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

Abstract

Differences in length of the heterochromatic short arms of the X and Y chromosomes in individuals of Peromyscus beatae are hypothesized to result from unequal crossing over. To test this hypothesis, we examined patterns of synapsis, chiasma formation, and segregation for male P. beatae which were either heterozygous or homozygous for the amount of short-arm sex heterochromatin. Synaptonemal complex analysis demonstrated that mitotic differences in heterochromatic short-arm 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.

Sex chromosomes polymorphisms inOryzomysaff.subflavus(Cricetidae, Rodentia) from Central Brazil

“…eliurus (FURTADO 1981) and in 0. nigripes (ALMEIDA and YONENAGA-YASSUDA 1991). Recently, SunMAN and GREENBAUM (1990) demonstrated that unequal crossing overs between the heterochromatic short arms of the X and Y chromosomes are responsible for the production and propagation of polymorphisms in the sexual pair of Peromyscus beatae.…”

Sex Chromosomes, Heterochromatin, and Retrotransposon Accumulation in Deer Mice

“…In Peromyscus, the heterochromatic short arm ofthe X chromosome and a corresponding arm of the heterochromatic Y chromosome comprise the pseudoautosomal region (Hale and Greenbaum, 1986;Sudman and Greenbaum, 1990;Hale et al, 1991;Fig. I).…”

“…Because genetic and molecular markers are not available for the pseudoautosomal region of the deer mouse, the possibility that X-Y recombination is limited to a very small segment within this region cannot be summarily excluded. The random distribution of chiasmata observed within the heterochromatic pseudoautosomal segments in deer mice (Hale and Greenbaum, 1986;Sudman and Greenbaum, 1990;Hale et al, 1991) and other rodent species (Murer-Orlando and Richer, 1983;Schmid et al, 1987;Latos-Bielenska and Vogel, 1992) could simply reflect progressive terminalization from a small recombinational hotspot located near the X and Y centromeres. However, cytogenetic data from populations of P. beatae exhibiting quantitative variation for the amount of pseudoautosomal heterochromatin clearly indicate that meiotic crossing over occurs throughout the pseudoautosomal region (Sudman and Greenbaum, 1990).…”

“…The random distribution of chiasmata observed within the heterochromatic pseudoautosomal segments in deer mice (Hale and Greenbaum, 1986;Sudman and Greenbaum, 1990;Hale et al, 1991) and other rodent species (Murer-Orlando and Richer, 1983;Schmid et al, 1987;Latos-Bielenska and Vogel, 1992) could simply reflect progressive terminalization from a small recombinational hotspot located near the X and Y centromeres. However, cytogenetic data from populations of P. beatae exhibiting quantitative variation for the amount of pseudoautosomal heterochromatin clearly indicate that meiotic crossing over occurs throughout the pseudoautosomal region (Sudman and Greenbaum, 1990). In male P. beatae heterozygous for the amount ofpseudoautosomal heterochromatin (i.e., the pseudoautosornal-region length of one sex chromosome was substantially different than that of the other sex chromosome), unequal X-Y recombination and heterochromatin exchange during prophase I generate quantitative variation in the size of the pseudoautosomal arms in metaphase II configurations and, ultimately, in offspring.…”

“…In male P. beatae heterozygous for the amount ofpseudoautosomal heterochromatin (i.e., the pseudoautosornal-region length of one sex chromosome was substantially different than that of the other sex chromosome), unequal X-Y recombination and heterochromatin exchange during prophase I generate quantitative variation in the size of the pseudoautosomal arms in metaphase II configurations and, ultimately, in offspring. This continuous length variation can be explained only by crossing over throughout the pseudoautosomal heterochromatin of heterozygous X-Y bivalents (Sudman and Greenbaum, 1990;P. D. Sudman, pers.…”