Molecular evolutionary analysis of seminal receptacle sperm storage organ genes of <i>Drosophila melanogaster</i>

Prokupek, A. M.; Eyun, Seong‐il; Ko, Li; Moriyama, Etsuko N.; Harshman, Lawrence G.

doi:10.1111/j.1420-9101.2010.01998.x

Cited by 44 publications

(26 citation statements)

References 105 publications

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“…The differences in sperm release efficiency between the seminal receptacle and spermathecae may be due, in part, to chemical differences within the lumens of these organs. The two types of organ differ in the secretable proteins that they produce (Allen and Spradling 2008; Prokupek et al 2008Prokupek et al , 2010. Thus the sperm stored within them are likely to be exposed to different environments.…”

Section: Resultsmentioning

confidence: 99%

Sex Peptide Is Required for the Efficient Release of Stored Sperm in Mated Drosophila Females

et al. 2010

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The Drosophila seminal fluid protein (SFP) sex peptide (SP) elicits numerous post-mating responses, including increased egg laying and decreased sexual receptivity, in the mated female. Unlike other SFPs, which are detectable in mated females for only a few hours post mating, SP is maintained-and its effects are sustained-for several days. The persistence of SP in the mated female's reproductive tract is thought to be a consequence of its binding to, and gradual release from, sperm in storage, which maintains SP's ability to act within the female reproductive tract. Recent studies have shown that several other SFPs, acting in a network, are needed for SP's localization to sperm and are necessary for the efficient release of sperm from storage. This result suggested an additional new role for SP modulating the release of sperm from storage. We tested for this possibility by examining sperm storage parameters in mated females that did not receive SP. We found that while sperm accumulation into storage was unaffected, sperm depletion from storage sites was significantly decreased (or impaired) in the absence of SP. Mates of males expressing a modified SP that is unable to be released from sperm showed a similar phenotype, indicating that release of sperm-bound SP is a necessary component of normal sperm depletion. Additionally, SP null males were more successful in a sperm competitive environment when they were first to mate, which is likely a consequence of higher retention of their sperm due to defective sperm release. Our findings illustrate a direct role for SP in the release of sperm from storage.

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Section: Resultsmentioning

confidence: 99%

Sex Peptide Is Required for the Efficient Release of Stored Sperm in Mated Drosophila Females

et al. 2010

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“…These results suggest that Neps are important in both the CNS and the spermathecae for normal egg laying but not hatchability and that either a combination of both sources or an as-yet untested source of Nep expression may be responsible for the majority of the reduction in egg laying observed. One possible source of expression is the seminal receptacle, where Nep1 and Nep2 transcripts have both been detected (Prokupek et al 2010). However, we cannot test this, as currently no GAL4 drivers target only this organ.…”

Section: Characterization Of the Hatchability Defects In Nep2 Null Mumentioning

confidence: 97%

Neprilysins: An Evolutionarily Conserved Family of Metalloproteases That Play Important Roles in Reproduction in Drosophila

et al. 2014

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Members of the M13 class of metalloproteases have been implicated in diseases and in reproductive fitness. Nevertheless, their physiological role remains poorly understood. To obtain a tractable model with which to analyze this protein family's function, we characterized the gene family in Drosophila melanogaster and focused on reproductive phenotypes. The D. melanogaster genome contains 24 M13 class protease homologs, some of which are orthologs of human proteases, including neprilysin. Many are expressed in the reproductive tracts of either sex. Using RNAi we individually targeted the five Nep genes most closely related to vertebrate neprilysin, Nep1-5, to investigate their roles in reproduction. A reduction in Nep1, Nep2, or Nep4 expression in females reduced egg laying. Nep1 and Nep2 are required in the CNS and the spermathecae for wild-type fecundity. Females that are null for Nep2 also show defects as hosts of sperm competition as well as an increased rate of depletion for stored sperm. Furthermore, eggs laid by Nep2 mutant females are fertilized normally, but arrest early in embryonic development. In the male, only Nep1 was required to induce normal patterns of female egg laying. Reduction in the expression of Nep2-5 in the male did not cause any dramatic effects on reproductive fitness, which suggests that these genes are either nonessential for male fertility or perform redundant functions. Our results suggest that, consistent with the functions of neprilysins in mammals, these proteins are also required for reproduction in Drosophila, opening up this model system for further functional analysis of this protein class and their substrates. P ROTEASES play key roles in diverse physiological systems. One such family of metalloproteases, the M13 class of neutral endopeptidases, consists mainly of membranebound zinc proteases that are involved in the processing of neuropeptides and peptide hormones (reviewed in Turner et al. 2000;Turner et al. 2001;Bland et al. 2008). In mammals, seven members of this family have been identified, of which neprilysin (NEP) and endothelin converting enzyme (ECE) are the best studied. These proteins have been implicated in various diseases including cardiovascular disease (Segura and Ruilope 2011;Wick et al. 2011), Alzheimer's disease (Mulder et al. 2012;Klein et al. 2013), inflammation and inflammatory disorders (Wong et al. 2011), and cancer (Smollich et al. 2007;Maguer-Satta et al. 2011).In addition to their role in disease, NEPs are essential for development and reproduction in mammals. The mammalian Neprilysin-2, called NL1 in mice, is highly expressed in the testis. NL1-deficient males sire fewer pups, even though spermatogenesis appears to be unaffected (Carpentier et al. 2004). In females, NEP expression in the uterus is modulated by estrogen treatment in rats (Pinto et al. 1999) and during the estrogen/progesterone cycle in humans (Head et al. 1993). In female rats and mice, controlled degradation of tachykinins, particularly substance-P, by NEP in the uterus ...

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“…These mating-regulated genes may include some that are important for sperm competition. Similarly, genes expressed specifically in the female sperm storage organs (Allen and Spradling 2008;Prokupek et al 2008Prokupek et al , 2009Prokupek et al , 2010Schnakenberg et al 2011) might produce products that influence sperm competition.Many studies of the female role in sperm competition have focused on the female reproductive tract. A priori, a focus on the female reproductive tract makes sense because this is where sperm competition occurs.…”

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confidence: 99%

Large Neurological Component to Genetic Differences Underlying Biased Sperm Use in Drosophila

2013

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Sperm competition arises as a result of complex interactions among male and female factors. While the roles of some male factors are known, little is known of the molecules or mechanisms that underlie the female contribution to sperm competition. The genetic tools available for Drosophila allow us to identify, in an unbiased manner, candidate female genes that are critical for mediating sperm competition outcomes. We first screened for differences in female sperm storage and use patterns by characterizing the natural variation in sperm competition in a set of 39 lines from the sequenced Drosophila Genetic Reference Panel (DGRP) of wild-derived inbred lines. We found extensive female variation in sperm competition outcomes. To generate a list of candidate female genes for functional studies, we performed a genome-wide association mapping, utilizing the common single-nucleotide polymorphisms (SNPs) segregating in the DGRP lines. Surprisingly, SNPs within ion channel genes and other genes with roles in the nervous system were among the top associated SNPs. Knockdown studies of three candidate genes (para, Rab2, and Rim) in sensory neurons innervating the female reproductive tract indicate that some of these candidate female genes may affect sperm competition by modulating the neural input of these sensory neurons to the female reproductive tract. More extensive functional studies are needed to elucidate the exact role of all these candidate female genes in sperm competition. Nevertheless, the female nervous system appears to have a previously unappreciated role in sperm competition. Our results indicate that the study of female control of sperm competition should not be limited to female reproductive tract-specific genes, but should focus also on diverse biological pathways. I N many organisms, sperm competition is an important source of reproductive variation and is critical to the reproductive success of both males and females. Sperm competition occurs when a female mates with and stores sperm from multiple males. Multiple mating creates a situation in which the males' sperm "compete" for successful fertilizations. While the ultimate outcome of a sperm competition depends on a complex interaction between male and female factors, the sexes often have different interests. Males are essentially in competition with other males, and while natural selection drives males to become better competitors with each other, it may result in males damaging the female through toxicity of seminal proteins (Wigby and Chapman 2004;Mueller et al. 2007). On the other hand, females benefit from simply being able to produce the most and highest-fitness offspring, and this may entail a specific response to male-produced molecules that influence sperm competition. The sexual conflict that arises from these different evolutionary goals of males and females implies that the genetic response to selection on sperm competition may be totally distinct in males and females. It remains largely unknown what genes drive this sexual antagon...

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Molecular evolutionary analysis of seminal receptacle sperm storage organ genes of Drosophila melanogaster

Cited by 44 publications

References 105 publications

Sex Peptide Is Required for the Efficient Release of Stored Sperm in Mated Drosophila Females

Sex Peptide Is Required for the Efficient Release of Stored Sperm in Mated Drosophila Females

Neprilysins: An Evolutionarily Conserved Family of Metalloproteases That Play Important Roles in Reproduction in Drosophila

Large Neurological Component to Genetic Differences Underlying Biased Sperm Use in Drosophila

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