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

Abstract

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 ovoD1rv23 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, Ovo32B and Ovo32B, accumulate during oogenesis, only Ovo32B is able to fulfill germinal ovo functions. Ovo32B is unable, even when overexpressed, to fully rescue oogenic defects resulting from the absence of wild type ovo product. By contrast, either Ovo32B or Ovo32B 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. © 2002 Elsevier Science (USA).