Chromosome synapsis, recombination and epigenetic modification in rams heterozygous for metacentric chromosome 3 of the domestic sheep Ovis aries and acrocentric homologs of the argali Ovis ammon

Hybridization of domestic animal breeds with their wild relatives is a promising method for increasing the genetic diversity of farm animals. Resource populations derived from the hybridization of various breeds of domestic sheep with mouflon and argali are an important source of breeding material. The karyotypes of argali and domestic sheep differ for a Robertsonian translocation, which occurred in the common ancestor of mouflon and domestic sheep (Ovis aries) due to the centric fusion of chromosomes 5 and 11 of the argali (O. ammon) into chromosome 3 of sheep. It is known that heterozygosity for translocation can lead to synapsis, recombination and chromosome segregation abnormalities in meiosis. Meiosis in the heterozygotes for translocation that distinguishes the karyotypes of sheep and argali has not yet been studied. We examined synapsis, recombination, and epigenetic modification of chromosomes involved in this rearrangement in heterozygous rams using immunolocalization of key proteins of meiosis. In the majority of cells, we observed complete synapsis between the sheep metacentric chromosome and two argali acrocentric chromosomes with the formation of a trivalent. In a small proportion of cells at the early pachytene stage we observed delayed synapsis in pericentromeric regions of the trivalent. Unpaired sites were subjected to epigenetic modification, namely histone H2A.X phosphorylation. However, by the end of the pachytene, these abnormalities had been completely eliminated. Asynapsis was replaced by a nonhomologous synapsis between the centromeric regions of the acrocentric chromosomes. By the end of the pachytene, the γH2A.X signal had been preserved only at the XY bivalent and was absent from the trivalent. The translocation trivalent did not differ from the normal bivalents of metacentric chromosomes for the number and distribution of recombination sites as well as for the degree of centromeric and crossover interference. Thus, we found that heterozygosity for the domestic sheep chromosome 3 and argali chromosomes 5 and 11 does not cause significant alterations in key processes of prophase I meiosis and, therefore, should not lead to a decrease in fertility of the offspring from interspecific sheep hybridization.

Thepam1Gene Is Required for Meiotic Bouquet Formation and Efficient Homologous Synapsis in Maize (Zea maysL.)

The clustering of telomeres on the nuclear envelope (NE) during meiotic prophase to form the bouquet arrangement of chromosomes may facilitate homologous chromosome synapsis. The pam1 (plural abnormalities of meiosis 1) gene is the first maize gene that appears to be required for telomere clustering, and homologous synapsis is impaired in pam1. Telomere clustering on the NE is arrested or delayed at an intermediate stage in pam1. Telomeres associate with the NE during the leptotene-zygotene transition but cluster slowly if at all as meiosis proceeds. Intermediate stages in telomere clustering including miniclusters are observed in pam1 but not in wild-type meiocytes. The tight bouquet normally seen at zygotene is a rare event. In contrast, the polarization of centromeres vs. telomeres in the nucleus at the leptotene-zygotene transition is the same in mutant and wild-type cells. Defects in homologous chromosome synapsis include incomplete synapsis, nonhomologous synapsis, and unresolved interlocks. However, the number of RAD51 foci on chromosomes in pam1 is similar to that of wild type. We suggest that the defects in homologous synapsis and the retardation of prophase I arise from the irregularity of telomere clustering and propose that pam1 is involved in the control of bouquet formation and downstream meiotic prophase I events.

Pericentric inversion in natural populations of Oligoryzomys nigripes (Rodentia: Sigmodontinae)

We analysed polymorphism for pericentric inversion in chromosome 3 of Oligoryzomys nigripes (Rodentia: Sigmodontinae) in several populations in Brazil and examined the meiotic behaviour of this chromosome in heterozygotes. We observed an orderly pairing of all chromosomes at pachytene in heterozygotes for the inverted chromosome 3. No indication of meiotic arrest and germ-cell death was found. Electron microscopy of synaptonemal complexes and conventional meiotic analysis indicated strictly nonhomologous synapsis and crossing-over suppression in the inverted region in the heterozygotes, which prevent the formation of unbalanced gametes. Thus, the pericentric inversion in chromosome 3 does not apparently result in any selective disadvantages in heterozygous carriers. In the majority of the populations studied, the frequencies of acrocentric homozygotes, metacentric homozygotes, and heterozygotes were in Hardy–Weinberg equilibrium. However, in some populations, we detected an excess of heterozygotes and a deficiency of acrocentric homozygotes.Key words: chromosome rearrangements, inversion, meiosis, Oligoryzomys nigripes.

Chiasma redistribution in the presence of different sized supernumerary segments in a grasshopper: dependence on nonhomologous synapsis

Eight different sized supernumerary segments located at distal ends of the long arms of chromosomes M4, M5, M6, and S8 of the grasshopper Stenobothrus festivus were studied in males with regard to the synaptic process and chiasma distribution in the bivalents that carry them. The M4, M5, and M6 bivalents heterozygous for extra segments were always monochiasmate, in contrast to their bichiasmate condition observed in basic homozygotes. Furthermore, the presence of any of these extra segments led to chiasma redistribution in the carrier bivalents, so that such chiasmata were formed preferentially further away from the extra segment. The intensity of this effect is dependent on the size of the segment. Not all heteromorphic bivalents exhibited synaptonemal complexes with equalized axes at pachytene, but there was always a variable proportion of heterosynapsis around the distal ends of the long arms that was dependent on both the size of the segment and the size of the carrier chromosome. It is proposed that the absence of chiasmata in nonhomologous synapsed regions is responsible for the results obtained. Length measurements of the different extra segments and their carrier chromosomes between pachytene and diplotene indicated that synaptonemal complex is underrepresented in supernumerary heterochromatin.Key words: chiasma distribution, grasshopper, heterosynapsis, supernumerary segment, synaptonemal complex.

Nonhomologous synapsis and reduced crossing over in a heterozygous paracentric inversion in Saccharomyces cerevisiae.

Homologous chromosome synapsis ("homosynapsis") and crossing over are well-conserved aspects of meiotic chromosome behavior. The long-standing assumption that these two processes are causally related has been challenged recently by observations in Saccharomyces cerevisiae of significant levels of crossing over (1) between small sequences at nonhomologous locations and (2) in mutants where synapsis is abnormal or absent. In order to avoid problems of local sequence effects and of mutation pleiotropy, we have perturbed synapsis by making a set of isogenic strains that are heterozygous and homozygous for a large chromosomal paracentric inversion covering a well marked genetic interval and then measured recombination. We find that reciprocal recombination in the marked interval in heterozygotes is reduced variably across the interval, on average to approximately 55% of that in the homozygotes, and that positive interference still modulates crossing over. Cytologically, stable synapsis across the interval is apparently heterologous rather than homologous, consistent with the interpretation that stable homosynapsis is required to initiate or consummate a large fraction of the crossing over observed in wild-type strains. When crossing over does occur in heterozygotes, dicentric and acentric chromosomes are formed and can be visualized and quantitated on blots though not demonstrated in viable spores. We find that there is no loss of dicentric chromosomes during the two meiotic divisions and that the acentric chromosome is recovered at only 1/3 to 1/2 of the expected level.

Synaptic adjustment of inversion loops in Neurospora crassa.

Heterozygotes for three long inversions on chromosome 1 were analyzed by serial reconstruction from electron micrographs. Measurements of loop lengths at different meiotic prophase substages revealed that the homologous synapsis of the inverted region was gradually replaced by nonhomologous synapsis as loops were eliminated during pachytene. This synaptic adjustment was apparently not affected by crossovers which occurred within the 150- and 160-cM long loops.

G-band position effects on meiotic synapsis and crossing over.

An examination of synaptic data from a series of X-autosome translocations and crossover data from an extensive series of autosome-autosome translocations and autosomal inversions in mice has lead to the development of a hypothesis which predicts synaptic and recombinational behavior of chromosomal aberrations during meiosis. This hypothesis predicts that in heterozygotes for chromosomal rearrangements that meiotically align G-light chromatin with G-light chromatin lack of homology will be recognized. If homologous synapsis cannot proceed, synaptonemal complex formation will cease and there will be no physical suppression of crossing over in such rearrangements. However, if a chromosomal rearrangement aligns G-light chromatin with G-dark chromatin at the time of synapsis, lack of homology will not be recognized and synaptonemal complex formation will proceed nonhomologously through the G-dark chromatin. Crossing over will be physically suppressed in this region and this suppression of crossing over will be confined to the chromosome in which the G-light chromatin is nonhomologously synapsed with G-dark chromatin. When G-light chromatin is once again aligned with G-light chromatin, lack of homology again will be recognized and either homologous synapsis will be reinitiated (as in an inversion loop), or will cease altogether (as in some translocations). Unlike the previously described "synaptic adjustment", this nonhomologous synapsis of G-light with G-dark chromatin appears to compete with homologous synapsis during early pachynema.