Characterization of Female Reproductive Proteases in a Butterfly from Functional and Evolutionary Perspectives

Plakke, Melissa S; Walker, Jennifer L.; Lombardo, J; Goetz, Breanna J; Pacella, G; Durrant, Jacob D.; Clark, Nathan L.; Morehouse, Nathan I

doi:10.1086/705722

Cited by 14 publications

(18 citation statements)

References 70 publications

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“…The distinct characteristics of the FRT tissue and fluid proteomes were initially apparent in their 1D SDS PAGE banding patterns, which indicated that their protein composition was substantially different (Fig S1A S3). In contrast, fluid proteins were enriched for GO annotations associated with enzymatic break down of proteins (Fig1B; Table S3), which was consistent with previously described proteolytic activity in insect FRT fluid (9,10,12). The small number (n = 32) of fluid-only proteins were also enriched for the regulation of proteolytic activity, thus providing further support for the enzymatic activity in the FRT fluid (Table S3).…”

Section: Frt Tissue and Fluid Proteomes Have Distinct Characteristicssupporting

confidence: 86%

Pronounced Postmating Response in the Drosophila Female Reproductive Tract Fluid Proteome

McDonough-Goldstein

Whittington

McCullough

et al. 2021

Molecular & Cellular Proteomics

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Section: Frt Tissue and Fluid Proteomes Have Distinct Characteristicssupporting

confidence: 86%

Pronounced Postmating Response in the Drosophila Female Reproductive Tract Fluid Proteome

McDonough-Goldstein

Whittington

McCullough

et al. 2021

Molecular & Cellular Proteomics

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“…Proteases and peptidases are central to reproduction across taxa, regulating proteolytic activity and initiating cascades of interactions among downstream proteins (Bayram et al, 2017(Bayram et al, , 2019LaFlamme et al, 2012;LaFlamme & Wolfner, 2013;Plakke et al, 2015Plakke et al, , 2019.…”

Section: Discussionmentioning

confidence: 99%

“…Divergence in proteases has been implicated in PMPZ isolation between other insect species in both the male ejaculate and the female reproductive tract secretions (Al-Wathiqui et al, 2018;Kelleher & Pennington, 2009;Kelleher et al, 2007;Marshall et al, 2009Marshall et al, , 2011McCullough et al, 2020;Meslin et al, 2017;Plakke et al, 2019).…”

Section: Discussionmentioning

confidence: 99%

“…We identified a number of proteases and peptidases (or inhibitors) that were differentially abundant between populations. Proteases and peptidases are central to reproduction across taxa, regulating proteolytic activity and initiating cascades of interactions among downstream proteins (Bayram et al., 2017, 2019; LaFlamme et al., 2012; LaFlamme & Wolfner, 2013; Plakke et al., 2015, 2019). Divergence in proteases has been implicated in PMPZ isolation between other insect species in both the male ejaculate and the female reproductive tract secretions (Al‐Wathiqui et al., 2018; Kelleher & Pennington, 2009; Kelleher et al., 2007; Marshall et al., 2009, 2011; McCullough et al., 2020; Meslin et al., 2017; Plakke et al., 2019).…”

Section: Discussionmentioning

confidence: 99%

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Seminal fluid protein divergence among populations exhibiting postmating prezygotic reproductive isolation

et al. 2020

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Despite holding a central role in fertilization, reproductive traits often show elevated rates of evolution and diversification. The rapid evolution of seminal fluid proteins (Sfps) within populations is predicted to cause mis‐signalling between the male ejaculate and the female during and after mating resulting in postmating prezygotic (PMPZ) isolation between populations. Crosses between Drosophila montana populations show PMPZ isolation in the form of reduced fertilization success in both noncompetitive and competitive contexts. Here we test whether male ejaculate proteins produced in the accessory glands or ejaculatory bulb differ between populations using liquid chromatography tandem mass spectrometry. We find more than 150 differentially abundant proteins between populations that may contribute to PMPZ isolation, including a number of proteases, peptidases and several orthologues of Drosophila melanogaster Sfps known to mediate fertilization success. Males from the population that elicit the stronger PMPZ isolation after mating with foreign females typically produced greater quantities of Sfps. The accessory glands and ejaculatory bulb show enrichment for different gene ontology (GO) terms and the ejaculatory bulb contributes more differentially abundant proteins. Proteins with a predicted secretory signal evolve faster than nonsecretory proteins. Finally, we take advantage of quantitative proteomics data for three Drosophila species to determine shared and unique GO enrichments of Sfps between taxa and which potentially mediate PMPZ isolation. Our study provides the first high‐throughput quantitative proteomic evidence showing divergence of reproductive proteins between populations that exhibit PMPZ isolation.

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“…If reproductive proteins do indeed evolve more rapidly than other classes of protein, then perhaps they play an outsized role in the emergence of functional differences and reproductive isolating barriers between lineages. For example, evidence suggests post-mating prezygotic traits frequently evolve rapidly in animals (e.g., Galindo et al, 2003;Dorus et al, 2004;Plakke et al, 2019) and, when divergent between species, could contribute to reproductive isolation (Howard, 1999;Palumbi, 2009;Snook et al, 2009;Castillo and Moyle, 2014). Similarly, divergence in post-pollination prezygotic reproductive molecules could be important contributors to species barrier formation among angiosperms (Moyle et al, 2014).…”

Section: Consequences Of Rapid Protein Evolution For the Evolution Of Reproductive Differences And Speciationmentioning

confidence: 99%

Reproductive Proteins Evolve Faster Than Non-reproductive Proteins Among Solanum Species

Moyle

Gibson

2021

Front. Plant Sci.

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Elevated rates of evolution in reproductive proteins are commonly observed in animal species, and are thought to be driven by the action of sexual selection and sexual conflict acting specifically on reproductive traits. Whether similar patterns are broadly observed in other biological groups is equivocal. Here, we examine patterns of protein divergence among wild tomato species (Solanum section Lycopersicon), to understand forces shaping the evolution of reproductive genes in this diverse, rapidly evolving plant clade. By comparing rates of molecular evolution among loci expressed in reproductive and non-reproductive tissues, our aims were to test if: (a) reproductive-specific loci evolve more rapidly, on average, than non-reproductive loci; (b) ‘male’-specific loci evolve at different rates than ‘female’-specific loci; (c) genes expressed exclusively in gametophytic (haploid) tissue evolve differently from genes expressed in sporophytic (diploid) tissue or in both tissue types; and (d) mating system variation (a potential proxy for the expected strength of sexual selection and/or sexual conflict) affects patterns of protein evolution. We observed elevated evolutionary rates in reproductive proteins. However, this pattern was most evident for female- rather than male-specific loci, both broadly and for individual loci inferred to be positively selected. These elevated rates might be facilitated by greater tissue-specificity of reproductive proteins, as faster rates were also associated with more narrow expression domains. In contrast, we found little evidence that evolutionary rates are consistently different in loci experiencing haploid selection (gametophytic-exclusive loci), or in lineages with quantitatively different mating systems. Overall while reproductive protein evolution is generally elevated in this diverse plant group, some specific patterns of evolution are more complex than those reported in other (largely animal) systems, and include a more prominent role for female-specific loci among adaptively evolving genes.

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Characterization of Female Reproductive Proteases in a Butterfly from Functional and Evolutionary Perspectives

Cited by 14 publications

References 70 publications

Pronounced Postmating Response in the Drosophila Female Reproductive Tract Fluid Proteome

Pronounced Postmating Response in the Drosophila Female Reproductive Tract Fluid Proteome

Seminal fluid protein divergence among populations exhibiting postmating prezygotic reproductive isolation

Reproductive Proteins Evolve Faster Than Non-reproductive Proteins Among Solanum Species

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