Cleavage of the Drosophila seminal protein Acp36DE in mated females enhances its sperm storage activity

Avila, Frank W.; Wolfner, Mariana F.

doi:10.1016/j.jinsphys.2017.06.015

Cited by 35 publications

(34 citation statements)

References 40 publications

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“…Reduced sperm storage in Dad - mated females may instead be a consequence of loss of secondary-cell–derived exosomes, the prostate-derived equivalent of which in mammals are known to fuse with sperm and stimulate motility (37). Reduced storage could also arise if secondary-cell BMP signaling inhibition affected SFPs such as the main-cell–produced Acp36DE and/or its associated cofactors, which are known to collectively promote sperm storage (38–42).…”

Section: Resultsmentioning

confidence: 99%

BMP signaling inhibition in Drosophila secondary cells remodels the seminal proteome and self and rival ejaculate functions

Hopkins

Sepil

Bonham

et al. 2019

Proc. Natl. Acad. Sci. U.S.A.

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Seminal fluid proteins (SFPs) exert potent effects on male and female fitness. Rapidly evolving and molecularly diverse, they derive from multiple male secretory cells and tissues. In Drosophila melanogaster, most SFPs are produced in the accessory glands, which are composed of ∼1,000 fertility-enhancing “main cells” and ∼40 more functionally cryptic “secondary cells.” Inhibition of bone morphogenetic protein (BMP) signaling in secondary cells suppresses secretion, leading to a unique uncoupling of normal female postmating responses to the ejaculate: refractoriness stimulation is impaired, but offspring production is not. Secondary-cell secretions might therefore make highly specific contributions to the seminal proteome and ejaculate function; alternatively, they might regulate more global—but hitherto undiscovered—SFP functions and proteome composition. Here, we present data that support the latter model. We show that in addition to previously reported phenotypes, secondary-cell-specific BMP signaling inhibition compromises sperm storage and increases female sperm use efficiency. It also impacts second male sperm, tending to slow entry into storage and delay ejection. First male paternity is enhanced, which suggests a constraint on ejaculate evolution whereby high female refractoriness and sperm competitiveness are mutually exclusive. Using quantitative proteomics, we reveal changes to the seminal proteome that surprisingly encompass alterations to main-cell–derived proteins, indicating important cross-talk between classes of SFP-secreting cells. Our results demonstrate that ejaculate composition and function emerge from the integrated action of multiple secretory cell types, suggesting that modification to the cellular make-up of seminal-fluid-producing tissues is an important factor in ejaculate evolution.

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Section: Resultsmentioning

confidence: 99%

BMP signaling inhibition in Drosophila secondary cells remodels the seminal proteome and self and rival ejaculate functions

Hopkins

Sepil

Bonham

et al. 2019

Proc. Natl. Acad. Sci. U.S.A.

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show abstract

“…Superficially, they resemble the sclerotized capsule of the spermathecae, but their distinct fluorescence pattern suggests compositional differences. Their presence in virgin females discounts a number of mechanisms through which they might form: sexually transmitted pathogens, localized immune responses to mating, or via male-derived seminal products, some of which enter into the storage organs [22][23][24][25][26]. The variation we detect across SDPs in terms of their size and localization may be due to genetic variation or represent different points in SDP development.…”

Section: Discussionmentioning

confidence: 76%

Structural variation in Drosophila melanogaster spermathecal ducts and its association with sperm competition dynamics

2020

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The ability of female insects to retain and use sperm for days, months, or even years after mating requires specialized storage organs in the reproductive tract. In most orders, these organs include a pair of sclerotized capsules known as spermathecae. Here, we report that some Drosophila melanogaster females exhibit previously uncharacterized structures within the distal portion of the muscular duct that links a spermatheca to the uterus. We find that these ‘spermathecal duct presences' (SDPs) may form in either or both ducts and can extend from the duct into the sperm-storing capsule itself. We further find that the incidence of SDPs varies significantly between genotypes, but does not change significantly with the age or mating status of females, the latter indicating that SDPs are not composed of or stimulated by sperm or male seminal proteins. We show that SDPs affect neither the number of first male sperm held in a spermatheca nor the number of offspring produced after a single mating. However, we find evidence that SDPs are associated with a lack of second male sperm in the spermathecae after females remate. This raises the possibility that SDPs provide a mechanism for variation in sperm competition outcome among females.

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“…Reduced sperm storage in Dad-mated females may instead be a consequence of loss of secondary-cell-derived exosomes, the prostate-derived equivalent of which in mammals are known to fuse with sperm and stimulate motility (34). Reduced storage could also arise if secondary cell BMP-signalling inhibition affected SFPs, such as the main cell-produced Acp36DE and/or its associated co-factors, which are known to collectively promote sperm storage (35–39).…”

Section: Resultsmentioning

confidence: 99%

BMP-signalling inhibition inDrosophilasecondary cells remodels the seminal proteome, and self and rival ejaculate functions

Hopkins

Sepil

Bonham

et al. 2019

Preprint

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51Seminal fluid proteins (SFPs) exert potent effects on male and female fitness. Rapidly evolving 52 and molecularly diverse, they derive from multiple male secretory cells and tissues. In 53 Drosophila melanogaster, most SFPs are produced in the accessory glands, which are 54 composed of ~1000 fertility-enhancing 'main cells' and ~40, more functionally cryptic, 55 'secondary cells'. Inhibition of BMP-signalling in secondary cells suppresses secretion, 56 leading to a unique uncoupling of normal female post-mating responses to the ejaculate: 57 refractoriness stimulation is impaired, but offspring production is not. Secondary cell 58 secretions might therefore make a highly specific contribution to the seminal proteome and 59 ejaculate function; alternatively, they might regulate more global -but hitherto-undiscovered 60 -SFP functions and proteome composition. Here, we present data that supports the latter 61 model. We show that in addition to previously reported phenotypes, secondary cell-specific 62 BMP-signalling inhibition compromises sperm storage and increases female sperm use 63 efficiency. It also impacts second male sperm, tending to slow entry into storage and delay 64 ejection. First male paternity is enhanced, which suggests a novel constraint on ejaculate 65 evolution whereby high female refractoriness and sperm competitiveness are mutually 66 exclusive. Using quantitative proteomics, we reveal a mix of specific and widespread changes 67 to the seminal proteome that surprisingly encompass alterations to main cell-derived proteins, 68indicating important cross-talk between classes of SFP-secreting cells. Our results demonstrate 69 that ejaculate composition and function emerge from the integrated action of multiple secretory 70 cell-types suggesting that modification to the cellular make-up of seminal fluid-producing 71 tissues is an important factor in ejaculate evolution. 72 73 74 75 76

show abstract

Cleavage of the Drosophila seminal protein Acp36DE in mated females enhances its sperm storage activity

Cited by 35 publications

References 40 publications

BMP signaling inhibition in Drosophila secondary cells remodels the seminal proteome and self and rival ejaculate functions

BMP signaling inhibition in Drosophila secondary cells remodels the seminal proteome and self and rival ejaculate functions

Structural variation in Drosophila melanogaster spermathecal ducts and its association with sperm competition dynamics

BMP-signalling inhibition inDrosophilasecondary cells remodels the seminal proteome, and self and rival ejaculate functions

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