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Csm4, in collaboration with Ndj1, mediates telomere-led chromosome dynamics and recombination during yeast meiosis.

Wanat JJ, Kim KP, Koszul R, Zanders S, Weiner B, Kleckner N, Alani E - PLoS Genet. (2008)

Bottom Line: In budding yeast, meiotic chromosomes exhibit dynamic movements, led by nuclear envelope (NE)-associated telomeres, throughout the zygotene and pachytene stages.Zygotene motion underlies the global tendency for colocalization of NE-associated chromosome ends in a "bouquet." In this study, we identify Csm4 as a new molecular participant in these processes and show that, unlike the two previously identified components, Ndj1 and Mps3, Csm4 is not required for meiosis-specific telomere/NE association.The recombination effects are discussed in the context of a model where the underlying defect is chromosome movement, the absence of which results in persistence of inappropriate chromosome relationships that, in turn, results in the observed mutant phenotypes.

View Article: PubMed Central - PubMed

Affiliation: Department of Molecular Biology and Genetics, Cornell University, Ithaca, New York, USA.

ABSTRACT
Chromosome movements are a general feature of mid-prophase of meiosis. In budding yeast, meiotic chromosomes exhibit dynamic movements, led by nuclear envelope (NE)-associated telomeres, throughout the zygotene and pachytene stages. Zygotene motion underlies the global tendency for colocalization of NE-associated chromosome ends in a "bouquet." In this study, we identify Csm4 as a new molecular participant in these processes and show that, unlike the two previously identified components, Ndj1 and Mps3, Csm4 is not required for meiosis-specific telomere/NE association. Instead, it acts to couple telomere/NE ensembles to a force generation mechanism. Mutants lacking Csm4 and/or Ndj1 display the following closely related phenotypes: (i) elevated crossover (CO) frequencies and decreased CO interference without abrogation of normal pathways; (ii) delayed progression of recombination, and recombination-coupled chromosome morphogenesis, with resulting delays in the MI division; and (iii) nondisjunction of homologs at the MI division for some reason other than absence of (the obligatory) CO(s). The recombination effects are discussed in the context of a model where the underlying defect is chromosome movement, the absence of which results in persistence of inappropriate chromosome relationships that, in turn, results in the observed mutant phenotypes.

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Cumulative genetic distance (cM) in WT, csm4Δ, mlh1Δ, msh5Δ, and ndj1Δ strains.In panels A and B, each bar is divided in sectors corresponding to genetic intervals in the region of the chromosome analyzed. A) Cumulative genetic distances between URA3 and HIS3 on chromosome XV in EAY1108/EAY1112 derived strains measured from tetrads (T) and single spores (S). B) Cumulative genetic distances between ADE2 and LEU2 on chromosome III, URA3 and CUP1 on chromosome VIII, and LYS5 and TRP5 on chromosome VII in the NH942/NH943 derived strains measured from tetrads (T) and single spores (S). See Tables 1 and S2 for raw data.
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pgen-1000188-g003: Cumulative genetic distance (cM) in WT, csm4Δ, mlh1Δ, msh5Δ, and ndj1Δ strains.In panels A and B, each bar is divided in sectors corresponding to genetic intervals in the region of the chromosome analyzed. A) Cumulative genetic distances between URA3 and HIS3 on chromosome XV in EAY1108/EAY1112 derived strains measured from tetrads (T) and single spores (S). B) Cumulative genetic distances between ADE2 and LEU2 on chromosome III, URA3 and CUP1 on chromosome VIII, and LYS5 and TRP5 on chromosome VII in the NH942/NH943 derived strains measured from tetrads (T) and single spores (S). See Tables 1 and S2 for raw data.

Mentions: We examined crossing over in 12 different intervals by tetrad analysis in WT and csm4Δ (Figure 3, Tables 1, S1, and S2). The csm4Δ mutation conferred a 30–40% increase in the level of COs for all four intervals in the SK1 congenic strains. In the analysis of complete tetrads, the URA3-LEU2 and ADE2-HIS3 intervals were significantly different from WT (G-test, p<0.007, 95% confidence level, Dunn-Sidak correction, [34],[35]) but the LEU2-LYS2 (p = 0.07) and the LYS2-ADE2 (p = 0.013) were not (Figure 3A). However, in the spore analysis, only the LEU2-LYS2 interval (p = 0.014) was not significantly different from WT (p<0.007, Figure 3A). Similarly, in isogenic SK1 strains, CO frequencies were increased in csm4Δ mutants at four out of eight analyzed intervals in complete tetrads and at six out of eight intervals in the spore analysis (G-test, p<0.05, 95% confidence level). At the HIS4-LEU2 interval on chromosome III, CO levels were indistinguishable between WT and csm4Δ in both data sets (Figure 3B).


Csm4, in collaboration with Ndj1, mediates telomere-led chromosome dynamics and recombination during yeast meiosis.

Wanat JJ, Kim KP, Koszul R, Zanders S, Weiner B, Kleckner N, Alani E - PLoS Genet. (2008)

Cumulative genetic distance (cM) in WT, csm4Δ, mlh1Δ, msh5Δ, and ndj1Δ strains.In panels A and B, each bar is divided in sectors corresponding to genetic intervals in the region of the chromosome analyzed. A) Cumulative genetic distances between URA3 and HIS3 on chromosome XV in EAY1108/EAY1112 derived strains measured from tetrads (T) and single spores (S). B) Cumulative genetic distances between ADE2 and LEU2 on chromosome III, URA3 and CUP1 on chromosome VIII, and LYS5 and TRP5 on chromosome VII in the NH942/NH943 derived strains measured from tetrads (T) and single spores (S). See Tables 1 and S2 for raw data.
© Copyright Policy
Related In: Results  -  Collection

Show All Figures
getmorefigures.php?uid=PMC2533701&req=5

pgen-1000188-g003: Cumulative genetic distance (cM) in WT, csm4Δ, mlh1Δ, msh5Δ, and ndj1Δ strains.In panels A and B, each bar is divided in sectors corresponding to genetic intervals in the region of the chromosome analyzed. A) Cumulative genetic distances between URA3 and HIS3 on chromosome XV in EAY1108/EAY1112 derived strains measured from tetrads (T) and single spores (S). B) Cumulative genetic distances between ADE2 and LEU2 on chromosome III, URA3 and CUP1 on chromosome VIII, and LYS5 and TRP5 on chromosome VII in the NH942/NH943 derived strains measured from tetrads (T) and single spores (S). See Tables 1 and S2 for raw data.
Mentions: We examined crossing over in 12 different intervals by tetrad analysis in WT and csm4Δ (Figure 3, Tables 1, S1, and S2). The csm4Δ mutation conferred a 30–40% increase in the level of COs for all four intervals in the SK1 congenic strains. In the analysis of complete tetrads, the URA3-LEU2 and ADE2-HIS3 intervals were significantly different from WT (G-test, p<0.007, 95% confidence level, Dunn-Sidak correction, [34],[35]) but the LEU2-LYS2 (p = 0.07) and the LYS2-ADE2 (p = 0.013) were not (Figure 3A). However, in the spore analysis, only the LEU2-LYS2 interval (p = 0.014) was not significantly different from WT (p<0.007, Figure 3A). Similarly, in isogenic SK1 strains, CO frequencies were increased in csm4Δ mutants at four out of eight analyzed intervals in complete tetrads and at six out of eight intervals in the spore analysis (G-test, p<0.05, 95% confidence level). At the HIS4-LEU2 interval on chromosome III, CO levels were indistinguishable between WT and csm4Δ in both data sets (Figure 3B).

Bottom Line: In budding yeast, meiotic chromosomes exhibit dynamic movements, led by nuclear envelope (NE)-associated telomeres, throughout the zygotene and pachytene stages.Zygotene motion underlies the global tendency for colocalization of NE-associated chromosome ends in a "bouquet." In this study, we identify Csm4 as a new molecular participant in these processes and show that, unlike the two previously identified components, Ndj1 and Mps3, Csm4 is not required for meiosis-specific telomere/NE association.The recombination effects are discussed in the context of a model where the underlying defect is chromosome movement, the absence of which results in persistence of inappropriate chromosome relationships that, in turn, results in the observed mutant phenotypes.

View Article: PubMed Central - PubMed

Affiliation: Department of Molecular Biology and Genetics, Cornell University, Ithaca, New York, USA.

ABSTRACT
Chromosome movements are a general feature of mid-prophase of meiosis. In budding yeast, meiotic chromosomes exhibit dynamic movements, led by nuclear envelope (NE)-associated telomeres, throughout the zygotene and pachytene stages. Zygotene motion underlies the global tendency for colocalization of NE-associated chromosome ends in a "bouquet." In this study, we identify Csm4 as a new molecular participant in these processes and show that, unlike the two previously identified components, Ndj1 and Mps3, Csm4 is not required for meiosis-specific telomere/NE association. Instead, it acts to couple telomere/NE ensembles to a force generation mechanism. Mutants lacking Csm4 and/or Ndj1 display the following closely related phenotypes: (i) elevated crossover (CO) frequencies and decreased CO interference without abrogation of normal pathways; (ii) delayed progression of recombination, and recombination-coupled chromosome morphogenesis, with resulting delays in the MI division; and (iii) nondisjunction of homologs at the MI division for some reason other than absence of (the obligatory) CO(s). The recombination effects are discussed in the context of a model where the underlying defect is chromosome movement, the absence of which results in persistence of inappropriate chromosome relationships that, in turn, results in the observed mutant phenotypes.

Show MeSH
Related in: MedlinePlus