Bicaudal C is required for the function of the follicular epithelium during oogenesis in Rhodnius prolixus

Abstract

The morphology and physiology of the oogenesis have been well studied in the vector of Chagas disease Rhodnius prolixus. However, the molecular interactions that regulate the process of egg formation, key for the reproductive cycle of the vector, is still largely unknown. In order to understand the molecular and cellular basis of the oogenesis we examined the function of the gene Bicaudal C (BicC) during oogenesis and early development of R. prolixus. We show that R. prolixus BicC (Rp-BicC) gene is expressed in the germarium, with cytoplasmic distribution, as well as in the follicular epithelium of the developing oocytes. RNAi silencing of Rp-BicC resulted in sterile females that lay few, small, non-viable eggs. The ovaries are reduced in size and show a disarray of the follicular epithelium. This indicates that Rp-BicC has a central role in the regulation of oogenesis. Although the follicular cells are able to form the chorion, the uptake of vitelline by the oocytes is compromised. We show evidence that the polarity of the follicular epithelium and the endocytic pathway, which is crucial for the proper yolk deposition, are affected. This study provides insights into the molecular mechanisms underlying oocyte development and show that Rp-BicC is important for de developenta of the egg and, therefore, a key player in the reproduction of this Chagas disease vector. Author summaryThe oogenesis is the process of egg formation. It is essential to guarantee transgenerational inheritance. It implies the differentiation of the gamete (oocyte) from a niche of stem cells in the germ line, the accumulation of yolk, and the formation of the chorion. These events are entangled in a regulated manner by the concerted communication between the different cell types that form the ovary. It is regulated by endogenous gene networks and linked to the physiological state of the insect by hormonal clues. This timely orchestrated process represents the interaction of gene networks. The genetic regulation behind the oogenesis is largely unknown in Rhodnius prolixus. Here we identified a gene required for egg formation that interferes the uptake of the yolk by affecting the functional integrity of the follicular epithelium. Our results are of interest for a better understanding of a complex process essential for the survival of vector populations and provide knowledge to envisage and design new strategies for vector control.