Differences in the meiotic pairing behavior of gonosomal heterochromatin between female and male Microtus agrestis: implications for the mechanism ofheterochromatin amplification on the X and Y

It is generally thought that pairing and recombination between the X and Y chromosome in eutherian mammals is important for the occurrence of normal m eiotic division and the production of functional gametes. Microtus agrestis is one of the examples whose giant and heterochromatin-rich sex chromosome s fail to establish a durable association at any stage of the first meiotic division in males. In contrast, in females, synapsis starts in the euchrom atic short arm and pairing progresses unidirectionally and continues until both X chromosomes have paired completely, as can be demonstrated by the us e of fluorescence in situ hybridization with a sequence confirmed to the no n-centromeric, gonosomal heterochromatin. However, compared with euchromati n, this association is apparently ephemeral and breaks off precociously in the pachytene and metaphase I stages. We demonstrate that a middle repetiti ve element is localized interspersed in the noncentromeric heterochromatin of both X and Y, except the telomeric region of the Y. No differences could be detected at the molecular level between male and female DNA, indicating that at least the bulk of these elements are organized in the same manner on the X and Y. Our data imply that the loss of synapsis and recombination between the X and Y might have preceded the process of heterochromatin ampl ification in the course of Microtinae evolution. Since asynapsed elements a re particularly susceptible to DNA strand breaks during prophase I, DNA rep air of double-strand breaks involving heterochromatic segments of the X and Y could have resulted in translocations of larger segments from the X to t he Y or vice verse during the course of chromosome evolution of the gonosom es, explaining the homology at the molecular level between the heterochroma tin of the asynaptic X and Ti in M. agrestis. Copyright (C) 2001 S, Karger AG, Basel.