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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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Synapsed lacO Foci Flanking Stretches of SC in FM7/X or X/X OocytesIn both X/X and FM7/X oocytes, paired lacO foci flank regions of SC. The positions of paired/synapsed lacO sites studied in X/X and FM7/X oocytes in zygotene/pachytene are shown at the left-most of each row. One to three optical sections show two partially overlapping or adjacent GFP foci (green) associated with a segment of SC (red). Distances between those GFP foci are shown at the right-most in each row. Due to the difficulty of accurately measuring the distance between overlapping foci, “<0.25” is used. Bars = 1 μm.
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pgen-0010067-g002: Synapsed lacO Foci Flanking Stretches of SC in FM7/X or X/X OocytesIn both X/X and FM7/X oocytes, paired lacO foci flank regions of SC. The positions of paired/synapsed lacO sites studied in X/X and FM7/X oocytes in zygotene/pachytene are shown at the left-most of each row. One to three optical sections show two partially overlapping or adjacent GFP foci (green) associated with a segment of SC (red). Distances between those GFP foci are shown at the right-most in each row. Due to the difficulty of accurately measuring the distance between overlapping foci, “<0.25” is used. Bars = 1 μm.

Mentions: Our initial analysis of chromosome pairing and synapsis in Drosophila oocytes focused on the study of four allelic pairs of lacO arrays located at 1C, 9B, 11A, and 18C on a pair of normal sequence X chromosomes (Table 1 and Figures 2 and 3). In SC-positive oocytes the two lacO sites are considered as paired and synapsed if any of the following three criteria are met: 1) there is only one visible green fluorescent protein (GFP) focus associated with a stretch of SC; 2) there are two clearly overlapping GFP foci associated with a stretch of SC (see the penultimate row in Figure 2); or 3) there are two distinct GFP foci that lie on opposite sides of a stretch of SC (see Figure 2). Using this method, the observed frequencies of failed synapsis for the four allelic pairs of lacO insertions studied in X/X oocytes ranged from 1.7% for the lacO insertion at 9B, to values ranging from 4.2%–4.6% for the lacO insertions at 1C, 11A, and 18C.


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 lacO Foci Flanking Stretches of SC in FM7/X or X/X OocytesIn both X/X and FM7/X oocytes, paired lacO foci flank regions of SC. The positions of paired/synapsed lacO sites studied in X/X and FM7/X oocytes in zygotene/pachytene are shown at the left-most of each row. One to three optical sections show two partially overlapping or adjacent GFP foci (green) associated with a segment of SC (red). Distances between those GFP foci are shown at the right-most in each row. Due to the difficulty of accurately measuring the distance between overlapping foci, “<0.25” is used. Bars = 1 μm.
© Copyright Policy
Related In: Results  -  Collection

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

pgen-0010067-g002: Synapsed lacO Foci Flanking Stretches of SC in FM7/X or X/X OocytesIn both X/X and FM7/X oocytes, paired lacO foci flank regions of SC. The positions of paired/synapsed lacO sites studied in X/X and FM7/X oocytes in zygotene/pachytene are shown at the left-most of each row. One to three optical sections show two partially overlapping or adjacent GFP foci (green) associated with a segment of SC (red). Distances between those GFP foci are shown at the right-most in each row. Due to the difficulty of accurately measuring the distance between overlapping foci, “<0.25” is used. Bars = 1 μm.
Mentions: Our initial analysis of chromosome pairing and synapsis in Drosophila oocytes focused on the study of four allelic pairs of lacO arrays located at 1C, 9B, 11A, and 18C on a pair of normal sequence X chromosomes (Table 1 and Figures 2 and 3). In SC-positive oocytes the two lacO sites are considered as paired and synapsed if any of the following three criteria are met: 1) there is only one visible green fluorescent protein (GFP) focus associated with a stretch of SC; 2) there are two clearly overlapping GFP foci associated with a stretch of SC (see the penultimate row in Figure 2); or 3) there are two distinct GFP foci that lie on opposite sides of a stretch of SC (see Figure 2). Using this method, the observed frequencies of failed synapsis for the four allelic pairs of lacO insertions studied in X/X oocytes ranged from 1.7% for the lacO insertion at 9B, to values ranging from 4.2%–4.6% for the lacO insertions at 1C, 11A, and 18C.

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