Cis-acting determinants affecting centromere function, sister-chromatid cohesion and reciprocal recombination during meiosis in Saccharomyces cerevisiae

D. D. Sears, J. H. Hegemann, J. H. Shero, P. Hieter

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Abstract

We have employed a system that utilizes homologous pairs of human DNA- derived yeast artificial chromosomes (YACs) as marker chromosomes to assess the specific role (s) of conserved centromere DNA elements (CDEI, CDEII and CDEIII) in meiotic chromosome disjunction fidelity. Thirteen different centromere (CEN) mutations were tested for their effects on meiotic centromere function. YACs containing a wild-type CEN DNA sequence segregate with high fidelity in meiosis I (99% normal segregation) and in meiosis II (96% normal segregation). YACs containing a 31-bp deletion mutation in centromere DNA element II (CDEIIΔ31) in either a heterocentric (mutant/wild type), homocentric (mutant/mutant) or monosomic (mutant/-) YAC pair configuration exhibited high levels (16-28%) of precocious sister-chromatid segregation (PSS) and increased levels (1-6%) of nondisjunction meiosis I (NDI). YACs containing this mutation also exhibit high levels (21%) of meiosis II nondisjunction. Interestingly, significant alterations in homolog recombination frequency were observed in the exceptional PSS class of tetrads, suggesting unusual interactions between prematurely separated sister chromatids and their homologous nonsister chromatids. We also have assessed the meiotic segregation effects of rare gene conversion events occurring at sites located immediately adjacent to or distantly from the centromere region. Proximal gene conversion events were associated with extremely high levels (60%) of meiosis I segregation errors (including both PSS and NDI), whereas distal events had no apparent effect. Taken together, our results indicate a critical role for CDEII in meiosis and underscore the importance of maintaining sister-chromatid cohesion for proper recombination in meiotic prophase and for proper disjunction in meiosis I.

Original languageEnglish (US)
Pages (from-to)1159-1173
Number of pages15
JournalGenetics
Volume139
Issue number3
StatePublished - Jan 1 1995
Externally publishedYes

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Chromatids
Centromere
Meiosis
Genetic Recombination
Saccharomyces cerevisiae
Yeast Artificial Chromosomes
Gene Conversion
DNA
Chromosomes
Prophase
Mutation
Sequence Deletion
Genetic Markers

ASJC Scopus subject areas

  • Genetics

Cite this

Cis-acting determinants affecting centromere function, sister-chromatid cohesion and reciprocal recombination during meiosis in Saccharomyces cerevisiae. / Sears, D. D.; Hegemann, J. H.; Shero, J. H.; Hieter, P.

In: Genetics, Vol. 139, No. 3, 01.01.1995, p. 1159-1173.

Research output: Contribution to journalArticle

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abstract = "We have employed a system that utilizes homologous pairs of human DNA- derived yeast artificial chromosomes (YACs) as marker chromosomes to assess the specific role (s) of conserved centromere DNA elements (CDEI, CDEII and CDEIII) in meiotic chromosome disjunction fidelity. Thirteen different centromere (CEN) mutations were tested for their effects on meiotic centromere function. YACs containing a wild-type CEN DNA sequence segregate with high fidelity in meiosis I (99{\%} normal segregation) and in meiosis II (96{\%} normal segregation). YACs containing a 31-bp deletion mutation in centromere DNA element II (CDEIIΔ31) in either a heterocentric (mutant/wild type), homocentric (mutant/mutant) or monosomic (mutant/-) YAC pair configuration exhibited high levels (16-28{\%}) of precocious sister-chromatid segregation (PSS) and increased levels (1-6{\%}) of nondisjunction meiosis I (NDI). YACs containing this mutation also exhibit high levels (21{\%}) of meiosis II nondisjunction. Interestingly, significant alterations in homolog recombination frequency were observed in the exceptional PSS class of tetrads, suggesting unusual interactions between prematurely separated sister chromatids and their homologous nonsister chromatids. We also have assessed the meiotic segregation effects of rare gene conversion events occurring at sites located immediately adjacent to or distantly from the centromere region. Proximal gene conversion events were associated with extremely high levels (60{\%}) of meiosis I segregation errors (including both PSS and NDI), whereas distal events had no apparent effect. Taken together, our results indicate a critical role for CDEII in meiosis and underscore the importance of maintaining sister-chromatid cohesion for proper recombination in meiotic prophase and for proper disjunction in meiosis I.",
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