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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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Prophase arrest and anaphase block caused by tid1Δ. (A) Kinetics of entry into the first meiotic division of wild-type and tid1Δ. Progression through the divisions is monitored by the behavior of the spindle (TUB1-GFP) and DAPI-stained chromatin. Cells at or past metaphase I are represented by cells with a single mass of chromatin with a spindle, by dumbbells, and by cells that have separated their chromatin into two (binucleates) or four masses (tetranucleates). wild-type, squares; tid1Δ, triangles. At least 200 cells were counted at each time point. (B) Three-dimensional images of chromatin (red, DAPI) and spindles (green, antibodies against tubulin) of dividing cells in wild-type (binucleate and tetranucleate) and tid1Δ (anaphase I and II dumbbells), displayed by isointensity surface extraction (and some rotation with respect to insets). The insets are gray-scale maximum intensity projections of the separate chromatin (right insets) and spindle signals (left insets) in the same cells. Bars, 4 μm.
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fig1: Prophase arrest and anaphase block caused by tid1Δ. (A) Kinetics of entry into the first meiotic division of wild-type and tid1Δ. Progression through the divisions is monitored by the behavior of the spindle (TUB1-GFP) and DAPI-stained chromatin. Cells at or past metaphase I are represented by cells with a single mass of chromatin with a spindle, by dumbbells, and by cells that have separated their chromatin into two (binucleates) or four masses (tetranucleates). wild-type, squares; tid1Δ, triangles. At least 200 cells were counted at each time point. (B) Three-dimensional images of chromatin (red, DAPI) and spindles (green, antibodies against tubulin) of dividing cells in wild-type (binucleate and tetranucleate) and tid1Δ (anaphase I and II dumbbells), displayed by isointensity surface extraction (and some rotation with respect to insets). The insets are gray-scale maximum intensity projections of the separate chromatin (right insets) and spindle signals (left insets) in the same cells. Bars, 4 μm.

Mentions: To determine the kinetics of progression through meiotic divisions, we used a strain with a single TUB1-GFP allele to visualize the spindles. Cells were stained with DAPI to visualize DNA. The majority of tid1Δ cells are blocked as mononucleate cells with no spindle (Fig. 1 A) and remain blocked even 26 h after the shift into sporulation. At the same time, tid1Δ does not affect the kinetics of formation and the appearance of the synaptonemal complex (SC), suggesting that Tid1p is not required for synapsis. The accumulation of cells with fully formed SC in tid1Δ indicates that the deletion of TID1 blocks cells in pachytene (Fig. S1, A and B, available at http://www.jcb.org/cgi/content/full/jcb.200505020/DC1). tid1Δ cells that were blocked in pachytene could be arrested by the pachytene checkpoint, which is triggered by unrepaired DSBs. Turnover of DSBs and formation of mature recombination products are delayed in tid1Δ (Fig. S1, C–F), confirming that pachytene arrest in tid1Δ is associated with the defective processing of DSBs.


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)

Prophase arrest and anaphase block caused by tid1Δ. (A) Kinetics of entry into the first meiotic division of wild-type and tid1Δ. Progression through the divisions is monitored by the behavior of the spindle (TUB1-GFP) and DAPI-stained chromatin. Cells at or past metaphase I are represented by cells with a single mass of chromatin with a spindle, by dumbbells, and by cells that have separated their chromatin into two (binucleates) or four masses (tetranucleates). wild-type, squares; tid1Δ, triangles. At least 200 cells were counted at each time point. (B) Three-dimensional images of chromatin (red, DAPI) and spindles (green, antibodies against tubulin) of dividing cells in wild-type (binucleate and tetranucleate) and tid1Δ (anaphase I and II dumbbells), displayed by isointensity surface extraction (and some rotation with respect to insets). The insets are gray-scale maximum intensity projections of the separate chromatin (right insets) and spindle signals (left insets) in the same cells. Bars, 4 μm.
© Copyright Policy
Related In: Results  -  Collection

Show All Figures
getmorefigures.php?uid=PMC2171180&req=5

fig1: Prophase arrest and anaphase block caused by tid1Δ. (A) Kinetics of entry into the first meiotic division of wild-type and tid1Δ. Progression through the divisions is monitored by the behavior of the spindle (TUB1-GFP) and DAPI-stained chromatin. Cells at or past metaphase I are represented by cells with a single mass of chromatin with a spindle, by dumbbells, and by cells that have separated their chromatin into two (binucleates) or four masses (tetranucleates). wild-type, squares; tid1Δ, triangles. At least 200 cells were counted at each time point. (B) Three-dimensional images of chromatin (red, DAPI) and spindles (green, antibodies against tubulin) of dividing cells in wild-type (binucleate and tetranucleate) and tid1Δ (anaphase I and II dumbbells), displayed by isointensity surface extraction (and some rotation with respect to insets). The insets are gray-scale maximum intensity projections of the separate chromatin (right insets) and spindle signals (left insets) in the same cells. Bars, 4 μm.
Mentions: To determine the kinetics of progression through meiotic divisions, we used a strain with a single TUB1-GFP allele to visualize the spindles. Cells were stained with DAPI to visualize DNA. The majority of tid1Δ cells are blocked as mononucleate cells with no spindle (Fig. 1 A) and remain blocked even 26 h after the shift into sporulation. At the same time, tid1Δ does not affect the kinetics of formation and the appearance of the synaptonemal complex (SC), suggesting that Tid1p is not required for synapsis. The accumulation of cells with fully formed SC in tid1Δ indicates that the deletion of TID1 blocks cells in pachytene (Fig. S1, A and B, available at http://www.jcb.org/cgi/content/full/jcb.200505020/DC1). tid1Δ cells that were blocked in pachytene could be arrested by the pachytene checkpoint, which is triggered by unrepaired DSBs. Turnover of DSBs and formation of mature recombination products are delayed in tid1Δ (Fig. S1, C–F), confirming that pachytene arrest in tid1Δ is associated with the defective processing of DSBs.

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