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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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Suppression of the tid1Δ sister chromatid separation defect by mcd1-1 rec8Δ in the spo11Δ spo13Δ background. (A) Percentage of cells with two separated chromatin masses (binucleates) after a shift to nonpermissive temperature at 2-h intervals. Cells were allowed to sporulate for at least 24 h after a shift to nonpermissive temperature before scoring. Fig. S3 (D–F; available at http://www.jcb.org/cgi/content/full/jcb.200505020/DC1) show the kinetics of the short spindle, dumbbell, and binucleate stages at 21°C during this experiment. (B and C) Percentage of binucleates (B) and dumbbells (C) after a shift from 21 to 33°C at 10 h. (D) Percentage of cells with short spindles after a shift from 21 to 33°C at 10 h. Progression of cells through the division is monitored by the behavior of the spindle (TUB1-GFP) and DAPI-stained chromatin. At least 200 cells were scored for each time point.
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fig6: Suppression of the tid1Δ sister chromatid separation defect by mcd1-1 rec8Δ in the spo11Δ spo13Δ background. (A) Percentage of cells with two separated chromatin masses (binucleates) after a shift to nonpermissive temperature at 2-h intervals. Cells were allowed to sporulate for at least 24 h after a shift to nonpermissive temperature before scoring. Fig. S3 (D–F; available at http://www.jcb.org/cgi/content/full/jcb.200505020/DC1) show the kinetics of the short spindle, dumbbell, and binucleate stages at 21°C during this experiment. (B and C) Percentage of binucleates (B) and dumbbells (C) after a shift from 21 to 33°C at 10 h. (D) Percentage of cells with short spindles after a shift from 21 to 33°C at 10 h. Progression of cells through the division is monitored by the behavior of the spindle (TUB1-GFP) and DAPI-stained chromatin. At least 200 cells were scored for each time point.

Mentions: Our data demonstrate that in the spo11Δ spo13Δ background, Mcd1p inactivation efficiently suppresses the tid1Δ anaphase block but only at early times in sporulation. This suggests that some other protein mediates persistent sister chromatid connections later in meiosis in the absence of Mcd1p. To determine whether the Mcd1p-independent sister connections are mediated by Rec8p, the effect of rec8Δ on the anaphase block of tid1Δ was studied in spo11Δ spo13Δ mcd1-1. Progression of cells through the divisions was monitored by using TUB1-GFP and DAPI-stained chromatin. Sporulating cells were shifted from permissive to nonpermissive temperature every 2 h, and binucleates were scored after 24 h of sporulation. The anaphase block of tid1Δ is suppressed by mcd1-1 rec8Δ at early times as well as at late times at 33°C (Fig. 6 A) despite the fact that cells with tid1Δ reach full anaphase block by 8–10 h of sporulation at 21°C (Fig. S3, D–F). A slight decrease in the level of suppression after 10 h coincides with the onset of chromatin fragmentation in a fraction of cells (not depicted). To confirm that persistent sister chromatid connections is the main reason for the anaphase block, spo11Δ spo13Δ mcd1-1 rec8Δ tid1Δ cells were allowed to block at anaphase (10 h of sporulation at 21°C) and were transferred to 33°C (Fig. 6, B–D). After a shift to 33°C, the turnover of anaphase-blocked cells (dumbbells and cells with a short spindle) in spo11Δ spo13Δ mcd1-1 rec8Δ tid1Δ occurs within 1 h, coinciding with an increase in binucleates. This quick and complete rescue indicates that both Mcd1p and Rec8p are required to maintain the sister chromatid connections that persist in spo11Δ spo13Δ tid1Δ.


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)

Suppression of the tid1Δ sister chromatid separation defect by mcd1-1 rec8Δ in the spo11Δ spo13Δ background. (A) Percentage of cells with two separated chromatin masses (binucleates) after a shift to nonpermissive temperature at 2-h intervals. Cells were allowed to sporulate for at least 24 h after a shift to nonpermissive temperature before scoring. Fig. S3 (D–F; available at http://www.jcb.org/cgi/content/full/jcb.200505020/DC1) show the kinetics of the short spindle, dumbbell, and binucleate stages at 21°C during this experiment. (B and C) Percentage of binucleates (B) and dumbbells (C) after a shift from 21 to 33°C at 10 h. (D) Percentage of cells with short spindles after a shift from 21 to 33°C at 10 h. Progression of cells through the division is monitored by the behavior of the spindle (TUB1-GFP) and DAPI-stained chromatin. At least 200 cells were scored for each time point.
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Related In: Results  -  Collection

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

fig6: Suppression of the tid1Δ sister chromatid separation defect by mcd1-1 rec8Δ in the spo11Δ spo13Δ background. (A) Percentage of cells with two separated chromatin masses (binucleates) after a shift to nonpermissive temperature at 2-h intervals. Cells were allowed to sporulate for at least 24 h after a shift to nonpermissive temperature before scoring. Fig. S3 (D–F; available at http://www.jcb.org/cgi/content/full/jcb.200505020/DC1) show the kinetics of the short spindle, dumbbell, and binucleate stages at 21°C during this experiment. (B and C) Percentage of binucleates (B) and dumbbells (C) after a shift from 21 to 33°C at 10 h. (D) Percentage of cells with short spindles after a shift from 21 to 33°C at 10 h. Progression of cells through the division is monitored by the behavior of the spindle (TUB1-GFP) and DAPI-stained chromatin. At least 200 cells were scored for each time point.
Mentions: Our data demonstrate that in the spo11Δ spo13Δ background, Mcd1p inactivation efficiently suppresses the tid1Δ anaphase block but only at early times in sporulation. This suggests that some other protein mediates persistent sister chromatid connections later in meiosis in the absence of Mcd1p. To determine whether the Mcd1p-independent sister connections are mediated by Rec8p, the effect of rec8Δ on the anaphase block of tid1Δ was studied in spo11Δ spo13Δ mcd1-1. Progression of cells through the divisions was monitored by using TUB1-GFP and DAPI-stained chromatin. Sporulating cells were shifted from permissive to nonpermissive temperature every 2 h, and binucleates were scored after 24 h of sporulation. The anaphase block of tid1Δ is suppressed by mcd1-1 rec8Δ at early times as well as at late times at 33°C (Fig. 6 A) despite the fact that cells with tid1Δ reach full anaphase block by 8–10 h of sporulation at 21°C (Fig. S3, D–F). A slight decrease in the level of suppression after 10 h coincides with the onset of chromatin fragmentation in a fraction of cells (not depicted). To confirm that persistent sister chromatid connections is the main reason for the anaphase block, spo11Δ spo13Δ mcd1-1 rec8Δ tid1Δ cells were allowed to block at anaphase (10 h of sporulation at 21°C) and were transferred to 33°C (Fig. 6, B–D). After a shift to 33°C, the turnover of anaphase-blocked cells (dumbbells and cells with a short spindle) in spo11Δ spo13Δ mcd1-1 rec8Δ tid1Δ occurs within 1 h, coinciding with an increase in binucleates. This quick and complete rescue indicates that both Mcd1p and Rec8p are required to maintain the sister chromatid connections that persist in spo11Δ spo13Δ tid1Δ.

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