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

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.

Retention of Induced Mutations in a Drosophila Reverse-Genetic Resource

“…The prevention of recombination and loss of mutant alleles is the major reason that balancer chromosomes contain multiple inversions, because rearrangement breakpoints suppress recombination (Gong et al 2005). It follows that alleles closer to rearrangement breakpoints will be less likely to undergo reciprocal recombination or gene conversion in heterozygotes.…”

Components of the RNAi Machinery That Mediate Long-Distance Chromosomal Associations Are Dispensable for Meiotic and Early Somatic Homolog Pairing inDrosophila melanogaster

“…In fact, in the somatic tissues of broader Dipterans, homologous chromosomes are paired (Metz 1916;Hiraoka et al 1993;Fung et al 1998). Thus, it has been proposed that somatic and meiotic pairing in Drosophila are achieved by the same mechanism and that meiotic pairing is simply an extension of pairing established in the mitotically dividing germline (Stevens 1908;Brown and Stack 1968;Vazquez et al 2002;Gong et al 2005;Sherizen et al 2005). The mechanism underlying the pairing interaction is thought to be mediated either directly by nucleic acid homology [through either direct DNA-DNA interactions (i.e., Wilson 1979, McGavin 1989 or interactions that may include transcribed RNA] or indirectly through protein-protein interactions (Comings and Riggs 1971;Gemkow et al 1998;Phillips et al 2005;Fritsch et al 2006;Phillips and Dernburg 2006).…”

The diverse roles of transverse filaments of synaptonemal complexes in meiosis

“…, which is effectively a null allele, still display homolog alignment; however, maintenance of alignment in euchromatic regions and sister chromatid arm cohesion appear to be affected (Gong et al 2005;Sherizen et al 2005). Furthermore, meiotic DSBs are reduced, though not eliminated (Jang et al 2003), and CO formation is abolished (Page and Hawley 2001, and references therein).…”

“…Similar to other species, TFs appear to create favorable preconditions for CO formation in Drosophila. Specifically, uninterrupted synapsis between defined boundaries on Drosophila chromosomes appear to promote CO formation (Gong et al 2005;Sherizen et al 2005).…”