Functional impact of silencing the <i>Helicoverpa armigera</i> sex‐peptide receptor on female reproductive behaviour

Hanin, Orly; Azrielli, A.; Applebaum, Shalom W.; Rafaeli, Ada

doi:10.1111/j.1365-2583.2011.01122.x

Cited by 31 publications

(33 citation statements)

References 34 publications

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“…Whether this occurs at the level of signalling, however, is not clear as the delay in the response could require higher amounts of SP to compensate for its degradation in the haemolymph. A puzzling discovery has been that SPR can bind MIPs in Drosophila and activate the receptor in cell culture, but injection of MIPs neither induces the SP response nor do MIPs act antagonistically to inhibit the SP response [19,40]. SPR is evolutionarily well conserved and functions in other insects also with ligands seemingly different from SP [19,40].…”

Section: Discussionmentioning

confidence: 99%

Multiple pathways mediate the sex-peptide-regulated switch in female Drosophila reproductive behaviours

et al. 2013

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Male-derived sex-peptide (SP) induces profound changes in the behaviour of Drosophila females, resulting in decreased receptivity to further mating and increased egg laying. SP can mediate the switch in female reproductive behaviours via a G protein-coupled receptor, SPR, in neurons expressing fruitless, doublesex and pickpocket. Whether SPR is the sole receptor and whether SP induces the postmating switch in a single pathway has not, to our knowledge been tested. Here we report that the SP response can be induced in the absence of SPR when SP is ectopically expressed in neurons or when SP, transferred by mating, can access neurons through a leaky blood brain barrier. Membrane-tethered SP can induce oviposition via doublesex, but not fruitless and pickpocket neurons in SPR mutant females. Although pickpocket and doublesex neurons rely on G(o) signalling to reduce receptivity and induce oviposition, G(o) signalling in fruitless neurons is required only to induce oviposition, but not to reduce receptivity. Our results show that SP's action in reducing receptivity and inducing oviposition can be separated in fruitless and doublesex neurons. Hence, the SP-induced postmating switch incorporates shared, but also distinct circuitry of fruitless, doublesex and pickpocket neurons and additional receptors.

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Section: Discussionmentioning

confidence: 99%

Multiple pathways mediate the sex-peptide-regulated switch in female Drosophila reproductive behaviours

et al. 2013

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“…The melSP-induced PMR in the moth appeared to be mediated by HaeSP-R, the moth ortholog of SPR (Hanin et al 2012). There is an SP-like peptide in the male accessory glands (Hanin et al 2011).…”

Section: Evolutionary Aspects Of Sp/spr-mediated Pmrmentioning

confidence: 99%

“…Heliconverpa armigera, such as inhibition of pheromone production, suppression of calling behavior, and a reduction of PBAN-receptor gene expression (Hanin et al 2012). The melSP-induced PMR in the moth appeared to be mediated by HaeSP-R, the moth ortholog of SPR (Hanin et al 2012).…”

Section: Evolutionary Aspects Of Sp/spr-mediated Pmrmentioning

confidence: 99%

“…Mutant females deleted for SPR do not respond to mating, accept repeated mating, and maintain a low level of oviposition (Yapici et al 2008). It has been demonstrated that SPR expression in a limited number of pickpocket-expressing neurons in the female common oviduct was sufficient to rescue the mutant phenotype, suggesting that these neurons are targeted by SP (Yang et al 2009;Hanin et al 2012). Interestingly, neuronally expressed SP reduced receptivity and increased oviposition in the absence of SPR, suggesting an additional pathway capable of inducing PMR (Haussmann et al 2013).…”

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confidence: 99%

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Visualizing Molecular Functions and Cross-Species Activity of Sex-Peptide in Drosophila

et al. 2015

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The Drosophila melanogaster sex-peptide (melSP) is a seminal fluid component that induces postmating responses (PMR) of females via the sex-peptide receptor (SPR) . Although SP orthologs are found in many Drosophila species, their functions remain poorly characterized. It is unknown whether SP functions are conserved across species or rather specific to each species. Here, we developed a GFP-tagged melSP (G-SP) and used it to visualize cross-species binding activity to the female reproductive system of various species. First we demonstrated that ectopically expressed G-SP induced PMR in D. melanogaster females and bound to the female reproductive system, most notably to the common oviduct. No binding occurred in the females lacking SPR, indicating that G-SP binding was dependent on SPR. Next we tested whether G-SP binds to the common oviducts from 11 Drosophila species using dissected reproductive tracts. The binding was observed in six species belonging to the D. melanogaster species group, but not to those outside the group. Injection of melSP reduced the receptivity of females belonging to the D. melanogaster species group, but not of those outside the group, being consistent with the ability to bind G-SP. Thus the SP-mediated PMR appears to be limited to this species group. SPR was expressed in the oviducts at high levels in this group; therefore, we speculate that an enhanced expression of SPR in the oviduct was critical to establish the SP-mediated PMR during evolution.KEYWORDS sex-peptide; SP receptor; GFP-tag; postmating response T HE mating behavior and physiology of Drosophila melanogaster females are dramatically modified after copulation: they reject courting males by extruding their ovipositor, a behavior not seen in virgin females and start to lay many eggs (Kubli 1992). Sex-peptide (SP), a seminal fluid peptide, has been shown to play a major role in eliciting postmating response (PMR). Injection of SP into the abdominal cavity of virgin females reduces receptivity and stimulates oviposition (Chen et al. 1988) and these phenotypes can be induced by ectopic expression of SP in virgin females (Aigaki et al. 1991). Furthermore, experiments involving an SP null mutant generated by gene targeting and dsRNAi-mediated gene knockdown unambiguously demonstrated that SP is a major component in inducing changes in receptivity, ovulation, and oviposition in mated females (Liu and Kubli 2003;Chapman et al. 2003). In addition, SP stimulates food intake (Hanin et al. 2011) and activates immune response genes (Peng et al. 2005b).An extensive transgenic RNAi screen identified a receptor for sex-peptide (SPR), a G-protein-coupled receptor broadly expressed in the female reproductive tracts and in some neural tissues (Yapici et al. 2008). Mutant females deleted for SPR do not respond to mating, accept repeated mating, and maintain a low level of oviposition (Yapici et al. 2008). It has been demonstrated that SPR expression in a limited number of pickpocket-expressing neurons in the female common oviduct was...

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“…SPR is a G-protein-coupled receptor, and its activity in a set of reproductive tract neurons in the female is necessary for sex peptide (SP), a 36-amino-acid peptide with diverse phenotypic effects (Chen et al 1988; Kubli 2003), to suppress receptivity through activation of SPR (Hasemeyer et al 2009; Yang et al 2009). The ortholog of SPR in Helicoverpa armigera is also essential for female postmating responses such as pheromone production (Fan et al 1999; Hanin et al 2012). Recent studies suggest that there may be additional receptors for SP, and that SPR may facilitate access of SP to the nervous system (Ja et al 2009; Haussmann et al 2013).…”

Section: Do Sfps Contribute To Postmating Sexual Conflict?mentioning

confidence: 99%

Sexual Conflict and Seminal Fluid Proteins: A Dynamic Landscape of Sexual Interactions

Sirot

Wong

Chapman

et al. 2014

Cold Spring Harb Perspect Biol

156

221

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Sexual reproduction requires coordinated contributions from both sexes to proceed efficiently. However, the reproductive strategies that the sexes adopt often have the potential to give rise to sexual conflict because they can result in divergent, sex-specific costs and benefits. These conflicts can occur at many levels, from molecular to behavioral. Here, we consider sexual conflict mediated through the actions of seminal fluid proteins. These proteins provide many excellent examples in which to trace the operation of sexual conflict from molecules through to behavior. Seminal fluid proteins are made by males and provided to females during mating. As agents that can modulate egg production at several steps, as well as reproductive behavior, sperm “management,” and female feeding, activity, and longevity, the actions of seminal proteins are prime targets for sexual conflict. We review these actions in the context of sexual conflict. We discuss genomic signatures in seminal protein (and related) genes that are consistent with current or previous sexual conflict. Finally, we note promising areas for future study and highlight real-world practical situations that will benefit from understanding the nature of sexual conflicts mediated by seminal proteins.

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Functional impact of silencing the Helicoverpa armigera sex‐peptide receptor on female reproductive behaviour

Cited by 31 publications

References 34 publications

Multiple pathways mediate the sex-peptide-regulated switch in female Drosophila reproductive behaviours

Multiple pathways mediate the sex-peptide-regulated switch in female Drosophila reproductive behaviours

Visualizing Molecular Functions and Cross-Species Activity of Sex-Peptide in Drosophila

Sexual Conflict and Seminal Fluid Proteins: A Dynamic Landscape of Sexual Interactions

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