ATM and ATR Influence Meiotic Crossover Formation Through Antagonistic and Overlapping Functions in Caenorhabditis elegans

Genetics. 2019 Jun;212(2):431-443. doi: 10.1534/genetics.119.302193. Epub 2019 Apr 23.


During meiosis, formation of double-strand breaks (DSBs) and repair by homologous recombination between homologs creates crossovers (COs) that facilitate chromosome segregation. CO formation is tightly regulated to ensure the integrity of this process. The DNA damage response kinases, Ataxia-telangiectasia mutated (ATM) and RAD3-related (ATR) have emerged as key regulators of CO formation in yeast, flies, and mice, influencing DSB formation, repair pathway choice, and cell cycle progression. The molecular networks that ATM and ATR influence during meiosis are still being resolved in other organisms. Here, we show that Caenorhabditis elegans ATM and ATR homologs, ATM-1 and ATL-1 respectively, act at multiple steps in CO formation to ultimately ensure that COs are formed on all chromosomes. We show a role for ATM-1 in regulating the choice of repair template, biasing use of the homologous chromosome instead of the sister chromatid. Our data suggest a model in which ATM-1 and ATL-1 have antagonistic roles in very early repair processing, but are redundantly required for accumulation of the RAD-51 recombinase at DSB sites. We propose that these features of ATM-1 and ATL-1 ensure both CO formation on all chromosomes and accurate repair of additional DSBs.

Keywords: ATM; ATR; C. elegans; DSB repair; meiosis.

Publication types

  • Research Support, N.I.H., Extramural
  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Ataxia Telangiectasia Mutated Proteins / genetics
  • Ataxia Telangiectasia Mutated Proteins / metabolism*
  • Ataxia Telangiectasia Mutated Proteins / physiology
  • Caenorhabditis elegans / genetics*
  • Caenorhabditis elegans / metabolism
  • Caenorhabditis elegans Proteins / metabolism*
  • Chromosome Segregation / genetics*
  • Crossing Over, Genetic*
  • DNA Breaks, Double-Stranded*
  • DNA Repair / genetics
  • Endodeoxyribonucleases / genetics
  • Meiosis / genetics*
  • Rad51 Recombinase / metabolism
  • Recombinational DNA Repair*


  • Caenorhabditis elegans Proteins
  • Atl-1 protein, C elegans
  • Ataxia Telangiectasia Mutated Proteins
  • atm-1 protein, C elegans
  • Rad51 Recombinase
  • rad-51 protein, C elegans
  • Endodeoxyribonucleases
  • meiotic recombination protein SPO11

Associated data

  • figshare/10.25386/genetics.7973795