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In the  Drosophila  ovary, somatic escort cells (ECs) form a niche that promotes differentiation of germline stem cell (GSC) progeny. The piRNA (Piwi-interacting RNA) pathway, which represses transposable elements (TEs), is required in ECs to prevent the accumulation of undifferentiated germ cells (germline tumor phenotype). The soma-specific piRNA cluster  flamenco  ( flam ) produces a substantial part of somatic piRNAs. Here, we characterized the biological effects of somatic TE activation on germ cell differentiation in  flam  mutants. We revealed that the choice between normal and tumorous phenotypes of  flam  mutant ovaries depends on the number of persisting ECs, which is determined at the larval stage. Accordingly, we found much more frequent DNA breaks in somatic cells of  flam  larval ovaries than in adult ECs. The absence of Chk2 or ATM checkpoint kinases dramatically enhanced oogenesis defects of  flam  mutants, in contrast to the germline TE-induced defects that are known to be mostly suppressed by  сhk2  mutation. These results demonstrate a crucial role of checkpoint kinases in protecting niche cells against deleterious TE activation and suggest substantial differences between DNA damage responses in ovarian somatic and germ cells.

Special vulnerability of somatic niche cells to transposable element activation in Drosophila larval ovaries