Spatial arrangement of the animal male germ cell genome: IV. Radiation-induced locus-specific translocations (2;3) and large-scale organization of Drosophila sperm nucleus

Abstract

At the previous papers (Alexandrov et al., 2007b, 2008), the specific megarosette-loop organization (but not polar-linear Rabl-configuration) of major haploid autosome 2 in Drosophila sperm nucleus has been proposed and experimentally substantiated by analysis of radiation-induced locus-specific inversions showing highly nonrandomly distribution of the second inversion breakpoints over the entire autosome. We have speculated that spatial organization of the other major chromosomes in Drosophila sperm nucleus must be the same. To test this expectations, the nature and frequency of radiation-induced interchromosomal exchanges (reciprocal translocations) between autosomes 2 and 3 with the first breaks invariantly associated with the same genetic loci (black or vestigial) on the autosome 2 were studied and, at once, the distribution patterns of the second translocation breakpoints over the entire autosome 3 were detected. Analysis of 23 translocations scored has shown that both black and vestigial loci highly non-randomly interact with certain, including pericentromeric heterochromatin, “hot” areas of autosome 3. Surprisingly, positioning of these areas found to be co-linear with that of “hot” areas for inversion breakpoints on the autosome 2 if both euchromatic arms and pericentromeric heterochromatic regions of two major autosomes arrange in parallel to each other, showing thereby that spatial organization of both autosomes 2 and 3 goes on concurrently with space and time. Using these data, 2D and 3D models of spatial arrangement of autosome 3 in Drosophila haploid sperm nucleus were constructed the principle features of which found to be well consistent with the megarosette-loop configuration proposed for the second chromosome. Independent reciprocal translocations (2;3) scored in the genome of the eight radiation-induced “point” black or vestigial mutants turned out to have the breakpoints within the autosomes 2 and 3 areas proximity of which is predetermined by the megarosette-loop configuration of these major chromosomes. These results show that approaches of the classical radiation cytogenetics and genetics employed in our genomic investigations may be useful strategy to assist in the elucidation of the other conceptual point in the dynamics of sperm nucleus as a self-organizing system, namely, whether the chromatic protein remodeling (histon -to- protamine transition) in late spermatids is coupled with the structural reorganization of primary polar-linear Rabl’s state of chromosomes in the early post-meiotic spermatids into the compact megarosette-loop structures in the fully mature spermatozoa.