Loss of meiotic double strand breaks triggers recruitment of recombination-independent pro-crossover factors in C. elegans spermatogenesis

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Abstract
A key event in meiosis is the conversion of a small subset of double strand breaks into interhomolog crossovers. In this study, we demonstrate that Caenorhabditis elegans male spermatogenesis has less robust mechanisms than hermaphrodite oogenesis in regulating crossover numbers. This is not a consequence of differences in meiotic prophase timing, sex chromosome genotype, or the presence or absence of germline apoptosis. Using the cyclin-like crossover marker COSA-1, we show that males are less efficient in both converting double strand breaks into crossover designated events and limiting their number, suggesting weakened crossover homeostasis. Surprisingly, we discovered that significant numbers of COSA-1 foci form at the very end of meiotic prophase in the absence of SPO-11 during spermatogenesis. These COSA-1-marked sites are also independent of homologous recombination, and Topoisomerases I and II. We find that the synaptonemal complex, which holds homologs in proximity, differently modulates COSA-1 enrichment to chromosomes in the absence of SPO-11 in males and hermaphrodites. Together, these findings suggest that males have less robust crossover control and that there are previously unrecognized lesions or structures at the end of meiotic prophase in spermatocytes that can accumulate crossover markers.
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Funding Information
  • Grantová Agentura ÄŒeské Republiky (GA23-04918S)
  • National Institute of General Medical Sciences (GM103860)
  • National Institute of General Medical Sciences (GM103860S1)
  • National Institute of General Medical Sciences (R25GM116690)
  • Medical Research Foundation (MC-A652-5PY60)

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