Differential mechanisms governing segregation of a univalent in oocytes and spermatocytes of Drosophila melanogaster

Abstract

In tricomplex heterozygotes in Drosophila melanogaster three metacentric autosomes (the TRI chromosomes) appear as a trivalent in meiosis while one autosome consisting of two homologous arms attached to the same centromere (a compound) behaves as an obligatory univalent. Cytological analysis of meiosis of tri-complex heterozygotes indicates that in oocytes the univalent compound behaves non-independently in relation to segregation of the trivalent. The compound is distributed preferentially to the same pole as one TRI chromosome. In spermatocytes the compound is distributed at random. In some oocytes the directed segregation is shown to be due to a disjunctional interaction between the compound and one partner of the trivalent at the same time as the other two chromosomes of the trivalent are separating from each other. The basic difference between the segregational mechanisms in the two sexes is discussed with a review of evidence indicating that in males segregation is determined by physical linkage that produces a stable orientation of the homologues at metaphase I. On the other hand, both genetic and cytological evidence indicate that in females a physical linkage (a chiasma) is non-essential for maintenance of co-orientation and stability after the onset of prometaphase. Genetic and cytological evidence support the hypothesis that disjunction is predetermined by non-random arrangement of the centromeric regions of chromosomes in the chromocentre - a suprachromosomal organization characteristic of maturing oocytes.

Meiotic spindle assembly in Drosophila females: behavior of nonexchange chromosomes and the effects of mutations in the nod kinesin-like protein.

“…A previous genetic model (Grell, 1976) postulated that distributive segregation involved a second round of pairing and segregation which followed the segregation of exchange chromosomes. Our data and previous cytological studies (Puro and Nokkala, 1977;Kimble and Church, 1983 ;Puro, 1991) are not consistent with a second round of pairing, as nonexchange chromosomes are positioned toward opposite poles before the spindle has fully formed . More recently, Carpenter (1991) has proposed that nonexchange homologs are linked by a microtubule bridge which substitutes for chiasma .…”

“…We have found that nonexchange chromosomes are positioned between the metaphase plate and the spindle pole in a bilaterally symmetric manner (Fig . 3), confirming the conclusion that these chromosomes are prepositioned toward the spindle poles (Puro and Nokkala, 1977 ;Puro, 1991 ;Kimble and Church, 1983) . The two fourth chromosomes, identifiable by their small size, are positioned between the metaphase plate and the poles, while the remaining chromosomes are tightly massed at the metaphase plate ( Fig .…”

Spindle Dynamics during Meiosis in Drosophila Oocytes

“…The centrosomal protein, DMAP190 (CP190), was not found at the poles of the meiosis I spindle ( Theurkauf and Hawley 1992 ), but it has recently been reported to localize to a ring- or disk-shaped structure between the two tandem meiosis II spindles of Drosophila oocytes ( Riparbelli and Callaini, 1996 ). The ring-shaped structure in the central pole region of the Drosophila meiosis II spindles was observed previously ( Puro, 1991 ) and was suggested to function in pole organization for the second meiotic division. Nucleation and organization of microtubules for assembly of the Drosophila meiosis I and II spindles could therefore differ from one another and from anastral spindles of other organisms.…”

Partner choice in heterologous chromosome segregation of the Y chromosome in competitive situations in the oocyte of Drosophila melanogaster

“…Most recently Puro (1991) has shown by means of cytological observations that in female meiosis of Drosophila melanogaster disjunction of both chiasmate and achiasmate chromosomes is predetermined by nonrandom arrangement of the centromeric regions of chromosomes in the chromocenter. Further, he suggests that this kind of system may be sensitive to disturbing factors affecting the internal organization of the chromocenter.…”

“…Such disturbing factors might be the presence of extrachromosomal elements, and the structural heterozygosity dealt with in the present study. According to Puro (1991), non-homologous pairing may be viewed as a kind of spatial arrangement of centromeric regions within the framework of the suprachromosomal organization, the chromocenter, characteristic of meiosis in oocytes in D. melanogaster.…”