The Homeodomain Protein Defective Proventriculus Is Essential for Male Accessory Gland Development to Enhance Fecundity in Drosophila

Minami, Ryunosuke; Wakabayashi, Miyuki; Sugimori, Seiko; Taniguchi, Kiichiro; Kokuryo, Akihiko; Imano, Takao; Adachi‐Yamada, Takashi; Watanabe, Naoko; Nakagoshi, Hideki

doi:10.1371/journal.pone.0032302

Cited by 36 publications

(36 citation statements)

References 44 publications

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“…Our results are consistent with findings about secondary cell function obtained independently by Minami et al, from their study of dve mutants [76]. The inability of iab-6 cocu males to maintain the PMR in their mates is consistent with perturbation of the function of the “LTR network”.…”

Section: Discussionsupporting

confidence: 93%

A Novel Function for the Hox Gene Abd-B in the Male Accessory Gland Regulates the Long-Term Female Post-Mating Response in Drosophila

et al. 2013

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In insects, products of the male reproductive tract are essential for initiating and maintaining the female post-mating response (PMR). The PMR includes changes in egg laying, receptivity to courting males, and sperm storage. In Drosophila, previous studies have determined that the main cells of the male accessory gland produce some of the products required for these processes. However, nothing was known about the contribution of the gland's other secretory cell type, the secondary cells. In the course of investigating the late functions of the homeotic gene, Abdominal-B (Abd-B), we discovered that Abd-B is specifically expressed in the secondary cells of the Drosophila male accessory gland. Using an Abd-B BAC reporter coupled with a collection of genetic deletions, we discovered an enhancer from the iab-6 regulatory domain that is responsible for Abd-B expression in these cells and that apparently works independently from the segmentally regulated chromatin domains of the bithorax complex. Removal of this enhancer results in visible morphological defects in the secondary cells. We determined that mates of iab-6 mutant males show defects in long-term egg laying and suppression of receptivity, and that products of the secondary cells are influential during sperm competition. Many of these phenotypes seem to be caused by a defect in the storage and gradual release of sex peptide in female mates of iab-6 mutant males. We also found that Abd-B expression in the secondary cells contributes to glycosylation of at least three accessory gland proteins: ovulin (Acp26Aa), CG1656, and CG1652. Our results demonstrate that long-term post-mating changes observed in mated females are not solely induced by main cell secretions, as previously believed, but that secondary cells also play an important role in male fertility by extending the female PMR. Overall, these discoveries provide new insights into how these two cell types cooperate to produce and maintain a robust female PMR.

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Section: Discussionsupporting

confidence: 93%

A Novel Function for the Hox Gene Abd-B in the Male Accessory Gland Regulates the Long-Term Female Post-Mating Response in Drosophila

et al. 2013

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“…This also agrees with previous studies, finding that knock down of phm and shd does not affect fertility of male Tribolium [66], and that ecdysteroids are essential for female, but not male, germ cell development in Drosophila [67]. Interestingly, a recent study found that the secondary cells of the Drosophila accessory glands produce a substance that induces a female post-mating response by influencing egg laying activity and sexual receptivity [68]. Considering the evidence that E has been observed to be a more potent stimulator of vitellogenesis than 20E [43], one could speculate that E may be produced by the secondary cells in Drosophila males and passed to the female during mating.…”

Section: Discussionsupporting

confidence: 93%

Accessory Gland as a Site for Prothoracicotropic Hormone Controlled Ecdysone Synthesis in Adult Male Insects

et al. 2013

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Insect steroid hormones (ecdysteroids) are important for female reproduction in many insect species and are required for the initiation and coordination of vital developmental processes. Ecdysteroids are also important for adult male physiology and behavior, but their exact function and site of synthesis remains unclear, although previous studies suggest that the reproductive system may be their source. We have examined expression profiles of the ecdysteroidogenic Halloween genes, during development and in adults of the flour beetle Tribolium castaneum. Genes required for the biosynthesis of ecdysone (E), the precursor of the molting hormone 20-hydroxyecdysone (20E), are expressed in the tubular accessory glands (TAGs) of adult males. In contrast, expression of the gene encoding the enzyme mediating 20E synthesis was detected in the ovaries of females. Further, Spookiest (Spot), an enzyme presumably required for endowing tissues with competence to produce ecdysteroids, is male specific and predominantly expressed in the TAGs. We also show that prothoracicotropic hormone (PTTH), a regulator of E synthesis during larval development, regulates ecdysteroid levels in the adult stage in Drosophila melanogaster and the gene for its receptor Torso seems to be expressed specifically in the accessory glands of males. The composite results suggest strongly that the accessory glands of adult male insects are the main source of E, but not 20E. The finding of a possible male-specific source of E raises the possibility that E and 20E have sex-specific roles analogous to the vertebrate sex steroids, where males produce primarily testosterone, the precursor of estradiol. Furthermore this study provides the first evidence that PTTH regulates ecdysteroid synthesis in the adult stage and could explain the original finding that some adult insects are a rich source of PTTH.

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“…Subsequent cell proliferation and functional differentiation of accessory glands require Drosophila homeodomain transcription factor prd [24], homeodomain transcriptional repressor defective proventriculus ( dve ) [31] and Hox gene Abdominal-B (Abd-B) [29]. In the present study, depletion of EcR in a prd -GAL4 dependent manner resulted in defective accessory glands that also lacked detectable Abd-B.…”

Section: Resultsmentioning

confidence: 78%

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

et al. 2017

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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.

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The Homeodomain Protein Defective Proventriculus Is Essential for Male Accessory Gland Development to Enhance Fecundity in Drosophila

Cited by 36 publications

References 44 publications

A Novel Function for the Hox Gene Abd-B in the Male Accessory Gland Regulates the Long-Term Female Post-Mating Response in Drosophila

A Novel Function for the Hox Gene Abd-B in the Male Accessory Gland Regulates the Long-Term Female Post-Mating Response in Drosophila

Accessory Gland as a Site for Prothoracicotropic Hormone Controlled Ecdysone Synthesis in Adult Male Insects

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

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