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Distinct functions of S. pombe Rec12 (Spo11) protein and Rec12-dependent crossover recombination (chiasmata) in meiosis I; and a requirement for Rec12 in meiosis II.

Sharif WD, Glick GG, Davidson MK, Wahls WP - Cell Chromosome (2002)

Bottom Line: CONCLUSIONS: Rec12 is a 345 amino acid protein required for most crossover recombination and for chiasmatic segregation of chromosomes during meiosis I.Rec12 also participates in a backup distributive (achiasmatic) system of chromosome segregation during meiosis I.In addition, catalytically-active Rec12 mediates some signal that is required for faithful equational segregation of chromosomes during meiosis II.

View Article: PubMed Central - HTML - PubMed

Affiliation: Department of Biochemistry and Molecular Biology, University of Arkansas for Medical Sciences, Little Rock, AR 72205, USA. WahlsWayneP@uams.edu

ABSTRACT
BACKGROUND: In most organisms proper reductional chromosome segregation during meiosis I is strongly correlated with the presence of crossover recombination structures (chiasmata); recombination deficient mutants lack crossovers and suffer meiosis I nondisjunction. We report that these functions are separable in the fission yeast Schizosaccharomyces pombe. RESULTS: Intron mapping and expression studies confirmed that Rec12 is a member of the Spo11/Top6A topoisomerase family required for the formation of meiotic dsDNA breaks and recombination. rec12-117, rec12-D15 (), and rec12-Y98F (active site) mutants lacked most crossover recombination and chromosomes segregated abnormally to generate aneuploid meiotic products. Since S. pombe contains only three chromosome pairs, many of those aneuploid products were viable. The types of aberrant chromosome segregation were inferred from the inheritance patterns of centromere linked markers in diploid meiotic products. The rec12-117 and rec12-D15 mutants manifest segregation errors during both meiosis I and meiosis II. Remarkably, the rec12-Y98F (active site) mutant exhibited essentially normal meiosis I segregation patterns, but still exhibited meiosis II segregation errors. CONCLUSIONS: Rec12 is a 345 amino acid protein required for most crossover recombination and for chiasmatic segregation of chromosomes during meiosis I. Rec12 also participates in a backup distributive (achiasmatic) system of chromosome segregation during meiosis I. In addition, catalytically-active Rec12 mediates some signal that is required for faithful equational segregation of chromosomes during meiosis II.

No MeSH data available.


Related in: MedlinePlus

Segregation patterns of chromosomes. (A) Normal meiosis produces four haploid products. Aberrant segregation may be monitored using centromere linked markers. Diploid spores resulting from MI nondisjunction (B) and precocious separation of sister chromatids (D) are predominantly heterozygous for the centromere, whereas those arising by MII nondisjunction (C) are homozygous for the centromere. (E) Diploid spore colonies were genotyped for heteroallelic marker loci tightly linked to each of the three centromeres (lys1, chromosome I; tps13, chromosome II; and ade6, chromosome III). Each value is based upon genotyping between 50 and 80 diploid spore colonies and the mean ± standard deviation for all three chromosomes in each mutant is indicated (black bars). The data were from crosses of strains: WSP1807 × WSP1216; WSP1825 × WSP1884; and WSP1670 × WSP1809.
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Figure 5: Segregation patterns of chromosomes. (A) Normal meiosis produces four haploid products. Aberrant segregation may be monitored using centromere linked markers. Diploid spores resulting from MI nondisjunction (B) and precocious separation of sister chromatids (D) are predominantly heterozygous for the centromere, whereas those arising by MII nondisjunction (C) are homozygous for the centromere. (E) Diploid spore colonies were genotyped for heteroallelic marker loci tightly linked to each of the three centromeres (lys1, chromosome I; tps13, chromosome II; and ade6, chromosome III). Each value is based upon genotyping between 50 and 80 diploid spore colonies and the mean ± standard deviation for all three chromosomes in each mutant is indicated (black bars). The data were from crosses of strains: WSP1807 × WSP1216; WSP1825 × WSP1884; and WSP1670 × WSP1809.

Mentions: Because each of the rec12 mutants had aberrant meiotic chromosome segregation (Figure 3), produced a high frequency of viable meiotic products (Figure 4A), and produced a high frequency of meiotic diploids (Figure 4B), we were able to monitor directly the segregation patterns of all three chromosome pairs in each of the mutants. Meiotic diploids were genotyped for heteroallelic, centromere-linked markers on each of the three chromosomes. Those data were compared to the inheritance patterns predicted for each type of chromosome missegregation (Figure 5).


Distinct functions of S. pombe Rec12 (Spo11) protein and Rec12-dependent crossover recombination (chiasmata) in meiosis I; and a requirement for Rec12 in meiosis II.

Sharif WD, Glick GG, Davidson MK, Wahls WP - Cell Chromosome (2002)

Segregation patterns of chromosomes. (A) Normal meiosis produces four haploid products. Aberrant segregation may be monitored using centromere linked markers. Diploid spores resulting from MI nondisjunction (B) and precocious separation of sister chromatids (D) are predominantly heterozygous for the centromere, whereas those arising by MII nondisjunction (C) are homozygous for the centromere. (E) Diploid spore colonies were genotyped for heteroallelic marker loci tightly linked to each of the three centromeres (lys1, chromosome I; tps13, chromosome II; and ade6, chromosome III). Each value is based upon genotyping between 50 and 80 diploid spore colonies and the mean ± standard deviation for all three chromosomes in each mutant is indicated (black bars). The data were from crosses of strains: WSP1807 × WSP1216; WSP1825 × WSP1884; and WSP1670 × WSP1809.
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Related In: Results  -  Collection

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Figure 5: Segregation patterns of chromosomes. (A) Normal meiosis produces four haploid products. Aberrant segregation may be monitored using centromere linked markers. Diploid spores resulting from MI nondisjunction (B) and precocious separation of sister chromatids (D) are predominantly heterozygous for the centromere, whereas those arising by MII nondisjunction (C) are homozygous for the centromere. (E) Diploid spore colonies were genotyped for heteroallelic marker loci tightly linked to each of the three centromeres (lys1, chromosome I; tps13, chromosome II; and ade6, chromosome III). Each value is based upon genotyping between 50 and 80 diploid spore colonies and the mean ± standard deviation for all three chromosomes in each mutant is indicated (black bars). The data were from crosses of strains: WSP1807 × WSP1216; WSP1825 × WSP1884; and WSP1670 × WSP1809.
Mentions: Because each of the rec12 mutants had aberrant meiotic chromosome segregation (Figure 3), produced a high frequency of viable meiotic products (Figure 4A), and produced a high frequency of meiotic diploids (Figure 4B), we were able to monitor directly the segregation patterns of all three chromosome pairs in each of the mutants. Meiotic diploids were genotyped for heteroallelic, centromere-linked markers on each of the three chromosomes. Those data were compared to the inheritance patterns predicted for each type of chromosome missegregation (Figure 5).

Bottom Line: CONCLUSIONS: Rec12 is a 345 amino acid protein required for most crossover recombination and for chiasmatic segregation of chromosomes during meiosis I.Rec12 also participates in a backup distributive (achiasmatic) system of chromosome segregation during meiosis I.In addition, catalytically-active Rec12 mediates some signal that is required for faithful equational segregation of chromosomes during meiosis II.

View Article: PubMed Central - HTML - PubMed

Affiliation: Department of Biochemistry and Molecular Biology, University of Arkansas for Medical Sciences, Little Rock, AR 72205, USA. WahlsWayneP@uams.edu

ABSTRACT
BACKGROUND: In most organisms proper reductional chromosome segregation during meiosis I is strongly correlated with the presence of crossover recombination structures (chiasmata); recombination deficient mutants lack crossovers and suffer meiosis I nondisjunction. We report that these functions are separable in the fission yeast Schizosaccharomyces pombe. RESULTS: Intron mapping and expression studies confirmed that Rec12 is a member of the Spo11/Top6A topoisomerase family required for the formation of meiotic dsDNA breaks and recombination. rec12-117, rec12-D15 (), and rec12-Y98F (active site) mutants lacked most crossover recombination and chromosomes segregated abnormally to generate aneuploid meiotic products. Since S. pombe contains only three chromosome pairs, many of those aneuploid products were viable. The types of aberrant chromosome segregation were inferred from the inheritance patterns of centromere linked markers in diploid meiotic products. The rec12-117 and rec12-D15 mutants manifest segregation errors during both meiosis I and meiosis II. Remarkably, the rec12-Y98F (active site) mutant exhibited essentially normal meiosis I segregation patterns, but still exhibited meiosis II segregation errors. CONCLUSIONS: Rec12 is a 345 amino acid protein required for most crossover recombination and for chiasmatic segregation of chromosomes during meiosis I. Rec12 also participates in a backup distributive (achiasmatic) system of chromosome segregation during meiosis I. In addition, catalytically-active Rec12 mediates some signal that is required for faithful equational segregation of chromosomes during meiosis II.

No MeSH data available.


Related in: MedlinePlus