A germline-specific splicing generates an extended ovo protein isoform required for Drosophila oogenesis

Most regulatory genes are employed multiple times to control different processes during development. The Drosophila Ovo/Shavenbaby (Svb) transcription factor is required both for germline and epidermal differentiation, two roles also found for its ortholog m-ovo1 in mice. In Drosophila, these two distinct functions are contributed by separate control regions directing the expression of Ovo/Svb in the germline (ovo) and soma (svb), respectively. We report here that alternative splicing represents an additional level of the regulation of Ovo/Svb functional specificity. Characterization of the ovo(D1rv23) mutation revealed that the intragenic insertion of a novel retrotransposon, romano, inactivates ovo without altering svb. We provide evidence that this insertion disrupts a germline-specific alternative exon, exon 2b, which encodes a 178-amino-acid internal extension (2B). While both isoforms, Ovo+2B and Ovo-2B, accumulate during oogenesis, only Ovo+2B is able to fulfill germinal ovo functions. Ovo-2B is unable, even when overexpressed, to fully rescue oogenic defects resulting from the absence of wild type ovo product. By contrast, either Ovo+2B or Ovo-2B germline protein can substitute for Svb in the epidermis. Our results emphasize the specific features of splicing in the germline, and reveal its functional importance for the control of ovo/svb-dependent ovarian and epidermal differentiation.