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Behavior of aberrant chromosome configurations in Drosophila melanogaster female meiosis I.

Gilliland WD, Colwell EM, Lane FM, Snouffer AA - G3 (Bethesda) (2014)

Bottom Line: We show that these genotypes complete congression normally, with their chromosomes bioriented at metaphase I arrest at the same rates that they segregate, indicating that orientation must be established during prometaphase I before congression.We also show that monovalent chromosomes can move out on the prometaphase I spindle, but the dot 4 chromosomes appear required for this movement.Finally, we show that, similar to achiasmate chromosomes, heterologous chromosomes can be connected by chromatin threads, suggesting a mechanism for how heterochromatic homology establishes these unusual biorientation patterns.

View Article: PubMed Central - PubMed

Affiliation: Department of Biological Sciences, DePaul University, Chicago, Illinois 60614-3207 wgillila@depaul.edu.

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Chromosomes without pairing partners. All spindles are oriented horizontally (scale bars = 5 µm) and are stained with DAPI (gray/blue). (A) Top panel shows prometaphase I in a C(1)RM, y v /Ø; svspa-pol oocyte, with the large C(1) out on the right spindle arm. Bottom panel shows metaphase I arrest in the same genotype, using 2L-3L (white), X (green), and 4 (red) probes, indicating the 4s are co-oriented with the C(1) oriented to the right pole. (B) Top panel shows prometaphase I in a C(2)EN, bw sp/Ø oocyte, with the large C(2) on the right arm of the spindle, between the normal 4 and the exchange X and 3. Bottom panel shows metaphase I arrest in the same genotype, using 2L-3L (white), 2L (green), and 3R (red) probes. Note the C(2) on the left is highlighted by both white and green probes, while small spots of 2L probe are found on the co-oriented 4s. (C) Top panel shows the only oocyte from 2-d mated y w f; C(4)RM, ci eyR/Ø females where the C(4) was found out on the spindle. The distance the C(4) has moved is quite small. Bottom panel shows metaphase I in the same genotype, with the same probes as in A, and the C(4) oriented left. Note the X also has a small spot of 4 probe. (D) The C(4) chromosome is competent to move out on the spindle, as can be seen in this C(4)/ svspa-pol oocyte. (E) In FM7/y w f; C(4)/Ø oocytes (labeled with same probes as (A), chromosome movements occur less often, but the C(4) can be found out on the spindle. Note both the normal X (left) and FM7 (right) chromosomes hybridize 4 probe near their centromeres, while the FM7 chromosome has most of the X probe moved distally by a large inversion, found in two spots near the center of the chromosome mass. (F) Top panel shows normal XC(4)<=>X coorientation in a y w f / y In(1)dl-49, v f; C(4)/Ø oocyte, while bottom panel shows heterologous XX<=>C(4) orientation.
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fig1: Chromosomes without pairing partners. All spindles are oriented horizontally (scale bars = 5 µm) and are stained with DAPI (gray/blue). (A) Top panel shows prometaphase I in a C(1)RM, y v /Ø; svspa-pol oocyte, with the large C(1) out on the right spindle arm. Bottom panel shows metaphase I arrest in the same genotype, using 2L-3L (white), X (green), and 4 (red) probes, indicating the 4s are co-oriented with the C(1) oriented to the right pole. (B) Top panel shows prometaphase I in a C(2)EN, bw sp/Ø oocyte, with the large C(2) on the right arm of the spindle, between the normal 4 and the exchange X and 3. Bottom panel shows metaphase I arrest in the same genotype, using 2L-3L (white), 2L (green), and 3R (red) probes. Note the C(2) on the left is highlighted by both white and green probes, while small spots of 2L probe are found on the co-oriented 4s. (C) Top panel shows the only oocyte from 2-d mated y w f; C(4)RM, ci eyR/Ø females where the C(4) was found out on the spindle. The distance the C(4) has moved is quite small. Bottom panel shows metaphase I in the same genotype, with the same probes as in A, and the C(4) oriented left. Note the X also has a small spot of 4 probe. (D) The C(4) chromosome is competent to move out on the spindle, as can be seen in this C(4)/ svspa-pol oocyte. (E) In FM7/y w f; C(4)/Ø oocytes (labeled with same probes as (A), chromosome movements occur less often, but the C(4) can be found out on the spindle. Note both the normal X (left) and FM7 (right) chromosomes hybridize 4 probe near their centromeres, while the FM7 chromosome has most of the X probe moved distally by a large inversion, found in two spots near the center of the chromosome mass. (F) Top panel shows normal XC(4)<=>X coorientation in a y w f / y In(1)dl-49, v f; C(4)/Ø oocyte, while bottom panel shows heterologous XX<=>C(4) orientation.

Mentions: We first examined females carrying monovalent compound chromosomes, which lack a homologous pairing partner entirely. In 2-d mated C(1)RM, y v/Ø; svspa-pol females, we found 56% of oocytes had chromosomes out on the prometaphase I spindle, with the unpaired C(1) chromosome out in 32% of oocytes (Table 1). The 4 chromosomes were found properly positioned on opposite sides of the spindle, and closer to the poles than the C(1) (Figure 1A, top). In aged virgins, we found 93% of oocytes with chromosomes in a single mass (Figure 1A, bottom). Of the exceptions, five were still in prometaphase with the 4s properly co-oriented (suggesting those oocytes had not yet completed congression), two had the major autosomes split into separate compact masses, and two were in a heterologous C(1)<=>44 configuration (2% HS). These cytological results are consistent with the rate of HS measured genetically in this stock (Table 1).


Behavior of aberrant chromosome configurations in Drosophila melanogaster female meiosis I.

Gilliland WD, Colwell EM, Lane FM, Snouffer AA - G3 (Bethesda) (2014)

Chromosomes without pairing partners. All spindles are oriented horizontally (scale bars = 5 µm) and are stained with DAPI (gray/blue). (A) Top panel shows prometaphase I in a C(1)RM, y v /Ø; svspa-pol oocyte, with the large C(1) out on the right spindle arm. Bottom panel shows metaphase I arrest in the same genotype, using 2L-3L (white), X (green), and 4 (red) probes, indicating the 4s are co-oriented with the C(1) oriented to the right pole. (B) Top panel shows prometaphase I in a C(2)EN, bw sp/Ø oocyte, with the large C(2) on the right arm of the spindle, between the normal 4 and the exchange X and 3. Bottom panel shows metaphase I arrest in the same genotype, using 2L-3L (white), 2L (green), and 3R (red) probes. Note the C(2) on the left is highlighted by both white and green probes, while small spots of 2L probe are found on the co-oriented 4s. (C) Top panel shows the only oocyte from 2-d mated y w f; C(4)RM, ci eyR/Ø females where the C(4) was found out on the spindle. The distance the C(4) has moved is quite small. Bottom panel shows metaphase I in the same genotype, with the same probes as in A, and the C(4) oriented left. Note the X also has a small spot of 4 probe. (D) The C(4) chromosome is competent to move out on the spindle, as can be seen in this C(4)/ svspa-pol oocyte. (E) In FM7/y w f; C(4)/Ø oocytes (labeled with same probes as (A), chromosome movements occur less often, but the C(4) can be found out on the spindle. Note both the normal X (left) and FM7 (right) chromosomes hybridize 4 probe near their centromeres, while the FM7 chromosome has most of the X probe moved distally by a large inversion, found in two spots near the center of the chromosome mass. (F) Top panel shows normal XC(4)<=>X coorientation in a y w f / y In(1)dl-49, v f; C(4)/Ø oocyte, while bottom panel shows heterologous XX<=>C(4) orientation.
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fig1: Chromosomes without pairing partners. All spindles are oriented horizontally (scale bars = 5 µm) and are stained with DAPI (gray/blue). (A) Top panel shows prometaphase I in a C(1)RM, y v /Ø; svspa-pol oocyte, with the large C(1) out on the right spindle arm. Bottom panel shows metaphase I arrest in the same genotype, using 2L-3L (white), X (green), and 4 (red) probes, indicating the 4s are co-oriented with the C(1) oriented to the right pole. (B) Top panel shows prometaphase I in a C(2)EN, bw sp/Ø oocyte, with the large C(2) on the right arm of the spindle, between the normal 4 and the exchange X and 3. Bottom panel shows metaphase I arrest in the same genotype, using 2L-3L (white), 2L (green), and 3R (red) probes. Note the C(2) on the left is highlighted by both white and green probes, while small spots of 2L probe are found on the co-oriented 4s. (C) Top panel shows the only oocyte from 2-d mated y w f; C(4)RM, ci eyR/Ø females where the C(4) was found out on the spindle. The distance the C(4) has moved is quite small. Bottom panel shows metaphase I in the same genotype, with the same probes as in A, and the C(4) oriented left. Note the X also has a small spot of 4 probe. (D) The C(4) chromosome is competent to move out on the spindle, as can be seen in this C(4)/ svspa-pol oocyte. (E) In FM7/y w f; C(4)/Ø oocytes (labeled with same probes as (A), chromosome movements occur less often, but the C(4) can be found out on the spindle. Note both the normal X (left) and FM7 (right) chromosomes hybridize 4 probe near their centromeres, while the FM7 chromosome has most of the X probe moved distally by a large inversion, found in two spots near the center of the chromosome mass. (F) Top panel shows normal XC(4)<=>X coorientation in a y w f / y In(1)dl-49, v f; C(4)/Ø oocyte, while bottom panel shows heterologous XX<=>C(4) orientation.
Mentions: We first examined females carrying monovalent compound chromosomes, which lack a homologous pairing partner entirely. In 2-d mated C(1)RM, y v/Ø; svspa-pol females, we found 56% of oocytes had chromosomes out on the prometaphase I spindle, with the unpaired C(1) chromosome out in 32% of oocytes (Table 1). The 4 chromosomes were found properly positioned on opposite sides of the spindle, and closer to the poles than the C(1) (Figure 1A, top). In aged virgins, we found 93% of oocytes with chromosomes in a single mass (Figure 1A, bottom). Of the exceptions, five were still in prometaphase with the 4s properly co-oriented (suggesting those oocytes had not yet completed congression), two had the major autosomes split into separate compact masses, and two were in a heterologous C(1)<=>44 configuration (2% HS). These cytological results are consistent with the rate of HS measured genetically in this stock (Table 1).

Bottom Line: We show that these genotypes complete congression normally, with their chromosomes bioriented at metaphase I arrest at the same rates that they segregate, indicating that orientation must be established during prometaphase I before congression.We also show that monovalent chromosomes can move out on the prometaphase I spindle, but the dot 4 chromosomes appear required for this movement.Finally, we show that, similar to achiasmate chromosomes, heterologous chromosomes can be connected by chromatin threads, suggesting a mechanism for how heterochromatic homology establishes these unusual biorientation patterns.

View Article: PubMed Central - PubMed

Affiliation: Department of Biological Sciences, DePaul University, Chicago, Illinois 60614-3207 wgillila@depaul.edu.

Show MeSH
Related in: MedlinePlus