Functional Diversity and Evolution of the Drosophila Sperm Proteome

Garlovsky, Martin D.; Sandler, Jessica; Karr, Timothy L.

doi:10.1016/j.mcpro.2022.100281

Cited by 15 publications

(18 citation statements)

References 69 publications

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“…The protein abundances followed a normal distribution ( Figure S4 ) and were found to be strongly correlated between the biological triplicates (Pearson’s correlation = 0.94 – 0.99) ( Figure S5 ). To further assess the reliability of our data, we compared the unstressed (N 1 and N 4 ) sperm proteomes of w m4H with the recently reported D. melanogaster sperm proteome 3 (DmSP3) (27, 28, 46). The comparison was carried out using the total proteins identified across the biological triplicates of N 1 and N 4 .…”

Section: Resultsmentioning

confidence: 99%

“…Sperm cells have long been thought to be translationally silent. However, with advancements in proteomics approaches, sperms in various organisms such as Drosophila (46,47) and humans (48) are now well-established to contain numerous ribosomal proteins (RPs). In Drosophila, for instance, 83 RPs have been identified in DmSP3 (46) and 72 by McCullough et al (47) out of 169 annotated so far (Flybase.org).…”

Section: Discussionmentioning

confidence: 99%

“…The degree of histone retention, however, is still unclear in Drosophila sperm chromatin. Though undetectable by immunofluorescence (29), there are indications of the presence of histones in Drosophila sperms from proteomics and chromatin immunoprecipitation-on-chip (ChIP-on-Chip) studies (46, 72). Notably, we observed downregulation of histone proteins in H 3 N 1 and H 4 , mainly canonical histone H2A and histone H2B, histone 3 variant H3.3, and histone 4 replacement H4r ( Figure 4 and Table S9 ), which were associated with GO terms ‘DNA-templated transcription-initiation’ and ‘chromatin organization’.…”

Section: Discussionmentioning

confidence: 99%

“…Collectively, these findings suggest a role of chromatin-based mechanisms in the MEI of heat stress memory in Drosophila via the male germline. While we have been able to capture certain chromatin-associated nuclear proteins, which are affected by heat stress, the sperm nuclear proteome is expected to be much more complex (81), and only improved proteomics approaches (46) or establishing nuclei purification protocols can provide a more detailed molecular insight.…”

Section: Discussionmentioning

confidence: 99%

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Multigenerational effect of heat stress on theDrosophila melanogastersperm proteome

Khan

Mishra

2022

Preprint

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The notion that genes are the sole units of heredity and that a barrier exists between soma and germline has been a major hurdle in elucidating the heritability of traits that were observed to follow a non-Mendelian inheritance pattern. It was only after the conception of epigenetics by Conrad Waddington that the effect of parental environment on subsequent generations via non-DNA sequence-based mechanisms, such as DNA methylation, chromatin modifications, non-coding RNAs and proteins, could be established, now referred to as multigenerational epigenetic inheritance. Despite growing evidence, the male gamete-derived epigenetic factors that mediate the transmission of such phenotypes are seldom explored, particularly in the model organismDrosophila melanogaster. Using the heat stress-induced multigenerational epigenetic inheritance paradigm in a widely used position-effect variegation line ofDrosophila, namedwhite-mottled, we have dissected the effect of heat stress on the sperm proteome in the current study. We demonstrate that multiple successive generations of heat stress at the early embryonic stage results in a significant downregulation of proteins associated with a diverse set of functions, such as translation, chromatin organization, microtubule-based processes, and generation of metabolites and energy, in the sperms. Based on our findings, we propose chromatin-based epigenetic mechanisms, a well-established mechanism for multigenerational effects, as a plausible way of transmitting heat stress memory via the male germline in this case. Moreover, we show that despite these heat stress-induced changes, the life-history traits, such as reproductive fitness and stress tolerance of the subsequent generations, are unaffected, probing the evolutionary relevance of multigenerational epigenetic effects.

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Section: Resultsmentioning

confidence: 99%

Section: Discussionmentioning

confidence: 99%

Section: Discussionmentioning

confidence: 99%

Section: Discussionmentioning

confidence: 99%

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Multigenerational effect of heat stress on theDrosophila melanogastersperm proteome

Khan

Mishra

2022

Preprint

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“…Functional categories of proteins that are associated with sexual reproduction, flagellar movement and metabolic processes, e.g. mitochondria-related ATP production, are enriched in spermatozoa across a wide range of vertebrate and invertebrate taxa (Bayram et al 2016, Whittington et al 2017, 2019, Rowe et al 2019, Garlovsky et al 2022, Poignet et al 2022). Moreover, the analysis of the whole seminal fluid proteome revealed that the fluids dataset is dominated by the ATP metabolic process (GO:0046034), which is linked to activated proteins (Fig.…”

Section: Functional Divergence Of Proteomesmentioning

confidence: 99%

Comparative sperm proteomics in selected passerine birds reflects sperm morphology and mitochondrial metabolism

Otčenášková,

Stopková,

Zemanová

et al. 2023

Journal of Vertebrate Biology

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Proteomic diversification of spermatostyles among six species of whirligig beetles

Gomez,

Dallai,

Sims‐West

et al. 2024

Molecular Reproduction Devel

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Seminal fluid protein composition is complex and commonly assumed to be rapidly divergent due to functional interactions with both sperm and the female reproductive tract (FRT), both of which evolve rapidly. In addition to sperm, seminal fluid may contain structures, such as mating plugs and spermatophores. Here, we investigate the evolutionary diversification of a lesser‐known ejaculate structure: the spermatostyle, which has independently arisen in several families of beetles and true bugs. We characterized the spermatostyle proteome, in addition to spermatostyle and FRT morphology, in six species of whirligig beetles (family Gyrinidae). Spermatostyles were enriched for proteolytic enzymes, and assays confirmed they possess proteolytic activity. Sperm‐leucylaminopeptidases (S‐LAPs) were particularly abundant, and their localization to spermatostyles was confirmed by immunohistochemistry. Although there was evidence for functional conservation of spermatostyle proteomes across species, phylogenetic regressions suggest evolutionary covariation between protein composition and the morphology of both spermatostyles and FRTs. We postulate that S‐LAPs (and other proteases) have evolved a novel structural role in spermatostyles and discuss spermatostyles as adaptations for delivering male‐derived materials to females.

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Functional Diversity and Evolution of the Drosophila Sperm Proteome

Cited by 15 publications

References 69 publications

Multigenerational effect of heat stress on theDrosophila melanogastersperm proteome

Multigenerational effect of heat stress on theDrosophila melanogastersperm proteome

Comparative sperm proteomics in selected passerine birds reflects sperm morphology and mitochondrial metabolism

Proteomic diversification of spermatostyles among six species of whirligig beetles

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