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Reproductive functions of venerose, a sexually transmitted sugar in the fruit fly Drosophila melanogaster

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Abstract
Seminal fluid is more than just carrier for sperm. Its complex composition, consisting of ions, peptides, proteins, lipids, and carbohydrates, actively communicates with the female reproductive system. However, the significance of non-protein substances such as present in seminal fluid remains largely underexplored. In this thesis, I utilized Drosophila melanogaster to investigate the influence of a seminal sugar on female reproduction. I found that a significant amount of phospho-galactoside named ‘venerose,’ present in the male seminal fluid, is incorporated into female ovaries and enters the haemolymph. The findings revealed that venerose acts as a signaling molecule for promoting the mating-induced germline stem cell (GSC) proliferation and enhancing sperm storage, particularly in undernourished females. Circulating venerose directly activates Dh44-PI neurons, nutrient-sensing cells in the brain. The secreted Dh44 stimulates GSC proliferation by activating its receptor in terminal filament cells and enhancing Decapentaplegic (Dpp) signaling. Additionally, the evidence indicates that undernourished females exhibit the increased Dh44 release in response to venerose. This increased Dh44 secretion delays the removal or expulsion of the ejaculate (sperm ejection), thereby increasing the sperm uptake and venerose absorption. This study establishes a framework for understanding the function of nutrient-like substances abundant in seminal fluid and provides mechanical insights into how females assess courtship feeding for sexual selection.
Author(s)
김성진
Issued Date
2025
Type
Thesis
URI
https://scholar.gist.ac.kr/handle/local/19638
Alternative Author(s)
Seong-Jin Kim
Department
대학원 생명과학부
Advisor
Kim, Young-Joon
Table Of Contents
Abstract
List of contents
List of figures and tables
Chapter 1. General introduction
1.1 The role of seminal plasma in enhancing male fertility
1.2 Complex roles of seminal fluid in Drosophila melanogaster reproduction
1.3 Germline stem cell proliferation in Drosophila melanogaster female
1.4 Sexual selection and courtship feeding
Chapter 2. Identification of venerose, a sexually transmitted sugar in the fruit fly and its reproductive functions
2.1 Introduction
2.2 Results
2.2.1. Venerose, a phospho-galactoside abundant in seminal fluid
2.2.2. Glucosyltransferase is required for venerose production
2.2.3. Females absorb venerose from the male ejaculate
2.2.4. Venerose is essential for mating-induced GSC proliferation
2.2.5. Venerose stimulates GSC proliferation via a brain factor
2.2.6. Dh44 acts on the ovaries to trigger GSC proliferation
2.2.7. Venerose stimulates GSC proliferation via Dh44-PI neurons
2.2.8. Venerose stimulates Dh44-PI neurons to secrete Dh 44
2.2.9. Venerose stimulates Dh44-PI neurons via Tret1- 1
2.2.10. Energy-deprived females absorb more venerose
2.2.11. Energy-dependent effects of venerose on EHP and sperm storage
2.2.12. Energy state determines Dh44 pool size
2.2.13. Females assess the energy status of male partners via venerose
2.2.14. Other functions of venerose in female systems
2.3. Discussion
2.3.1. Venerose is a signaling molecule that activates the Dh44 system during mating
2.3.2. Dh44 regulates GSC proliferation and EHP expansion via distinct GPCR pathways
2.3.3. Venerose, a non-protein seminal substance that promotes GSC proliferation
2.3.4. Venerose transfer is a form of courtship feeding signaling male quality
2.3.5. Nutritional stress enhances acceptance of courtship feeding
2.3.6. The Dh44 system couples oogenesis with energy state
2.3.7. A potential implication in mammalian systems
2.3.8. Limitations of this study
2.4. Material and Methods
Chapter 3. General Conclusion
Chapter 4. References
List of figures and tables
Figures
Figure 1. Interplay of nutritional and seminal signals regulating germline stem cell proliferation and reproductive responses in Drosophila melanogaster
Figure 2. Identification of venerose, a sugar-like substance rich in male Drosophila ejaculate
Figure 3. Structural analysis of native venerose
Figure 4. Venerose production requires the 1,2-Diacyl-glycerol (DAG) biosynthesis genes or lipase genes in the MAG
Figure 5. MAG-specific knockdown of the glycosyltransferase UGT305A1 inhibits venerose production
Figure 6. UGT305A1 knockdown had limited effects on MAG morphology or SP content
Figure 7. MAG-specific knockdown of the glycosyltransferase UGT305A1 reduces phosphorus accumulation in the ovaries of females mated with knockdown males
Figure 8. Venerose, enhancing egg-laying activity, has a limited impact on sperm fertility or offspring survival rate
Figure 9. Females mated with UGT305A1 knockdown males show defects in GSC proliferation, but this effect can be restored by venerose injection
Figure 10. Venerose stimulates GSC proliferation by boosting BMP signaling activity to GSCs
Figure 11. Venerose stimulates GSC proliferation via the brain
Figure 12. Dh44-R2 and Bab1-Gal4 expression do not overlap in the ovary
Figure 13. The neuropeptide Dh44, secreted by brain Dh44-PI neurons, and its receptor Dh44-R2, expressed in GSC niche cells, are essential for venerose-induced GSC proliferation
Figure 14. Dh44-R2 knockdown females show no increase in GSC proliferation upon mating
Figure 15. Venerose stimulates Ca2+ transients and Dh44 secretion in Dh44-PI neurons via the sugar transporter Tret1- 1
Figure 16. Females with Tret1-1 knockdown in Dh44-PI neurons exhibit do not differentiate between nutritive D-glucose and non-nutritive L-glucose
Figure 17. Nutritional stress in females extends EHP duration and enhances venerose absorption
Figure 18. Starvation decreases the neural activity of Dh44-PI neurons
Figure 19. Nutritional stress in females extends EHP duration by increasing the Dh44 pool available for venerose-induced secretion
Figure 20. Under nutritional stress conditions, females discern the energy states of their mates by extending EHP, absorbing more venerose, and storing a greater amount of sperm from well-nourished males compared to undernourished males
Figure 21 Females mated with venerose-depleted males partially decreases mating-induced vitellogenesis, which is fully rescued by venerose injection
Figure 22. Venerose is not utilized as an oral energy source in females
Figure 23. Venerose can alters gut gene expression, and defecation activity
Figure 24. Starved females mated with well-nourished males exhibit stronger GSC proliferation upon mating than those mated with starved males. Oamb-deficient females show GSC proliferation in response to synthetic venerose injection
Degree
Doctor
Appears in Collections:
Department of Life Sciences > 4. Theses(Ph.D)
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