Nonrandom Chromosome Arrangements in Germ Line Nuclei of Sciara coprophila Males: The Basis for Nonrandom Chromosome Segregation on the Meiosis I Spindle

Meiosis I in males of the Dipteran $ciara coprophila results in the nonrandom distribution of maternally and paternally derived chromosome sets to the two division products. Based on an earlier study (Kubai, D. E 1982. J. Cell Biol. 93:655-669), I suggested that the meiosis I spindle does not play a direct role in the nonrandom sorting of chromosomes but that, instead, haploid sets are already separated in prophase nuclei well before the onset of spindle formation. Here I report more direct evidence that this hypothesis is true; this evidence was gained from ultrastructural reconstruction analyses of the arrangement of chromosomes in germ line nuclei (prophase nuclei in spermatogonia and spermatocytes) of males heterozygous for an X-autosome chromosome translocation. Because of this translocation, the maternal and paternal chromosome sets are distinguishable, so it is possible to demonstrate that (a) the two haploid chromosome sets occupy distinct maternal and paternal nuclear compartments and that (b) nuclei are oriented so that the two haploid chromosome sets have consistent relationships to a well-defined cellular axis. The consequences of such nonrandom aspects of nuclear structure for chromosome behavior on premeiotic and meiotic spindles are discussed. T HE idea that chromosomes are arranged nonrandomly in interphase or prophase nuclei is an old one, first suggested by the work of Rabl (20) and Boveri (7) and supported by diverse evidence (for review see reference 2). In the last few years, the credibility of the idea has increased appreciably, due mainly to studies such as those by Ashley (1, 2) and Bennett (see review in reference 3) and their collaborators. These investigators have clearly documented cases in which chromosomes assume specific arrangements in nuclei and on the mitotic spindle, and they have shown how those arrangements can have important implications for chromosome behavior. Ashley and her associates, for example, found that the three chromosomes in the haploid complement of Ornithogalum virens usually exhibit a particular end-to-end order (1) and provided a model to show how the arrangement of two such haploid arrays in diploid nuclei could facilitate meiotic pairing (2). Bennett (3) and his co-workers discovered that in grasses the two haploid chromosome sets occupy separate domains on the mitotic spindle. In interspecies and intergeneric hybrids, one parental chromosome set is nearer the outside of the spindle, concentric with the second parent's chromosomes. Such hybrids tend to lose chromosomes derived from one parent, the very parent that contributes chromosomes nearer the outside of the spindle. Thus, Bennett's observations suggest that nonrandom chromosome positioning on the spindle is causally linked to nonrandom chromosome loss. Another instance where a particular course of chromosome behavior and a particular arrangement of chromosomes within nuclei appear to be related occurs in the Dipteran Sciara coprophila. Here we are concerned with the perfectly nonrandom chromosome distribution that occurs during meiosis I in males. In this division, maternal chromosomes move poleward on a unique monopolar spindle, while paternal chromosomes remain in place, far from the spindle pole. As a result, all maternal chromosomes are transmitted to sperm and all paternal chromosomes are lost (for details see references 13 and 16). In my study of meiosis I in wildtype S. coprophila (13), I found that maternal and paternal chromosome sets are always in separate halves of the meiosis I spindle-maternals close to the pole and paternals far from i t even in the earliest stage examined. Moreover, I found indications that a similar segregation of maternal and paternal chromosomes exists in prophase nuclei, before the spindle forms. Consequently, I argued that the monopolar meiosis I spindle has no role in sorting chromosomes into maternal and paternal sets; it serves simply to increase the distance between chromosomes that were already nonrandomly arrayed in prophase nuclei. In this paper, I present more direct evidence that the peculiar nonrandom meiotic chromosome distribution characteristic of S. coprophila males is most likely dependent upon the nonrandom structure of premeiotic nuclei. This evidence was obtained by exploiting a translocation that alters chromosome sizes (10) so that in males heterozygous for the 9 The Rockefeller University Press, 0021-9525/87/12/2433/14 $2.00 The Journal of Cell Biology, Volume 105 (No. 6, Pt. I), Dec. 1987 2433-2446 2433 on M ay 4, 2017 D ow nladed fom Published December 1, 1987