1014

    Google Scholar 

  • John B (1976) Myths and mechanisms of meiosis. Chromosoma 54:295–325

    Google Scholar 

  • John B (1988) The biology of heterochromatin. In: Verma RS (ed) Heterochromatin: Molecular and structural aspects. Cambridge Univ Press, Cambridge, pp 1–147

    Google Scholar 

  • Keitges EA, Schorderet DF, Gartler SM (1987) Linkage of the steroid sulfatase gene to the Sex-reversed mutation in the mouse. Genetics 116:465–468

    Google Scholar 

  • Kurnit DM (1979) Satellite DNA and heterochromatin variants: The case for unequal mitotic crossing over. Hum Genet 47:169–186

    Google Scholar 

  • Lee MR, Elder FFB (1980) Yeast stimulation of bone marrow mitosis for cytogenetic investigations. Cytogenet Cell Genet 26:36–40

    Google Scholar 

  • Miklos GLG, John B (1979) Heterochromatin and satellite DNA in man: Properties and prospects. Am J Hum Genet 31:264–280

    Google Scholar 

  • Moses MJ (1977) Synaptonemal complex karyotyping in spermatocytes of the chinese hamster (Cricetulus griseus) I. Morphology of the autosomal complement in spread preparations. Chromosoma 60:99–125

    Google Scholar 

  • Moses MJ, Poorman PA, Roderick TH, Davisson MT (1982) Synaptonemal complex analysis of mouse chromosomal rearrangements IV. Synapsis and synaptic adjustment in two paracentric inversions. Chromosoma 84:457–474

    Google Scholar 

  • Mürer-Orlando M, Richer CL (1983) Heterochromatin heterogeneity in Chinese hamster sex bivalents. Cytogenet Cell Genet 35:195–199

    Google Scholar 

  • Page DC, de la Chapelle A, Weissenbach J (1986) Chromosome Y-specific DNA in related human XX males. Nature 315:224–226

    Google Scholar 

  • Pathak S, Hsu TC, Arrighi FE (1973) Chromosomes ofPeromyscus (Rodentia, Cricetidae) IV. The role of heterochromatin in karyotype evolution. Cytogenet Cell Genet 12:315–326

    Google Scholar 

  • Petit C, de la Chapelle A, Castillo S, Noël B, Weissenbach J (1987) An abnormal terminal X-Y interchange accounts for most but not all cases of human XX maleness. Cell 49:595–602

    Google Scholar 

  • Rao SRV, Vasantha K, Thelma BK, Joyal RC, Jhanwar SC (1983) Heterochromatin variation and sex chromosome polymorphism inNesokia indica: A population study. Cytogenet Cell Genet 35:233–237

    Google Scholar 

  • Rogers DS, Greenbaum IF, Gunn SJ, Engstrom MD (1984) Cytosystematic value of chromosomal inversion data in the genusPeromyscus (Rodentia: Cricetidae). J Mammal 65:457–465

    Google Scholar 

  • Rouyer F, Simmler M-C, Johnsson C, Vergnaud G, Cooke HJ, Weissenbach J (1986) A gradient of sex linkage in the pseudoautosomal region of the human sex chromosomes. Nature 319:291–295

    Google Scholar 

  • Satya-Prakash KL, Aswathanarayana NV (1984) Behavior of sex chromosomes during meiosis in the house shrew. J Hered 75:149–150

    Google Scholar 

  • Schmid M, Johannisson R, Haaf T, Neitzel H (1987) The chromosomes ofMicromys minutus (Rodentia, Murinae). II. Pairing pattern of X and Y chromosomes in meiotic prophase. Cytogenet Cell Genet 45:121–131

    Google Scholar 

  • Schmidly DJ, Cato P, Bradley RD (1988) Morphometric differentiation and taxonomy of chromosomally characterized populations ofPeromyscus boylii from east-central Mexico. J Mammal 69:462–480

    Google Scholar 

  • Schweizer D, Ambros P, Andrle M (1978) Modification of DAPI banding on human chromosomes by prestaining with a DNA-binding oligopeptide antibiotic, distamycin A. Expl Cell Res 111:327–332

    Google Scholar 

  • Seabright M (1971) A rapid banding technique for human chromosomes. Lancet ii:971–972

    Google Scholar 

  • Sharma T, Raman R (1973) Variation of constitutive heterochromatin in the sex chromosomes of the rodentBandicota bengalensis bengalensis (Gray). Chromosoma 41:75–84

    Google Scholar 

  • Smith GP (1976) Evolution of repeated DNA sequences by unequal crossing over. Science 191:528–535

    Google Scholar 

  • Smith SA, Bradley RD, Greenbaum IF (1986) Karyotypic conservatism in thePeromyscus mexicanus group. J Mammal 67:584–586

    Google Scholar 

  • Solari AJ (1974) The relationship between chromosomes and axes in the chiasmatic XY pair of the Armenian hamster (Cricetulus migratorius). Chromosoma 48:89–109

    Google Scholar 

  • Soriano P, Keitges EA, Schorderet DF, Harbers K, Gartler SM, Jaenisch R (1987) High rate of recombination and double crossovers in the mouse pseudoautosomal region during male meiosis. Proc Natl Acad Sci USA 84:7218–7220

    Google Scholar 

  • Stack S, Anderson L (1986) Two-dimensional spreads of synaptonemal complexes from solanaceous plants. III. Recombination nodules and crossing over inLycopersicon esculentum (tomato). Chromosoma 94:253–258

    Google Scholar 

  • Stangl FB Jr, Baker RJ (1984) Evolutionary relationships in Peromyscus: congruence in chromosomal, genic and classical data sets. J Mammal 65:643–654

    Google Scholar 

  • Sudman PD (1990) Cryogenic preservation of testicular material for synaptonemal complex analysis. Cytogenet Cell Genet 52:88–89

    Google Scholar 

  • Sudman PD, Greenbaum IF (1989) Visualization of kinetochores in mammalian meiotic preparations and observations of argentophilic differences between mitotic and meiotic kinetochores. Genome 32:380–382

    Google Scholar 

  • Sumner AT (1972) A simple technique for demonstrating centromeric heterochromatin. Exp Cell Res 75:304–306

    Google Scholar 

  • Therman E, Kuhm EM (1976) Mitotic crossing-over and segregation in man. Hum Genet 59:93–100

    Google Scholar 

  • Vistorin G, Gamperl R, Rosenkranz W (1977) Studies on sex chromosomes of four hamster species:Cricetus cricetus, Cricetulus griseus, Mesocricetus auratus, andPhodopus sungorus. Cytogenet Cell Genet 18:24–32

    Google Scholar 

  • Wahlström J, Kyllerman M, Hansson A, Taranger J (1985) Unequal mitotic sister chromatid exchange and different length of Y chromosomes. Hum Genet 70:185–188

    Google Scholar 

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Sudman, P.D., Greenbaum, I.F. Unequal crossing over and heterochromatin exchange in the X-Y bivalents of the deer mouse,Peromyscus beatae . Chromosoma 99, 183–189 (1990). https://doi.org/10.1007/BF01731128

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  • DOI: https://doi.org/10.1007/BF01731128

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