Pseudosynapsis and decreased stringency of meiotic repair pathway choice on the hemizygous sex chromosome of Caenorhabditis elegans males

Paula M. Checchi, Katherine S. Lawrence, Mike V. Van, Braden J. Larson, Joanne Engebrecht

Research output: Contribution to journalArticle

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Abstract

During meiosis, accurate chromosome segregation relies on homology to mediate chromosome pairing, synapsis, and crossover recombination. Crossovers are dependent upon formation and repair of double-strand breaks (DSBs) by homologous recombination (HR). In males of many species, sex chromosomes are largely hemizygous, yet DSBs are induced along nonhomologous regions. Here we analyzed the genetic requirements for meiotic DSB repair on the completely hemizygous X chromosome of Caenorhabditis elegans males. Our data reveal that the kinetics of DSB formation, chromosome pairing, and synapsis are tightly linked in the male germ line. Moreover, DSB induction on the X is concomitant with a brief period of pseudosynapsis that may allow X sister chromatids to masquerade as homologs. Consistent with this, neither meiotic kleisins nor the SMC-5/6 complex are essential for DSB repair on the X. Furthermore, early processing of X DSBs is dependent on the CtIP/Sae2 homolog COM-1, suggesting that as with paired chromosomes, HR is the preferred pathway. In contrast, the X chromosome is refractory to feedback mechanisms that ensure crossover formation on autosomes. Surprisingly, neither RAD-54 nor BRC-2 are essential for DSB repair on the X, suggesting that unlike autosomes, the X is competent for repair in the absence of HR. When both RAD-54 and the structure-specific nuclease XPF-1 are abrogated, X DSBs persist, suggesting that single-strand annealing is engaged in the absence of HR. Our findings indicate that alteration in sister chromatid interactions and flexibility in DSB repair pathway choice accommodate hemizygosity on sex chromosomes.

Original languageEnglish (US)
Pages (from-to)543-560
Number of pages18
JournalGenetics
Volume197
Issue number2
DOIs
StatePublished - 2014

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Chromosome Pairing
Sex Chromosomes
Homologous Recombination
Caenorhabditis elegans
Chromatids
X Chromosome
Chromosome Segregation
Meiosis
Germ Cells
Genetic Recombination
Chromosomes

ASJC Scopus subject areas

  • Genetics

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Pseudosynapsis and decreased stringency of meiotic repair pathway choice on the hemizygous sex chromosome of Caenorhabditis elegans males. / Checchi, Paula M.; Lawrence, Katherine S.; Van, Mike V.; Larson, Braden J.; Engebrecht, Joanne.

In: Genetics, Vol. 197, No. 2, 2014, p. 543-560.

Research output: Contribution to journalArticle

Checchi, Paula M. ; Lawrence, Katherine S. ; Van, Mike V. ; Larson, Braden J. ; Engebrecht, Joanne. / Pseudosynapsis and decreased stringency of meiotic repair pathway choice on the hemizygous sex chromosome of Caenorhabditis elegans males. In: Genetics. 2014 ; Vol. 197, No. 2. pp. 543-560.
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