Seminal fluid proteins induce transcriptome changes in the Aedes aegypti female lower reproductive tract

Abstract Background Mating induces behavioral and physiological changes in the arbovirus vector Aedes aegypti, including stimulation of egg development and oviposition, increased survival, and reluctance to re-mate with subsequent males. Transferred seminal fluid proteins and peptides derived from the male accessory glands induce these changes, though the mechanism by which they do this is not known. Results To determine transcriptome changes induced by seminal proteins, we injected extract from male accessory glands and seminal vesicles (MAG extract) into females and examined female lower reproductive tract (LRT) transcriptomes 24 h later, relative to non-injected controls. MAG extract induced 87 transcript-level changes, 31 of which were also seen in a previous study of the LRT 24 h after a natural mating, including 15 genes with transcript-level changes similarly observed in the spermathecae of mated females. The differentially-regulated genes are involved in diverse molecular processes, including immunity, proteolysis, neuronal function, transcription control, or contain predicted small-molecule binding and transport domains. Conclusions Our results reveal that seminal fluid proteins, specifically, can induce gene expression responses after mating and identify gene targets to further investigate for roles in post-mating responses and potential use in vector control.

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Proteomic analysis of Drosophila mojavensis male accessory glands suggests novel classes of seminal fluid proteins

Insect Biochemistry and Molecular Biology ◽

10.1016/j.ibmb.2009.03.003 ◽

2009 ◽

Vol 39 (5-6) ◽

pp. 366-371 ◽

Cited By ~ 39

Author(s):

Erin S. Kelleher ◽

Thomas D. Watts ◽

Brooke A. LaFlamme ◽

Paul A. Haynes ◽

Therese A. Markow

Keyword(s):

Proteomic Analysis ◽

Seminal Fluid ◽

Drosophila Mojavensis ◽

Seminal Fluid Proteins ◽

Male Accessory Glands ◽

Accessory Glands

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Reproductive functions and genetic architecture of the seminal fluid and sperm proteomes of the mosquito Aedes aegypti

10.1101/405431 ◽

2018 ◽

Cited By ~ 2

Author(s):

Ethan C. Degner ◽

Yasir H. Ahmed-Braimah ◽

Kiril Borziak ◽

Mariana F. Wolfner ◽

Laura C. Harrington ◽

...

Keyword(s):

Aedes Aegypti ◽

Seminal Fluid ◽

Protein Translation ◽

Chromosome 1 ◽

Composition Analysis ◽

Seminal Fluid Proteins ◽

Accessory Glands ◽

Significant Enrichment ◽

Intimate Knowledge ◽

Reproductive Processes

AbstractThe yellow fever mosquito, Aedes aegypti, transmits several viruses, including dengue, Zika, and chikungunya. Some proposed efforts to control this vector involve manipulating reproduction to suppress wild populations or replacing them with disease-resistant mosquitoes. The design of such strategies requires an intimate knowledge of reproductive processes, yet our basic understanding of reproductive genetics in this vector remains largely incomplete. To accelerate future investigations, we have comprehensively catalogued sperm and seminal fluid proteins (SFPs) transferred to females in the ejaculate using tandem mass spectrometry. By excluding female-derived proteins using an isotopic labelling approach, we identified 870 sperm proteins and 280 seminal fluid proteins. Functional composition analysis revealed parallels with known aspects of sperm biology and SFP function in other insects. To corroborate our proteome characterization, we also generated transcriptomes for testes and the male accessory glands—the primary contributors to Ae. aegypti sperm and seminal fluid, respectively. Differential gene expression of accessory glands from virgin and mated males suggests that protein translation is upregulated post-mating. Several SFP transcripts were also modulated after mating, but >90% remained unchanged. Finally, a significant enrichment of SFPs was observed on chromosome 1, which harbors the male sex determining locus in this species. Our study provides a comprehensive proteomic and transcriptomic characterization of ejaculate production and composition and thus provides a foundation for future investigations of Ae. aegypti reproductive biology, from functional analysis of individual proteins to broader examination of reproductive processes.

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The Drosophila melanogaster X-Linked mfs(1)6E Locus Is Required for Production of Normal Seminal Fluid by the Male Accessory Glands

Experimental Cell Research ◽

10.1006/excr.2001.5246 ◽

2001 ◽

Vol 267 (1) ◽

pp. 1-12 ◽

Cited By ~ 2

Author(s):

Pedro P. López ◽

Juán F. Santarén ◽

M.Fernanda Ruiz ◽

Pedro Esponda ◽

Lucas Sánchez

Keyword(s):

Drosophila Melanogaster ◽

Seminal Fluid ◽

Male Accessory Glands ◽

Accessory Glands

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Differences in Postmating Transcriptional Responses between Conspecific and Heterospecific Matings in Drosophila

Molecular Biology and Evolution ◽

10.1093/molbev/msaa264 ◽

2020 ◽

Author(s):

Yasir H Ahmed-Braimah ◽

Mariana F Wolfner ◽

Andrew G Clark

Keyword(s):

Reproductive Tract ◽

Evolutionary Dynamics ◽

Seminal Fluid ◽

Female Reproductive Tract ◽

Additional Stress ◽

Reproductive Proteins ◽

Transcriptional Responses ◽

Seminal Fluid Proteins ◽

Reproductive Genes ◽

Imd Pathway

Abstract In many animal species, females undergo physiological and behavioral changes after mating. Some of these changes are driven by male-derived seminal fluid proteins and are critical for fertilization success. Unfortunately, our understanding of the molecular interplay between female and male reproductive proteins remains inadequate. Here, we analyze the postmating response in a Drosophila species that has evolved strong gametic incompatibility with its sister species; Drosophila novamexicana females produce only ∼1% fertilized eggs in crosses with Drosophila americana males, compared to ∼98% produced in within-species crosses. This incompatibility is likely caused by mismatched male and female reproductive molecules. In this study, we use short-read RNA sequencing to examine the evolutionary dynamics of female reproductive genes and the postmating transcriptome response in crosses within and between species. First, we found that most female reproductive tract genes are slow-evolving compared to the genome average. Second, postmating responses in con- and heterospecific matings are largely congruent, but heterospecific matings induce expression of additional stress-response genes. Some of those are immunity genes that are activated by the Imd pathway. We also identify several genes in the JAK/STAT signaling pathway that are induced in heterospecific, but not conspecific mating. While this immune response was most pronounced in the female reproductive tract, we also detect it in the female head and ovaries. These results show that the female’s postmating transcriptome-level response is determined in part by the genotype of the male, and that divergence in male reproductive genes and/or traits can have immunogenic effects on females.

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Inhibition of Male Accessory Glands of Aedes aegypti by Larval Treatment with Apholate12

Journal of Economic Entomology ◽

10.1093/jee/63.3.745 ◽

1970 ◽

Vol 63 (3) ◽

pp. 745-748 ◽

Cited By ~ 4

Author(s):

Jeffrey R. Powell ◽

George B. Graig

Keyword(s):

Aedes Aegypti ◽

Male Accessory Glands ◽

Accessory Glands

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Differences in post-mating transcriptional responses between conspecific and heterospecific matings in Drosophila

10.1101/2020.03.25.009068 ◽

2020 ◽

Cited By ~ 1

Author(s):

Yasir H. Ahmed-Braimah ◽

Mariana F. Wolfner ◽

Andrew G. Clark

Keyword(s):

Reproductive Tract ◽

Evolutionary Dynamics ◽

Seminal Fluid ◽

Female Reproductive Tract ◽

Additional Stress ◽

Reproductive Proteins ◽

Transcriptional Responses ◽

Seminal Fluid Proteins ◽

Reproductive Genes ◽

Imd Pathway

AbstractIn many animal species, females undergo physiological and behavioral changes after mating. Some of these changes are driven by male-derived seminal fluid proteins, and are critical for fertilization success. Unfortunately, our understanding of the molecular interplay between female and male reproductive proteins remains superficial. Here we analyze the post-mating response in a Drosophila species that has evolved strong gametic incompatibility with its sister species; D. novamexicana females produce only 1% fertilized eggs in crosses with D. americana males, compared to ~98% produced in within-species crosses. This incompatibility is likely caused by mismatched male and female reproductive molecules. In this study we use short-read RNA sequencing to examine the evolutionary dynamics of female reproductive genes and the post-mating transcriptome response in crosses within and between species. First, we found that most female reproductive tract genes are slow-evolving compared to the genome average. Second, post-mating responses in con- and heterospecific matings are largely congruent, but heterospecific mating induces expression of additional stress-response genes. Some of those are immunity genes that are activated by the Imd pathway. We also identify several genes in the JAK/STAT signaling pathway that are induced in heterospecific, but not conspecific mating. While this immune response was most pronounced in the female reproductive tract, we also detect it in the female head and ovaries. Our results show that the female’s post-mating transcriptome-level response is determined in part by the genotype of the male, and that divergence in male reproductive genes and/or traits can have immunogenic effects on females.

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BMP-regulated exosomes from Drosophila male reproductive glands reprogram female behavior

The Journal of Cell Biology ◽

10.1083/jcb.201401072 ◽

2014 ◽

Vol 206 (5) ◽

pp. 671-688 ◽

Cited By ~ 71

Author(s):

Laura Corrigan ◽

Siamak Redhai ◽

Aaron Leiblich ◽

Shih-Jung Fan ◽

Sumeth M.W. Perera ◽

...

Keyword(s):

Reproductive Tract ◽

Seminal Fluid ◽

Bmp Signaling ◽

Female Reproductive Tract ◽

Female Behavior ◽

Accessory Glands ◽

Morphogenetic Protein ◽

Downstream Effectors ◽

Membrane Bound

Male reproductive glands secrete signals into seminal fluid to facilitate reproductive success. In Drosophila melanogaster, these signals are generated by a variety of seminal peptides, many produced by the accessory glands (AGs). One epithelial cell type in the adult male AGs, the secondary cell (SC), grows selectively in response to bone morphogenetic protein (BMP) signaling. This signaling is involved in blocking the rapid remating of mated females, which contributes to the reproductive advantage of the first male to mate. In this paper, we show that SCs secrete exosomes, membrane-bound vesicles generated inside late endosomal multivesicular bodies (MVBs). After mating, exosomes fuse with sperm (as also seen in vitro for human prostate-derived exosomes and sperm) and interact with female reproductive tract epithelia. Exosome release was required to inhibit female remating behavior, suggesting that exosomes are downstream effectors of BMP signaling. Indeed, when BMP signaling was reduced in SCs, vesicles were still formed in MVBs but not secreted as exosomes. These results demonstrate a new function for the MVB–exosome pathway in the reproductive tract that appears to be conserved across evolution.

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FUNCTIONS OF THE MALE ACCESSORY GLAND SECRETIONS OF AEDES MOSQUITOES (DIPTERA: CULICIDAE): TRANSPLANTATION STUDIES

The Canadian Entomologist ◽

10.4039/ent108955-9 ◽

1976 ◽

Vol 108 (9) ◽

pp. 955-960 ◽

Cited By ~ 23

Author(s):

S. Ramalingam ◽

G. B. Craig

Keyword(s):

Aedes Aegypti ◽

Secretory Granules ◽

Accessory Gland ◽

Anterior Region ◽

Male Accessory Gland ◽

Male Accessory Glands ◽

Accessory Glands ◽

Aedes Mosquitoes ◽

Species Specific

AbstractIn Aedes aegypti, the ’matrone’ substance which caused mating inhibition and stimulated oviposition in females, was present in the anterior secretory region of the male accessory glands. In the divided accessory glands of male A. triseriatus, however, it was present in the posterior glands. The posterior gland substance in A. triseriatus was not species specific. It stimulated oviposition in A. aegypti and caused mating inhibition in A. atropalpus. The secretory substance of the posteriormost region in the glands of both species of mosquitoes was mucin in nature. This mucin substance effectively glued the secretory granules of the anterior region(s).

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