Functional male accessory glands and fertility in Drosophila require novel ecdysone receptor

Abstract

In many insects, the accessory gland, a secretory tissue of the male reproductive system, is essential for male fertility. Male accessory gland is the major source of proteinaceous secretions, collectively called as seminal proteins (or accessory gland proteins), which upon transfer, manipulate the physiology and behavior of mated females. Insect hormones such as ecdysteroids and juvenoids play a key role in accessory gland development and protein synthesis but little is known about underlying molecular players and their mechanism of action. Therefore, in the present study, we examined the roles of hormone-dependent transcription factors (Nuclear Receptors), in accessory gland development, function and male fertility of a genetically tractable insect model, Drosophila melanogaster. First, we carried out an RNAi screen involving 19 hormone receptors, individually and specifically, in a male reproductive tissue (accessory gland) for their requirement in Drosophila male fertility. Subsequently, by using independent RNAi/ dominant negative forms, we show that Ecdysone Receptor (EcR) is essential for male fertility due to its requirement in the normal development of accessory glands in Drosophila: EcR depleted glands fail to make seminal proteins and have dying cells. Further, our data point to a novel ecdysone receptor that does not include Ultraspiracle but is probably comprised of EcR isoforms in Drosophila male accessory glands. Our data suggest that this novel ecdysone receptor might act downstream of homeodomain transcription factor paired (prd) in the male accessory gland. Overall, the study suggests novel ecdysone receptor as an important player in the hormonal regulation of seminal protein production and insect male fertility.

Disruption of the ovarian serine protease (Osp) gene causes female sterility in Bombyx mori and Spodoptera litura

“…76,77 Oar1 and Oar2 are G protein-coupled octopamine receptors involved in the transmission of signals from the central nervous system that cause physiological changes in the female reproductive tract to regulate ovulation. [78][79][80][81] Our data indicate that mutation of BmOsp down-regulates these related genes in silkworm, which presumably disrupts various steps in the reproductive process to result in female sterility.…”

Functional characterization of ultraspiracle in Leptinotarsa decemlineata using RNA interference assay

“…In D. melanogaster male adults, for example, EcR‐depleted (but not USP‐depleted) accessory glands fail to make seminal proteins and have dying cells. The active receptor may be a homodimer, probably involving all the isoforms of EcR (Sharma et al , ) . A similar paradigm is observed in the expression of genes encoding glue proteins in the salivary glands (Costantino et al , ).…”

The insect HR38 nuclear receptor, a member of the NR4A subfamily, is a synchronizer of reproductive activity in a moth

“…The only available information is that the A. ipsilon EcR and USP are expressed at high levels in SAGs (E. Gassias, unpublished data), thereby indicating that this reproductive organ is a target of ecdysteroid signalling in this species. Another interesting observation is that the Agrotis HR38 depleted SAGs, which exhibited a reduced protein synthesis, were phenotypically identical to the Drosophila EcR depleted SAGs . Together with the age‐dependent increase in the SAG AiHR38 expression paralleled with the increased levels of circulating 20E, these observations lead us to speculate that as in ALs, the SAG AiHR38 may be an actor of putative 20E/EcR/USP pathway in the control of secretory activity of SAGs in A. ipsilon male.…”

“…It is well established that the growth and the stimulation of protein synthesis in the male SAGs are under the influence of 20E [61,62]. In several insect species, high activity of EcR/USP complex was observed in SAGs and putative EcRE has been located in the upstream region of some of the Acps genes [32,[63][64][65], thus revealing the significance of EcR/USP-dependent ecdysteroid signalling in the secretory function of this tissue. In D. melanogaster male, a recent study offered evidence that EcR may function without USP by forming stable homodimers in transmitting the 20E signal within the SAGs [65].…”