Endocrine network essential for reproductive success in Drosophila melanogaster

Abstract

Ecdysis-triggering hormone (ETH) was originally discovered and characterized as a molt termination signal in insects through its regulation of the ecdysis sequence. Here we report that ETH persists in adult Drosophila melanogaster, where it functions as an obligatory allatotropin to promote juvenile hormone (JH) production and reproduction. ETH signaling deficits lead to sharply reduced JH levels and consequent reductions of ovary size, egg production, and yolk deposition in mature oocytes. Expression of ETH and ETH receptor genes is in turn dependent on ecdysone (20E). Furthermore, 20E receptor knockdown specifically in Inka cells reduces fecundity. Our findings indicate that the canonical developmental roles of 20E, ETH, and JH during juvenile stages are repurposed to function as an endocrine network essential for reproductive success.ecdysis triggering hormone | ecdysone | juvenile hormone | fecundity | oogenesis T he life history of insects is characterized by radical morphogenetic transformations, whereby tissues are reorganized and hormones are repurposed for roles associated with stage-specific functions. During development, larvae complete each molt by shedding the cuticle under control of ecdysis triggering hormones (ETHs) targeting central peptidergic ensembles to orchestrate an innate behavioral sequence (1-3). Previous observations that Inka cells, the sole source of ETHs, persist into the adult stage (4) suggest possible reproductive functions for these peptides.We hypothesized that ETHs regulate juvenile hormone (JH) levels, based on the report of ETH receptor (ETHR) expression in the corpora allata (CA) of the silkworm, Bombyx mori (5). Evidence that ETH functions as an allatotropin in the yellow fever mosquito Aedes aegypti came from a recent study showing its activation of JH acid methyltransferase (6).JH is a sesquiterpenoid hormone with well-known morphogenetic and gonadotropic functions. In Drosophila, adult phenotypes resulting from reduction of JH levels have been characterized through induction of cell death in the CA or through enhancement of its degradation (7,8). Based on evidence from studies on Bombyx and Aedes, we investigated whether ETH functions as an allatotropin in adult Drosophila and the extent to which it may be necessary for reproductive functions.Previous studies showed that ecdysone (20E) regulates synthesis and release of ETH and expression of ETHR during larval stages of moths and mosquitoes (9-12). More recently, selftranscribing active regulatory region sequencing (STARR-Seq) data confirm that 20E induces 20E receptor (EcR) enhancer activity in promoters of both ETH and ETHR genes (13). Because circulating 20E levels are of major physiological and reproductive relevance (14), we also asked whether 20E influences ETH gene expression during the adult stage.Here we describe functional roles for 20E, ETH, and JH as a hormonal triad essential for reproductive success in Drosophila.In particular, we confirm persistence of ETH signaling throughout adulthood and demonstrate it...

Recent advances in neuropeptide signaling in Drosophila, from genes to physiology and behavior

“…shown that ETH is present in adult Inka cells (peritracheal cells) and it also promotes JH production and associated reproductive physiology via activation of ETH receptor in the corpora allata [494]. The release of ETH is dependent on 20E just like it is during the larval ecdysis (see next section) [292,495,496].…”

Transcriptome analysis reveals nutrition‐ and age‐related patterns of gene expression in the fat body of pre‐overwintering bumble bee queens

“…The list contained an orthologue to the gene encoding ETHR. This gene encodes two isoforms of a G protein‐coupled receptor (Park, Kim, Dupriez, & Adams, ) that mediate JH signalling in adult flies (Lee et al, ; Meiselman et al, ). Chronologically, this gene was up‐regulated at ages 3 and 6 days, then down‐regulated in the oldest group (age 12 days), but still expressed at a higher level than the age 0 day group (Figure a).…”

“…ETH was originally characterized for its role in early development and ecdysis (Zitnan, Kingan, Hermesman, & Adams, ). Interestingly, a recent study in the fruit fly showed that ETH also regulates oogenesis and fecundity through JH production in adults (Meiselman et al, ), although its role in the adult fat body is unknown. We also found evidence that there are interactive effects of nutrition and age.…”

“…Interestingly, a recent study in the fruit fly showed that ETH F I G U R E 3 Hierarchical clustering analysis using the top 100 most differentially expressed genes (significant at FDR-corrected p < .05) in deseq2 also regulates oogenesis and fecundity through JH production in adults (Meiselman et al, 2017), although its role in the adult fat body is unknown. We also found evidence that there are interactive effects of nutrition and age.…”

Genómica, proteómica y fisiología de neuropéptidos en el insecto triatomino Rhodnius prolixus

“…En principio, los resultados de RhoprE75 para el silenciamiento con dsOKs parecen contradictorios con el resto de los datos. Sin embargo, E75 se ha observado en algunas especies que responde negativamente a JH (Meiselman, Lee et al 2017). Reportes recientes han demostrado que la hormona ETH (en combinación con 20E) regula positivamente la síntesis de JH en procesos asociados a la muda y ovogénesis en dípteros (Meiselman, Lee et al 2017).…”