Mating-Induced Trade-Offs upon Egg Production versus Fertilization and Offspring’s Survival in a Sawfly with Facultative Parthenogenesis
Abstract
:Simple Summary
Abstract
1. Introduction
2. Materials and Methods
2.1. Sample Collection
2.2. Library Preparation and Sequencing
2.3. Quality Control and Assembly
2.4. Differential Expression Analysis
2.5. Functional Annotation and Enrichment Analysis of Differentially Expressed Genes (DEGs)
2.6. Validation by qRT-PCR
3. Results
3.1. Sequencing and Assembly
3.2. Outline of Mating-Induced Transcriptional Changes
3.3. Transcriptional Changes at 1 h Post-Mating
3.4. Transcriptional Changes at 6 h Post-Mating
3.5. Transcriptional Changes at 24 h Post-Mating
3.6. Validation of RNAseq by qRT-PCR
4. Discussion
Supplementary Materials
Author Contributions
Funding
Institutional Review Board Statement
Data Availability Statement
Acknowledgments
Conflicts of Interest
References
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GeneID | log2FoldChange | Padj | Annotation | Function | Reference |
---|---|---|---|---|---|
Mated-1 h vs. Virgin-1 h | |||||
DN64818_c0_g6 | −3.51325 | 0.02376 | Follicle cell protein 3C | Encodes a major protein component of the vitelline membrane. | [33] |
DN64030_c0_g1 | 9.66278 | 0.00015 | CYP2C (Cytochrome P450 family) | Detoxification and the biosynthesis of hormones. | [34] |
Mated-6 h vs. Virgin-6 h | |||||
DN65980_c5_g3 | −9.14964 | 1.05 × 10−8 | Vitellogenin-2 | Plays vital role in oocytes and embryo development in insects. | [35,36] |
N55390_c2_g3 | −7.75002 | 0.00289 | Vitellogenin-A2-like | ||
N52188_c2_g1 | −6.37534 | 0.00062 | Vitellogenin-A2-like | ||
DN71364_c1_g1 | −2.39804 | 2.43 × 10−11 | Vitellogenin-like | ||
DN59614_c4_g1 | −2.34561 | 1.55 × 10−10 | Vitellogenin-like | ||
DN78694_c0_g1 | −3.45314 | 0.03932 | Haemolymph juvenile hormone binding protein | Protect the labile hormone molecules from degradation by esterase. | [37,38] |
DN63882_c0_g1 | −2.75932 | 0.00064 | |||
DN65663_c1_g1 | −2.48229 | 1.04 × 10−8 | |||
DN65191_c2_g1 | −2.34190 | 0.02528 | Protein takeout-like | Takeout is part of a large gene family found throughout insects with roles in metabolism, circadian behavior, aging, and male courtship behavior. | [39] |
DN69612_c3_g1 | −1.58633 | 0.03611 | Protein takeout-like | ||
DN66978_c2_g1 | −2.71257 | 0.00840 | UDP-glucosyltransferase | Positive modulator of fecundity. | [40] |
DN71428_c0_g1 | −8.16014 | 9.90 × 10−5 | Matrix metalloproteinase-16 | Some members of matrix metalloproteinase may play roles in corpus luteum formation, follicular development, and ovulation. | [41] |
DN69614_c4_g4 | −2.86011 | 0.04696 | CYP4 (Cytochrome P450 family) | Detoxification and the biosynthesis of hormones. | [34] |
DN52313_c1_g5 | −2.81364 | 3.33 × 10−14 | CYP4 (Cytochrome P450 family) | ||
DN69106_c0_g1 | −2.15773 | 0.00170 | CYP4 (Cytochrome P450 family) | ||
DN53829_c6_g2 | −2.00810 | 0.01412 | CYP4 (Cytochrome P450 family) | ||
Mated-24 h vs. Virgin-24 h | |||||
DN65980_c5_g3 | −9.44195 | 1.71 × 10−14 | Vitellogenin-2 | Plays vital role in oocytes and embryo development in insects. | [35,36] |
DN71047_c1_g1 | −8.99780 | 8.17 × 10−11 | Vitellogenin-A2-like | ||
DN55390_c2_g3 | −8.55112 | 1.39 × 10−7 | Vitellogenin-A2-like | ||
DN52188_c2_g1 | −8.51720 | 2.32 × 10−7 | Vitellogenin-A2-like | ||
DN49694_c0_g1 | −2.51669 | 0.00038 | Vitellogenin-like | ||
DN59614_c4_g1 | −2.30309 | 0.02439 | Vitellogenin-like | ||
DN71364_c1_g1 | −2.31618 | 0.02594 | Vitellogenin-like | ||
DN54912_c7_g1 | 9.02029 | 1.51 × 10−11 | Vitellogenin receptor | ||
DN58744_c7_g1 | 9.28253 | 8.58 × 10−14 | Zona pellucida sperm-binding protein (ZP) 1-like | ||
DN32813_c0_g1 | 9.32544 | 3.72 × 10−14 | Zp1 | ||
DN67043_c1_g1 | 11.27687 | 2.07 × 10−52 | Zp1 | ||
DN44634_c0_g2 | 10.29005 | 2.97 × 10−23 | Zp2 | ||
DN93387_c0_g1 | 7.70158 | 0.002245 | Zp3 | ||
DN50223_c1_g2 | 8.04870 | 5.28 × 10−5 | Zp3 | ||
DN12342_c0_g1 | 8.89036 | 1.66 × 10−10 | Zp3 | ||
DN63118_c0_g5 | 9.43726 | 3.94 × 10−15 | Zp3 | ||
DN42788_c0_g1 | 9.81002 | 1.13 × 10−18 | Zp3 | ||
DN44618_c0_g1 | 9.87890 | 1.89 × 10−52 | Zp3 | The zona pellucida is a glycoprotein layer surrounding the plasma membrane of oocytes. It is a vital constitutive part of the oocyte and functions in primary binding and induction of the sperm acrosome reaction. | [42,43,44] |
DN43523_c0_g1 | 10.0620 | 5.22 × 10−21 | Zp3 | ||
DN22329_c0_g1 | 10.18637 | 3.23 × 10−22 | Zp3 | ||
DN47551_c0_g1 | 10.48415 | 1.26 × 10−43 | Zp3 | ||
DN48592_c0_g2 | 11.49147 | 9.56 × 10−37 | Zp3 | ||
DN63118_c0_g2 | 11.49933 | 2.70 × 10−64 | Zp3 | ||
DN47452_c0_g3 | 11.88468 | 1.13 × 10−41 | Zp3 | ||
DN49748_c0_g1 | 12.50758 | 6.61 × 10−49 | Zp3 | ||
DN100350_c0_g1 | 12.60210 | 5.74 × 10−50 | Zp3 | ||
DN63118_c0_g1 | 13.09691 | 3.27 × 10−70 | Zp3 | ||
DN67043_c2_g1 | 7.96939 | 4.36 × 10−26 | Zp4 | ||
DN67043_c1_g2 | 8.81695 | 6.03 × 10−10 | Zp4 | ||
DN72297_c0_g1 | 9.81754 | 9.66 × 10−19 | Zp4 | ||
DN67043_c2_g3 | 10.63913 | 5.50 × 10−62 | Zp4 | ||
DN67258_c0_g10 | 10.78996 | 1.26 × 10−28 | Zp4 | ||
DN50530_c5_g14 | 9.970503 | 3.83 × 10−20 | ZP domain-containing protein-like | ||
DN46494_c0_g1 | 12.88190 | 4.01 × 10−53 | ZP domain-containing protein-like | ||
DN64127_c3_g3 | 9.64628 | 4.61 × 10−17 | Embryonic poly(A)-binding protein A | Required for oocyte maturation and female fertility. | [45] |
DN82911_c0_g1 | 8.20682 | 7.04 × 10−6 | Insulinase | Destroys or inactivates insulin. Elevated insulin promotes oogenesis and inhibits immune responses. | [1,46] |
DN49876_c0_g1 | 8.44020 | 2.62 × 10−7 | Insulinase | ||
DN46576_c0_g1 | 8.18360 | 9.56 × 10−6 | G1/S-specific cyclin-E-like | Oocyte maturation and the onset of embryogenesis. | [47,48,49] |
DN49363_c0_g1 | 9.49947 | 1.08 × 10−15 | G2/mitotic-specific cyclin-A | ||
DN49147_c0_g1 | 11.21366 | 1.90 × 10−33 | G2/mitotic-specific cyclin-B | ||
DN15801_c0_g1 | 9.55009 | 3.72 × 10−16 | G2/mitotic-specific cyclin-B | ||
DN47388_c2_g1 | 10.19335 | 2.76 × 10−22 | G2/mitotic-specific cyclin-B-like | ||
DN49534_c0_g1 | 9.76583 | 2.58 × 10−46 | G2/mitotic-specific cyclin-B-like isoform X4 | ||
DN8940_c0_g1 | 10.33337 | 1.07 × 10−23 | Cell division cycle protein 20 homolog | ||
DN50119_c0_g2 | −6.06256 | 3.33 × 10−13 | Apolipophorin III | Plays roles in lipid uptake by insect oocytes. | [50] |
DN71428_c0_g1 | −8.39452 | 1.39 × 10−6 | Matrix metalloproteinase-16 | Some members of matrix metalloproteinase may play roles in corpus luteum formation, follicular development, and ovulation. | [41] |
DN56705_c2_g7 | −3.79775 | 0.01004 | Matrix metalloproteinase-24-like | ||
DN37027_c0_g1 | 11.90835 | 5.60 × 10−42 | Zygote arrest protein 1 | Ovary-specific maternal factor that plays essential roles during the oocyte-to-embryo transition. | [51] |
DN94405_c0_g1 | 12.16383 | 4.47 × 10−45 | Zygote arrest protein 1 | ||
DN84630_c0_g1 | 8.95337 | 5.28 × 10−11 | Astacin-like; Ovastacin | Cleaves ZP2 and prevents polyspermy; degrades egg envelope and releases the embryo from its intracapsular life. | [52] |
DN47329_c0_g1 | 10.45829 | 5.41 × 10−25 | Oocyte-specific histone RNA stem-loop-binding protein 2 | Plays a role in the storage of replication-dependent histone mRNAs and proteins during oogenesis. | [53] |
Pathway | Padj | Number of Genes | First Category | Second Category | Function |
---|---|---|---|---|---|
Mated-1 h vs. Virgin-1 h: Up regulated DEGs | |||||
Steroid hormone biosynthesis | 0.03602 | 1 | Metabolism | Lipid metabolism | Egg maturation |
Mated-24 h vs. Virgin-24 h: Down regulated DEGs | |||||
Estrogen signaling pathway | 0.01301 | 4 | Organismal Systems | Endocrine system | Fecundity |
Mated-24 h vs. Virgin-24 h: Up regulated DEGs | |||||
Oocyte meiosis | 0.01082 | 18 | Cellular Processes | Cell growth and death | Egg maturation |
Progesterone-mediated oocyte maturation | 0.03177 | 13 | Organismal Systems | Endocrine system | Egg maturation |
GeneID | log2FoldChange | Padj | Annotation | Function | Reference |
---|---|---|---|---|---|
Mated-1 h vs. Virgin-1 h | |||||
DN70573_c2_g1 | −5.42272 | 1.27 × 10−9 | Defensin | Insect antimicrobial peptides. | [54] |
DN60391_c5_g2 | −5.02886 | 2.84 × 10−8 | Hymenoptaecin | ||
Mated-6 h vs. Virgin-6 h | |||||
DN63597_c1_g1 | −3.53279 | 4.53 × 10−12 | Phenoloxidase | Phenoloxidase involved in defensive melanization and production of oxidative free radicals. | [1] |
Mated-24 h vs. Virgin-24 h | |||||
DN45974_c0_g1 | −6.77749 | 5.08 × 10−7 | Megourin | Insect antimicrobial peptides. | [54] |
DN45254_c0_g1 | −6.34763 | 4.15 × 10−17 | Fungal protease inhibitor-1-like | Against fungal infection. | [55] |
DN71273_c1_g5 | −2.95068 | 0.00896 | C-type lysozyme | Defends against bacterial infection by hydrolyzing the bacterial cell walls and causing bacterial lysis. | [56] |
DN51648_c2_g8 | −6.63010 | 9.23 × 10−11 | Heat shock protein 27.2 (sHsp family) | Heat shock and stress response. | [4] |
DN47336_c0_g1 | −5.01800 | 1.63 × 10−12 | Heat shock protein 27.2 (sHsp family) | ||
DN71108_c1_g3 | −4.29401 | 3.40 × 10−11 | Heat shock protein 27.2 (sHsp family) | ||
DN56298_c0_g1 | −3.69216 | 0.02212 | Heat shock protein 27.2 (sHsp family) | ||
DN70765_c7_g9 | −4.25919 | 1.24 × 10−13 | Heat shock protein 70-like (Hsp70 family) | ||
DN57953_c3_g2 | −3.39554 | 5.58 × 10−10 | Heat shock protein 70-like (Hsp70 family) | ||
DN62526_c5_g1 | −6.22937 | 1.06 × 10−7 | Heat shock protein 70 cognate (Hsp70 family) | ||
DN62526_c5_g4 | −4.59306 | 0.04497 | Heat shock protein 70 cognate (Hsp70 family) | ||
DN67613_c0_g10 | 10.89725 | 7.42 × 10−30 | Heat shock protein 70 (Hsp70 family) | ||
DN67613_c0_g5 | 8.479329 | 6.81 × 10−21 | Heat shock protein 70 (Hsp70 family) | ||
DN67090_c3_g8 | 8.29444 | 2.51 × 10−6 | Heat shock protein 70 domain containing protein (Hsp70 family) | ||
DN64447_c3_g1 | 7.39234 | 0.03894 | Heat shock protein 75 (Hsp90 family) | ||
DN64447_c4_g1 | 3.92852 | 4.91 × 10−11 | Heat shock protein 90 (Hsp90 family) |
Pathway | Padj | Number of Genes | First Category | Second Category | Function |
---|---|---|---|---|---|
Mated-1 h vs. Virgin-1 h: Down regulated DEGs | |||||
Inflammatory bowel disease (IBD) | 0.02764 | 1 | Human Diseases | Immune disease | Defense |
Legionellosis | 0.02981 | 1 | Human Diseases | Infectious disease: bacterial | Defense |
Salmonella infection | 0.03185 | 1 | Human Diseases | Infectious disease: bacterial | Defense |
Pathogenic Escherichia coli infection | 0.03341 | 1 | Human Diseases | Infectious disease: bacterial | Defense |
Mated-1 h vs. Virgin-1 h: Up regulated DEGs | |||||
Inflammatory mediator regulation of TRP channels | 0.03394 | 1 | Organismal Systems | Sensory system | Defense |
Complement and coagulation cascades | 0.03397 | 1 | Organismal Systems | Immune system | Defense |
Mated-6 h vs. Virgin-6 h: Down regulated DEGs | |||||
Complement and coagulation cascades | 0.00061 | 5 | Organismal Systems | Immune system | Defense |
Staphylococcus aureus infection | 0.00791 | 3 | Human Diseases | Infectious disease: bacterial | Defense |
Platelet activation | 0.01418 | 4 | Organismal Systems | Immune system | Defense |
Mated-24 h vs. Virgin-24 h: Down regulated DEGs | |||||
Antigen processing and presentation | 0.00018 | 6 | Organismal Systems | Immune system | Defense |
Legionellosis | 0.00046 | 6 | Human Diseases | Infectious disease: bacterial | Defense |
Measles | 0.00319 | 5 | Human Diseases | Infectious disease: viral | Defense |
Complement and coagulation cascades | 0.00620 | 4 | Organismal Systems | Immune system | Defense |
Influenza A | 0.00987 | 5 | Human Diseases | Infectious disease: viral | Defense |
Toxoplasmosis | 0.01130 | 4 | Human Diseases | Infectious disease: parasitic | Defense |
Tuberculosis | 0.02795 | 4 | Human Diseases | Infectious disease: bacterial | Defense |
Amoebiasis | 0.02986 | 3 | Human Diseases | Infectious disease: parasitic | Defense |
Staphylococcus aureus infection | 0.04516 | 2 | Human Diseases | Infectious disease: bacterial | Defense |
Longevity regulating pathway - multiple species | 0.01139 | 4 | Organismal Systems | Aging | Aging |
Mated-24 h vs. Virgin-24 h: Up regulated DEGs | |||||
Pathogenic Escherichia coli infection | 6.25 × 10−5 | 18 | Human Diseases | Infectious disease: bacterial | Defense |
Legionellosis | 0.01178 | 16 | Human Diseases | Infectious disease: bacterial | Defense |
Viral myocarditis | 0.02943 | 10 | Human Diseases | Cardiovascular disease | Defense |
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Yu, H.; Shi, M.-R.; Xu, J.; Chen, P.; Liu, J.-H. Mating-Induced Trade-Offs upon Egg Production versus Fertilization and Offspring’s Survival in a Sawfly with Facultative Parthenogenesis. Insects 2021, 12, 693. https://doi.org/10.3390/insects12080693
Yu H, Shi M-R, Xu J, Chen P, Liu J-H. Mating-Induced Trade-Offs upon Egg Production versus Fertilization and Offspring’s Survival in a Sawfly with Facultative Parthenogenesis. Insects. 2021; 12(8):693. https://doi.org/10.3390/insects12080693
Chicago/Turabian StyleYu, Hong, Min-Rui Shi, Jin Xu, Peng Chen, and Jian-Hong Liu. 2021. "Mating-Induced Trade-Offs upon Egg Production versus Fertilization and Offspring’s Survival in a Sawfly with Facultative Parthenogenesis" Insects 12, no. 8: 693. https://doi.org/10.3390/insects12080693