Bicaudal Cis required for the function of the follicular epithelium during oogenesis inRhodnius prolixus

Abstract

11The morphology and physiology of the oogenesis have been well studied in 12 the vector of Chagas disease Rhodnius prolixus. However, the molecular 13 interactions that regulate the process of egg formation, key for the reproductive 14 cycle of the vector, is still largely unknown. In order to understand the molecular 15 and cellular basis of the oogenesis we examined the function of the gene 16 Bicaudal C (BicC) during oogenesis and early development of R. prolixus. We 17 show that R. prolixus BicC (Rp-BicC) gene is expressed in the germarium, with 18 cytoplasmic distribution, as well as in the follicular epithelium of the developing 19 oocytes. RNAi silencing of Rp-BicC resulted in sterile females that lay few, small, 20 non-viable eggs. The ovaries are reduced in size and show a disarray of the 21 follicular epithelium. This indicates that Rp-BicC has a central role in the 22 regulation of oogenesis. Although the follicular cells are able to form the chorion, 23 the uptake of vitelline by the oocytes is compromised. We show evidence that the 24 polarity of the follicular epithelium and the endocytic pathway, which is crucial for 25 the proper yolk deposition, are affected. This study provides insights into the 26 molecular mechanisms underlying oocyte development and show that Rp-BicC 27 is important for de developenta of the egg and, therefore, a key player in the 28 reproduction of this Chagas disease vector. 29 30 Author summary 31 The oogenesis is the process of egg formation. It is essential to guarantee 32 transgenerational inheritance. It implies the differentiation of the gamete (oocyte) 33 from a niche of stem cells in the germ line, the accumulation of yolk, and the 34 formation of the chorion. These events are entangled in a regulated manner by 35 the concerted communication between the different cell types that form the ovary. 36 It is regulated by endogenous gene networks and linked to the physiological state 37 of the insect by hormonal clues. This timely orchestrated process represents the 38 interaction of gene networks. The genetic regulation behind the oogenesis is 39 largely unknown in Rhodnius prolixus. Here we identified a gene required for egg 40 formation that interferes the uptake of the yolk by affecting the functional integrity 41 of the follicular epithelium. Our results are of interest for a better understanding 42 of a complex process essential for the survival of vector populations and provide 43 knowledge to envisage and design new strategies for vector control. 44 45 46 Introduction 47 Rhodnius prolixus, is a hematophagous insect and, like other triatomines, is 48 the vector of Trypanosoma cruzi, the agent of Chagas disease [1,2]. Chagas 49 disease is a life-threatening disease affecting millions of people worldwide [3]. As 50 vaccine are unavailable and disease treatment is unsafe, vector control is still the 51 most useful method to control the illness. In this context, as oogenesis is crucial 52 for embryo viability and population dynamics, molecular investigation on this 53...

Vector Control: Insights Arising from the Post-Genomics Findings on Insects’ Reproductive Biology

“…On that note, several genes that are somehow essential for oogenesis and generate unviable embryos have been identified and functionally tested in R. prolixus. The orthologue of Bicaudal C (BicC), a gene originally identified in D. melanogaster involved in embryonic patterning has shown to be maternally expressed and essential for the arrangement of the follicle cells [27]. The control of iron and heme homeostasis is particularly critical for hematophagous insects, especially for the strictly hematophagous triatomines, such R. prolixus.…”