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All paired up with no place to go: pairing, synapsis, and DSB formation in a balancer heterozygote.

Gong WJ, McKim KS, Hawley RS - PLoS Genet. (2005)

Bottom Line: 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.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.

View Article: PubMed Central - PubMed

Affiliation: Stowers Institute for Medical Research, Kansas City, Missouri, United States of America.

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.

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Related in: MedlinePlus

Synapsed and Unsynapsed lacO Sites in X/X (10A/11A) OocytesNote that in the lower (unsynapsed) case, the two GFP foci are displaced along the length of the same stretch of SC. In these images, which consist of one to two optical sections, two GFP foci (green) are associated with a segment of SC (red). Distances between those GFP foci are shown at the right-most in each row. Bars = 1 μm.
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pgen-0010067-g004: Synapsed and Unsynapsed lacO Sites in X/X (10A/11A) OocytesNote that in the lower (unsynapsed) case, the two GFP foci are displaced along the length of the same stretch of SC. In these images, which consist of one to two optical sections, two GFP foci (green) are associated with a segment of SC (red). Distances between those GFP foci are shown at the right-most in each row. Bars = 1 μm.

Mentions: The analysis presented above assumes that if two lacO arrays were frequently separated, even by small distances, we would still be able to visualize them as two separate dots. To estimate the effect of displacing two lacO arrays on the separation of GFP foci, we also assessed pairing and synapsis in X/X females carrying a lacO insertion at position 10A on one homolog and a lacO insertion at position 11A on the other. These two sites are separated by a physical distance of 0.9 Mb. Figure 4 presents examples of two nuclei in which the two foci were associated with a stretch of SC. In the upper case the two GFP foci were opposite from each other across the SC and scored as paired and synapsed, while in the lower case the two foci were well separated on the same stretch of SC and were considered to be unpaired. As shown in Table 1, among the 57 oocytes with two distinct GFP foci we saw 26 examples in which the two foci appeared as synapsed foci separated only by a stretch of SC. Among those 31 cases in which the two foci were not paired, 25 were nonetheless still associated with the same stretch of SC, and there were also six oocytes in which distant foci were not connected by SC. There were also 43 oocytes with just one GFP focus.


All paired up with no place to go: pairing, synapsis, and DSB formation in a balancer heterozygote.

Gong WJ, McKim KS, Hawley RS - PLoS Genet. (2005)

Synapsed and Unsynapsed lacO Sites in X/X (10A/11A) OocytesNote that in the lower (unsynapsed) case, the two GFP foci are displaced along the length of the same stretch of SC. In these images, which consist of one to two optical sections, two GFP foci (green) are associated with a segment of SC (red). Distances between those GFP foci are shown at the right-most in each row. Bars = 1 μm.
© Copyright Policy
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC1285065&req=5

pgen-0010067-g004: Synapsed and Unsynapsed lacO Sites in X/X (10A/11A) OocytesNote that in the lower (unsynapsed) case, the two GFP foci are displaced along the length of the same stretch of SC. In these images, which consist of one to two optical sections, two GFP foci (green) are associated with a segment of SC (red). Distances between those GFP foci are shown at the right-most in each row. Bars = 1 μm.
Mentions: The analysis presented above assumes that if two lacO arrays were frequently separated, even by small distances, we would still be able to visualize them as two separate dots. To estimate the effect of displacing two lacO arrays on the separation of GFP foci, we also assessed pairing and synapsis in X/X females carrying a lacO insertion at position 10A on one homolog and a lacO insertion at position 11A on the other. These two sites are separated by a physical distance of 0.9 Mb. Figure 4 presents examples of two nuclei in which the two foci were associated with a stretch of SC. In the upper case the two GFP foci were opposite from each other across the SC and scored as paired and synapsed, while in the lower case the two foci were well separated on the same stretch of SC and were considered to be unpaired. As shown in Table 1, among the 57 oocytes with two distinct GFP foci we saw 26 examples in which the two foci appeared as synapsed foci separated only by a stretch of SC. Among those 31 cases in which the two foci were not paired, 25 were nonetheless still associated with the same stretch of SC, and there were also six oocytes in which distant foci were not connected by SC. There were also 43 oocytes with just one GFP focus.

Bottom Line: 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.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.

View Article: PubMed Central - PubMed

Affiliation: Stowers Institute for Medical Research, Kansas City, Missouri, United States of America.

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.

Show MeSH
Related in: MedlinePlus