The transcription factor Capicua maintains the oocyte polarity in the panoistic ovary of the German cockroach

Abstract

The establishment of the symmetry axis is crucial for the development of all organisms. In insects, this process begins early in oogenesis with the correct distribution of the mRNAs and proteins in the oocyte. One protein that plays a role in organizing this distribution is the transcription factor Capicua (Cic). Cic has been studied in the context of oogenesis and embryonic development in Drosophila melanogaster. It is maternally expressed, begins essential for establishing the dorsoventral axis, and functions as a transcriptional repressor. Although the Cic sequences are conserved across species, their function in other types of insect ovaries is still little known. We wondered whether the function of Cic in insects has been maintained through evolution despite the ovary type or if it has been modified in parallel to the ovary evolution. To address this, we studied the Cic function in a phylogenetically basal insect, the cockroach Blattella germanica, a species with panoistic ovaries. Our findings show that B. germanica Cic is essential for oocyte development and the maturation of ovarian follicles. A loss of Cic function leads to disrupted cytoskeletal organization, defects in anterior-posterior polarity, and compromised follicle integrity. The conservation and functional divergence of Cic across different species suggest evolutionary adaptations in the mechanisms of insect oogenesis.