Proteomics

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


ABSTRACT: Seminal fluid proteins (SFPs) exert potent effects on male and female fitness. These rapidly evolving and molecularly diverse proteins derive from multiple male secretory cells and tissues. In Drosophila melanogaster most SFPs are produced in the accessory glands, which are composed of ~1000 fertility-enhancing ‘main cells’ and ~40, more functionally cryptic, ‘secondary cells’. Previous work shows that inhibition of BMP-signalling in secondary cells suppresses secretion, leading to a surprising uncoupling of normal female post-mating responses: refractoriness stimulation is impaired, but offspring production is not. Secondary cell secretions might therefore make a highly specific contribution to the seminal proteome and ejaculate function; alternatively, they might play a more global – but hitherto-undiscovered – role in regulating SFPs and their interconnected functions. Here, we present data that supports the latter model. We show that in addition to previously reported phenotypes, secondary cell-specific BMP-inhibition compromises sperm storage and increases female sperm use efficiency. Moreover, it alters sperm competition: second male sperm enter storage more slowly, ejaculates are ejected later, and first male paternity share improves. This result suggests a novel constraint on ejaculate evolution whereby female refractoriness and sperm competitiveness cannot be simultaneously maximised. 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.

INSTRUMENT(S): Q Exactive

ORGANISM(S): Drosophila Melanogaster (fruit Fly)

TISSUE(S): Accessory Sex Gland

SUBMITTER: Philip Charles  

LAB HEAD: Stuart Wigby

PROVIDER: PXD015253 | Pride | 2020-05-26

REPOSITORIES: Pride

Dataset's files

Source:
Action DRS
BenHopkins_progenesis_mgf.mgf Mgf
BenHopkins_progenesis_mgf.pride.mgf.gz Mgf
F282551.mzid.gz Mzid
F282551.pride.mztab.gz Mztab
QE838_MSQ1154_20171005_BenHopkins_S1.raw Raw
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Publications

BMP signaling inhibition in <i>Drosophila</i> secondary cells remodels the seminal proteome and self and rival ejaculate functions.

Hopkins Ben R BR   Sepil Irem I   Bonham Sarah S   Miller Thomas T   Charles Philip D PD   Fischer Roman R   Kessler Benedikt M BM   Wilson Clive C   Wigby Stuart S  

Proceedings of the National Academy of Sciences of the United States of America 20191118 49


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 <i>Drosophila melanogaster</i>, 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 unc  ...[more]

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