All Paired Up with No Place to Go: Pairing, Synapsis, and DSB Formation in a Balancer Heterozygote

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Abstract
The multiply inverted X chromosome balancer FM7 strongly suppresses, or eliminates, the occurrence of crossing over when heterozygous with a normal sequence homolog. We have utilized the LacI-GFP: lacO system to visualize the effects of FM7 on meiotic pairing, synapsis, and double-strand break formation in Drosophila oocytes. Surprisingly, the analysis of meiotic pairing and synapsis for three lacO reporter couplets in FM7/X heterozygotes revealed they are paired and synapsed during zygotene/pachytene in 70%–80% of oocytes. Moreover, the regions defined by these lacO couplets undergo double-strand break formation at normal frequency. Thus, even complex aberration heterozygotes usually allow high frequencies of meiotic pairing, synapsis, and double-strand break formation in Drosophila oocytes. However, the frequencies of failed pairing and synapsis were still 1.5- to 2-fold higher than were observed for corresponding regions in oocytes with two normal sequence X chromosomes, and this effect was greatest near a breakpoint. We propose that heterozygosity for breakpoints creates a local alteration in synaptonemal complex structure that is propagated across long regions of the bivalent in a fashion analogous to chiasma interference, which also acts to suppress crossing over. One of the more intriguing mysteries in chromosome biology lies in the ability of homologous chromosomes to pair during meiosis, the process that creates haploid gametes. This pairing is the crucial first step in seeing to it that each gamete receives one, and only one, copy of each chromosome. The later steps in this process include recombination and the actual segregation of paired homologs into different daughter cells. During the last century of study, people who worked on meiosis believed that changes in chromosome structure that disrupted the meiotic processes did so by impeding the pairing process. Here the authors show that pairing occurs quite normally even in cells carrying a highly rearranged chromosome. Surprisingly, even recombination is normally initiated, but not completed. These data are allowing them to reconsider several old and cherished views of the process called meiosis.