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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

Distributions of Distances between GFP Foci in Both X/X and FM7/X OocytesThese data report, in histogram form, the distribution of distances between GFP foci in those oocytes with two distinct GFP foci (including those oocytes with overlapping foci). For those oocytes with overlapping foci, the distance is measured as < 0.25 μm.(A) The distribution of distances in oocytes containing two lacO insertions at allelic sites in X/X females (upper panel) and nearby lacO couplets in FM7/X oocytes (lower panel).(B) The distribution of distances for non-allelic lacO insertion sites in X/X and FM7/X females. The distribution for an allelic pair of lacO insertions at 11A is provided as a control.(C) The distribution of distances in oocytes containing two lacO insertions at an allelic site (11A) in X/X; c(3)G females (left) and a nearby lacO couplet (18A/18C) in FM7/X ; c(3)G oocytes (right panel).
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pgen-0010067-g003: Distributions of Distances between GFP Foci in Both X/X and FM7/X OocytesThese data report, in histogram form, the distribution of distances between GFP foci in those oocytes with two distinct GFP foci (including those oocytes with overlapping foci). For those oocytes with overlapping foci, the distance is measured as < 0.25 μm.(A) The distribution of distances in oocytes containing two lacO insertions at allelic sites in X/X females (upper panel) and nearby lacO couplets in FM7/X oocytes (lower panel).(B) The distribution of distances for non-allelic lacO insertion sites in X/X and FM7/X females. The distribution for an allelic pair of lacO insertions at 11A is provided as a control.(C) The distribution of distances in oocytes containing two lacO insertions at an allelic site (11A) in X/X; c(3)G females (left) and a nearby lacO couplet (18A/18C) in FM7/X ; c(3)G oocytes (right panel).

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)

Distributions of Distances between GFP Foci in Both X/X and FM7/X OocytesThese data report, in histogram form, the distribution of distances between GFP foci in those oocytes with two distinct GFP foci (including those oocytes with overlapping foci). For those oocytes with overlapping foci, the distance is measured as < 0.25 μm.(A) The distribution of distances in oocytes containing two lacO insertions at allelic sites in X/X females (upper panel) and nearby lacO couplets in FM7/X oocytes (lower panel).(B) The distribution of distances for non-allelic lacO insertion sites in X/X and FM7/X females. The distribution for an allelic pair of lacO insertions at 11A is provided as a control.(C) The distribution of distances in oocytes containing two lacO insertions at an allelic site (11A) in X/X; c(3)G females (left) and a nearby lacO couplet (18A/18C) in FM7/X ; c(3)G oocytes (right panel).
© Copyright Policy
Related In: Results  -  Collection

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

pgen-0010067-g003: Distributions of Distances between GFP Foci in Both X/X and FM7/X OocytesThese data report, in histogram form, the distribution of distances between GFP foci in those oocytes with two distinct GFP foci (including those oocytes with overlapping foci). For those oocytes with overlapping foci, the distance is measured as < 0.25 μm.(A) The distribution of distances in oocytes containing two lacO insertions at allelic sites in X/X females (upper panel) and nearby lacO couplets in FM7/X oocytes (lower panel).(B) The distribution of distances for non-allelic lacO insertion sites in X/X and FM7/X females. The distribution for an allelic pair of lacO insertions at 11A is provided as a control.(C) The distribution of distances in oocytes containing two lacO insertions at an allelic site (11A) in X/X; c(3)G females (left) and a nearby lacO couplet (18A/18C) in FM7/X ; c(3)G oocytes (right panel).
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