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Recombination protein Tid1p controls resolution of cohesin-dependent linkages in meiosis in Saccharomyces cerevisiae.

Kateneva AV, Konovchenko AA, Guacci V, Dresser ME - J. Cell Biol. (2005)

Bottom Line: Genetic results indicate that the primary defect in these cells is a failure to resolve Mcd1p-mediated connections.Tid1p interacts with recombination enzymes Dmc1p and Rad51p and has an established role in recombination repair.We propose that Tid1p remodels Mcd1p-mediated cohesion early in meiotic prophase to facilitate interhomologue recombination and the subsequent segregation of homologous chromosomes.

View Article: PubMed Central - PubMed

Affiliation: Program in Molecular, Cell, and Developmental Biology, Oklahoma Medical Research Foundation, Oklahoma City, OK 73104.

ABSTRACT
Sister chromatid cohesion and interhomologue recombination are coordinated to promote the segregation of homologous chromosomes instead of sister chromatids at the first meiotic division. During meiotic prophase in Saccharomyces cerevisiae, the meiosis-specific cohesin Rec8p localizes along chromosome axes and mediates most of the cohesion. The mitotic cohesin Mcd1p/Scc1p localizes to discrete spots along chromosome arms, and its function is not clear. In cells lacking Tid1p, which is a member of the SWI2/SNF2 family of helicase-like proteins that are involved in chromatin remodeling, Mcd1p and Rec8p persist abnormally through both meiotic divisions, and chromosome segregation fails in the majority of cells. Genetic results indicate that the primary defect in these cells is a failure to resolve Mcd1p-mediated connections. Tid1p interacts with recombination enzymes Dmc1p and Rad51p and has an established role in recombination repair. We propose that Tid1p remodels Mcd1p-mediated cohesion early in meiotic prophase to facilitate interhomologue recombination and the subsequent segregation of homologous chromosomes.

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Delayed dissociation of Mcd1p and Rec8p from chromatin in tid1Δ. Spread preparations of sporulating cells were immunostained with antibodies against tubulin (red) and GFP (Rec8p-GFP, green) or Mcd1p (green). Chromatin is visualized with DAPI (blue). (A) Chromatin-associated Rec8p in wild-type and tid1Δ cells in the first (MI) and second (MII) division. (B and D) Quantification of Rec8p- (B) and Mcd1p-positive (D) cells in the first (1 spindle or 2SPB) and second (2 spindles) division. The differences in the numbers of cells that have Rec8p (B) and Mcd1p (D) associated with chromatin in wild-type and tid1Δ are statistically significant (P < 0.05; X2 test) both for the cells with two spindles and for the cells with one spindle or two SPB. 1 spindle or 2 SPB, cells with long spindle or two SPBs on opposite sides of chromatin mass. Numbers above the bars represent Rec8p- or Mcd1p-positive cells/total number of cells counted in a given class. (C) Chromatin-associated Mcd1p in wild-type and tid1Δ cells in the first (MI) and second (MII) division. Bars, 4 μm.
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fig7: Delayed dissociation of Mcd1p and Rec8p from chromatin in tid1Δ. Spread preparations of sporulating cells were immunostained with antibodies against tubulin (red) and GFP (Rec8p-GFP, green) or Mcd1p (green). Chromatin is visualized with DAPI (blue). (A) Chromatin-associated Rec8p in wild-type and tid1Δ cells in the first (MI) and second (MII) division. (B and D) Quantification of Rec8p- (B) and Mcd1p-positive (D) cells in the first (1 spindle or 2SPB) and second (2 spindles) division. The differences in the numbers of cells that have Rec8p (B) and Mcd1p (D) associated with chromatin in wild-type and tid1Δ are statistically significant (P < 0.05; X2 test) both for the cells with two spindles and for the cells with one spindle or two SPB. 1 spindle or 2 SPB, cells with long spindle or two SPBs on opposite sides of chromatin mass. Numbers above the bars represent Rec8p- or Mcd1p-positive cells/total number of cells counted in a given class. (C) Chromatin-associated Mcd1p in wild-type and tid1Δ cells in the first (MI) and second (MII) division. Bars, 4 μm.

Mentions: Failure to segregate chromosomes in both divisions in tid1Δ is likely caused by Mcd1p- and Rec8p-dependent connections that persist in anaphase I and II. To confirm this possibility, the association of Mcd1p and Rec8p with chromatin was tested in both anaphase I and II in spread preparations of meiotic nuclei. Spindle behavior was used as an internal marker for progression through the meiotic divisions in order to compare cohesin dissociation from chromatin in tid1Δ with wild-type. Rec8p and Mcd1p were visualized by immunolabeling in spread nuclei of sporulating tid1Δ and wild-type cells. Although none of the wild-type cells have Rec8p that is associated with chromatin in anaphase II, Rec8p signal remains in 24% of tid1Δ cells that have two fully elongated spindles. Thus, the dissociation of Rec8p from chromatin is delayed in tid1Δ (Fig. 7, A and B). Aside from this delay, there were no obvious differences in the appearance of Rec8p in wild-type and tid1Δ cells (not depicted), which is consistent with the normal appearance of SCs in tid1Δ (Fig. S1 A).


Recombination protein Tid1p controls resolution of cohesin-dependent linkages in meiosis in Saccharomyces cerevisiae.

Kateneva AV, Konovchenko AA, Guacci V, Dresser ME - J. Cell Biol. (2005)

Delayed dissociation of Mcd1p and Rec8p from chromatin in tid1Δ. Spread preparations of sporulating cells were immunostained with antibodies against tubulin (red) and GFP (Rec8p-GFP, green) or Mcd1p (green). Chromatin is visualized with DAPI (blue). (A) Chromatin-associated Rec8p in wild-type and tid1Δ cells in the first (MI) and second (MII) division. (B and D) Quantification of Rec8p- (B) and Mcd1p-positive (D) cells in the first (1 spindle or 2SPB) and second (2 spindles) division. The differences in the numbers of cells that have Rec8p (B) and Mcd1p (D) associated with chromatin in wild-type and tid1Δ are statistically significant (P < 0.05; X2 test) both for the cells with two spindles and for the cells with one spindle or two SPB. 1 spindle or 2 SPB, cells with long spindle or two SPBs on opposite sides of chromatin mass. Numbers above the bars represent Rec8p- or Mcd1p-positive cells/total number of cells counted in a given class. (C) Chromatin-associated Mcd1p in wild-type and tid1Δ cells in the first (MI) and second (MII) division. Bars, 4 μm.
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fig7: Delayed dissociation of Mcd1p and Rec8p from chromatin in tid1Δ. Spread preparations of sporulating cells were immunostained with antibodies against tubulin (red) and GFP (Rec8p-GFP, green) or Mcd1p (green). Chromatin is visualized with DAPI (blue). (A) Chromatin-associated Rec8p in wild-type and tid1Δ cells in the first (MI) and second (MII) division. (B and D) Quantification of Rec8p- (B) and Mcd1p-positive (D) cells in the first (1 spindle or 2SPB) and second (2 spindles) division. The differences in the numbers of cells that have Rec8p (B) and Mcd1p (D) associated with chromatin in wild-type and tid1Δ are statistically significant (P < 0.05; X2 test) both for the cells with two spindles and for the cells with one spindle or two SPB. 1 spindle or 2 SPB, cells with long spindle or two SPBs on opposite sides of chromatin mass. Numbers above the bars represent Rec8p- or Mcd1p-positive cells/total number of cells counted in a given class. (C) Chromatin-associated Mcd1p in wild-type and tid1Δ cells in the first (MI) and second (MII) division. Bars, 4 μm.
Mentions: Failure to segregate chromosomes in both divisions in tid1Δ is likely caused by Mcd1p- and Rec8p-dependent connections that persist in anaphase I and II. To confirm this possibility, the association of Mcd1p and Rec8p with chromatin was tested in both anaphase I and II in spread preparations of meiotic nuclei. Spindle behavior was used as an internal marker for progression through the meiotic divisions in order to compare cohesin dissociation from chromatin in tid1Δ with wild-type. Rec8p and Mcd1p were visualized by immunolabeling in spread nuclei of sporulating tid1Δ and wild-type cells. Although none of the wild-type cells have Rec8p that is associated with chromatin in anaphase II, Rec8p signal remains in 24% of tid1Δ cells that have two fully elongated spindles. Thus, the dissociation of Rec8p from chromatin is delayed in tid1Δ (Fig. 7, A and B). Aside from this delay, there were no obvious differences in the appearance of Rec8p in wild-type and tid1Δ cells (not depicted), which is consistent with the normal appearance of SCs in tid1Δ (Fig. S1 A).

Bottom Line: Genetic results indicate that the primary defect in these cells is a failure to resolve Mcd1p-mediated connections.Tid1p interacts with recombination enzymes Dmc1p and Rad51p and has an established role in recombination repair.We propose that Tid1p remodels Mcd1p-mediated cohesion early in meiotic prophase to facilitate interhomologue recombination and the subsequent segregation of homologous chromosomes.

View Article: PubMed Central - PubMed

Affiliation: Program in Molecular, Cell, and Developmental Biology, Oklahoma Medical Research Foundation, Oklahoma City, OK 73104.

ABSTRACT
Sister chromatid cohesion and interhomologue recombination are coordinated to promote the segregation of homologous chromosomes instead of sister chromatids at the first meiotic division. During meiotic prophase in Saccharomyces cerevisiae, the meiosis-specific cohesin Rec8p localizes along chromosome axes and mediates most of the cohesion. The mitotic cohesin Mcd1p/Scc1p localizes to discrete spots along chromosome arms, and its function is not clear. In cells lacking Tid1p, which is a member of the SWI2/SNF2 family of helicase-like proteins that are involved in chromatin remodeling, Mcd1p and Rec8p persist abnormally through both meiotic divisions, and chromosome segregation fails in the majority of cells. Genetic results indicate that the primary defect in these cells is a failure to resolve Mcd1p-mediated connections. Tid1p interacts with recombination enzymes Dmc1p and Rad51p and has an established role in recombination repair. We propose that Tid1p remodels Mcd1p-mediated cohesion early in meiotic prophase to facilitate interhomologue recombination and the subsequent segregation of homologous chromosomes.

Show MeSH
Related in: MedlinePlus