Drosophila oocyte proteome composition covaries with female mating status

Abstract

Oocyte composition can directly influence offspring fitness, particularly in oviparous species such as most insects, where it is the primary form of parental investment. Oocyte production is also energetically costly, dependent on female condition and responsive to external cues. Here, we investigated whether mating influences mature oocyte composition in Drosophila melanogaster using a quantitative proteomic approach. Our analyses robustly identified 4,485 oocyte proteins and revealed that stage-14 oocytes from mated females differed significantly in protein composition relative to oocytes from unmated females. Proteins forming a highly interconnected network enriched for translational machinery and transmembrane proteins were increased in oocytes from mated females, including calcium binding and transport proteins. This mating-induced modulation of oocyte maturation was also significantly associated with proteome changes that are known to be triggered by egg activation. We propose that these compositional changes are likely to have fitness consequences and adaptive implications given the importance of oocyte protein composition, rather than active gene expression, to the maternal-to-zygotic transition and early embryogenesis.

Transcriptome Analysis Provides Insights into Copulation, Fertilization, and Gestation in Sebastes schlegelii

“…Previous studies in Atlantic cod [ 27 ], yak [ 28 ], chickens [ 29 ], and insects [ 30 ] also reported similar pathways involved in oogenesis. In addition, in Drosophila [ 31 ], mating-induced oocyte maturation with calcium binding and transport proteins increased, as well as calcium signaling pathways that were also significantly enriched in the present study.…”

A male pheromone that improves the quality of the oogenic germline

“…Therefore, our finding that ascr#10 improves oocyte maintenance supports the idea that this pheromone communicates a higher demand for quality oocytes in anticipation of mating to promote reproductive success ( 19 , 21 ). In other species, female reproductive physiology is substantially altered by mating, at least in part due to components of the seminal fluid ( 41 ) that can alter the germline ( 42 ) as well as organ systems required to sustain the germline ( 43 , 44 ).…”

Functional Diversity and Evolution of the Drosophila Sperm Proteome

“…The finding of a large number of ribosomal proteins in the DmSP3 was unexpected given sperm are thought to be transcriptionally quiescent. Therefore, we next compared the representation of ribosomal proteins found in the DmSP3 to three other recent proteomic studies in D. melanogaster which used Lumos Fusion Orbitrap mass-spectrometers, representing the female germline and two somatic tissues; embryo (43), unfertilized oocyte (44), and brain (45). All four tissue/cell types identified most cytoplasmic ribosomal proteins, with a slight underrepresentation of large cytoplasmic subunits in the brain (Fig.…”