The impact of developmental stage, tissue type, and sex on DNA double-strand break repair in Drosophila melanogaster

PLoS Genet. 2024 Apr 29;20(4):e1011250. doi: 10.1371/journal.pgen.1011250. eCollection 2024 Apr.

Abstract

Accurate repair of DNA double-strand breaks (DSBs) is essential for the maintenance of genome integrity, as failure to repair DSBs can result in cell death. The cell has evolved two main mechanisms for DSB repair: non-homologous end-joining (NHEJ) and homology-directed repair (HDR), which includes single-strand annealing (SSA) and homologous recombination (HR). While certain factors like age and state of the chromatin are known to influence DSB repair pathway choice, the roles of developmental stage, tissue type, and sex have yet to be elucidated in multicellular organisms. To examine the influence of these factors, DSB repair in various embryonic developmental stages, larva, and adult tissues in Drosophila melanogaster was analyzed through molecular analysis of the DR-white assay using Tracking across Indels by DEcomposition (TIDE). The proportion of HR repair was highest in tissues that maintain the canonical (G1/S/G2/M) cell cycle and suppressed in both terminally differentiated and polyploid tissues. To determine the impact of sex on repair pathway choice, repair in different tissues in both males and females was analyzed. When molecularly examining tissues containing mostly somatic cells, males and females demonstrated similar proportions of HR and NHEJ. However, when DSB repair was analyzed in male and female premeiotic germline cells utilizing phenotypic analysis of the DR-white assay, there was a significant decrease in HR in females compared to males. This study describes the impact of development, tissue-specific cycling profile, and, in some cases, sex on DSB repair outcomes, underscoring the complexity of repair in multicellular organisms.

Publication types

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

MeSH terms

  • Animals
  • Cell Cycle / genetics
  • DNA Breaks, Double-Stranded*
  • DNA End-Joining Repair / genetics
  • DNA Repair / genetics
  • Drosophila Proteins / genetics
  • Drosophila Proteins / metabolism
  • Drosophila melanogaster* / genetics
  • Drosophila melanogaster* / growth & development
  • Female
  • Homologous Recombination / genetics
  • Male
  • Recombinational DNA Repair

Substances

  • Drosophila Proteins

Grants and funding

This work was supported by National Institute of General Medical Sciences, United States- US (1R15GM129628; including salary support to J.R.L.), the Georgetown University Summer Mentored Undergraduate Research Fellowship Program (E.L.G.), the Georgetown University Provost’s Undergraduate Research Fellowship Program (E.L.G.), and the Georgetown University Laidlaw Program (S.G.). The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript. Publication fees were supported in part from Georgetown University Medical Center.