TY - JOUR
T1 - Functional Diversity and Evolution of the Drosophila Sperm Proteome
AU - Garlovsky, Martin D.
AU - Sandler, Jessica A.
AU - Karr, Timothy L.
N1 - Funding Information:
We thank Caitlin McDonough-Goldstein and Maria Vibranovski for helpful discussion, Alison Wright, Daniela Palmer, and Leeban Yusef for advice analyzing evolutionary rates. We are grateful to Eric Sedore and Larne Pekowsky who provided computing services (Syracuse University HTC Campus Grid), the authors whose data was used in this study, and the curators of FlyBase.org for continued maintenance of this essential resource. We are grateful to three anonymous reviewers who provided helpful feedback and comments on the article. This work was funded in part by the NSF award ACI-1341006, the Biodesign Institute and ASU Knowledge Enterprise Mass Spectrometry Research Facility.
Funding Information:
Acknowledgments—We thank Caitlin McDonough-Goldstein and Maria Vibranovski for helpful discussion, Alison Wright, Daniela Palmer, and Leeban Yusef for advice analyzing evolutionary rates. We are grateful to Eric Sedore and Larne Pekowsky who provided computing services (Syracuse University HTC Campus Grid), the authors whose data was used in this study, and the curators of FlyBase.org for continued maintenance of this essential resource. We are grateful to three anonymous reviewers who provided helpful feedback and comments on the article. This work was funded in part by the NSF award ACI-1341006, the Biodesign Institute and ASU Knowledge Enterprise Mass Spectrometry Research Facility.
Publisher Copyright:
© 2022 THE AUTHORS. Published by Elsevier Inc on behalf of American Society for Biochemistry and Molecular Biology.
PY - 2022/10
Y1 - 2022/10
N2 - Spermatozoa are central to fertilization and the evolutionary fitness of sexually reproducing organisms. As such, a deeper understanding of sperm proteomes (and associated reproductive tissues) has proven critical to the advancement of the fields of sexual selection and reproductive biology. Due to their extraordinary complexity, proteome depth-of-coverage is dependent on advancements in technology and related bioinformatics, both of which have made significant advancements in the decade since the last Drosophila sperm proteome was published. Here, we provide an updated version of the Drosophila melanogaster sperm proteome (DmSP3) using improved separation and detection methods and an updated genome annotation. Combined with previous versions of the sperm proteome, the DmSP3 contains a total of 3176 proteins, and we provide the first label-free quantitation of the sperm proteome for 2125 proteins. The top 20 most abundant proteins included the structural elements α- and β-tubulins and sperm leucyl-aminopeptidases. Both gene content and protein abundance were significantly reduced on the X chromosome, consistent with prior genomic studies of X chromosome evolution. We identified 9 of the 16 Y-linked proteins, including known testis-specific male fertility factors. We also identified almost one-half of known Drosophila ribosomal proteins in the DmSP3. The role of this subset of ribosomal proteins in sperm is unknown. Surprisingly, our expanded sperm proteome also identified 122 seminal fluid proteins (Sfps), proteins originally identified in the accessory glands. We show that a significant fraction of ‘sperm-associated Sfps’ are recalcitrant to concentrated salt and detergent treatments, suggesting this subclass of Sfps are expressed in testes and may have additional functions in sperm, per se. Overall, our results add to a growing landscape of both sperm and seminal fluid protein biology and in particular provides quantitative evidence at the protein level for prior findings supporting the meiotic sex-chromosome inactivation model for male-specific gene and X chromosome evolution.
AB - Spermatozoa are central to fertilization and the evolutionary fitness of sexually reproducing organisms. As such, a deeper understanding of sperm proteomes (and associated reproductive tissues) has proven critical to the advancement of the fields of sexual selection and reproductive biology. Due to their extraordinary complexity, proteome depth-of-coverage is dependent on advancements in technology and related bioinformatics, both of which have made significant advancements in the decade since the last Drosophila sperm proteome was published. Here, we provide an updated version of the Drosophila melanogaster sperm proteome (DmSP3) using improved separation and detection methods and an updated genome annotation. Combined with previous versions of the sperm proteome, the DmSP3 contains a total of 3176 proteins, and we provide the first label-free quantitation of the sperm proteome for 2125 proteins. The top 20 most abundant proteins included the structural elements α- and β-tubulins and sperm leucyl-aminopeptidases. Both gene content and protein abundance were significantly reduced on the X chromosome, consistent with prior genomic studies of X chromosome evolution. We identified 9 of the 16 Y-linked proteins, including known testis-specific male fertility factors. We also identified almost one-half of known Drosophila ribosomal proteins in the DmSP3. The role of this subset of ribosomal proteins in sperm is unknown. Surprisingly, our expanded sperm proteome also identified 122 seminal fluid proteins (Sfps), proteins originally identified in the accessory glands. We show that a significant fraction of ‘sperm-associated Sfps’ are recalcitrant to concentrated salt and detergent treatments, suggesting this subclass of Sfps are expressed in testes and may have additional functions in sperm, per se. Overall, our results add to a growing landscape of both sperm and seminal fluid protein biology and in particular provides quantitative evidence at the protein level for prior findings supporting the meiotic sex-chromosome inactivation model for male-specific gene and X chromosome evolution.
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U2 - 10.1016/j.mcpro.2022.100281
DO - 10.1016/j.mcpro.2022.100281
M3 - Article
C2 - 35985624
AN - SCOPUS:85140031703
SN - 1535-9476
VL - 21
JO - Molecular and Cellular Proteomics
JF - Molecular and Cellular Proteomics
IS - 10
M1 - 100281
ER -