Abstract
Inadequate gonadal maturation and poor spawning performance increasingly threaten the sustainability of shrimp aquaculture. Unraveling the mechanisms regulating ovarian development and maturation hence is critical to address industry challenges. Vitellogenin (Vtg), a precursor of yolk protein found in the hepatopancreas and ovary of shrimp, plays a key role in facilitating shrimp’s oocyte maturation and embryonic development after oviposition. This study found that FpVtg was specifically expressed in F. penicillatus hepatopancreas and ovary. FpVtg was localized predominantly in the oocyte cytoplasm and distributed uniformly in the hepatopancreas tissue. Silencing FpVtg led to apoptosis in both hepatopancreas and ovary tissues. Furthermore, FpVtg depletion upregulated the expression of ovarian peritrophin 1, ovarian peritrophin 2, serine proteinase inhibitor 6, and juvenile hormone esterase-like carboxylesterase 1, while downregulated that of vitellogenin, delta-9 desaturase, and insulin-like receptor. KEGG pathway analysis implicated such as PI3K-AKT signaling, RNA transport, ECM-receptor interaction, hippo signaling, oocyte meiosis, and apoptosis were enriched and involved in ovarian development. These findings have provided insights into the FpVtg’s reproductive role and the associated regulatory genes and pathways in F. penicillatus. This knowledge can contribute to establishing strategies to improve the breeding and aquaculture production of F. penicillatus by elucidating its vitellogenesis regulation in redtail prawn and other penaeid species. Further characterization of the implicated pathways and genes will clarify the intricacies underlying ovarian maturation.
Similar content being viewed by others
Data Availability
Data will be made available upon request.
References
Brady P, Elizur A, Cummins SF, Ngyuen NH, Williams R, Knibb W (2013) Differential expression microarrays reveal candidate genes potentially associated with reproductive dysfunction of captive-reared prawn Penaeus monodon. Aquaculture 400:14–28
Cai S, Huang Y, Wang B, Jian J, Xu Y (2017) Tumor necrosis factor receptor-associated factor 6 (TRAF6) participates in peroxinectin gene expression in Fenneropenaeus penicillatus. Fish Shellfish Immunol 64:193–201
Cappello F, David S, Rappa F, Bucchieri F, Marasà L, Bartolotta TE, Farina F, Zummo G (2005) The expression of HSP60 and HSP10 in large bowel carcinomas with lymph node metastase. BMC Cancer 5:139
Chang CF, Shih TW (1995) Reproductive cycle of ovarian development and vitellogenin profiles in the freshwater prawns, Macrobrachium rosenbergii. Invertebr Reprod Dev 27:11–20
Chen W, Syldath U, Bellmann K, Burkart V, Kolb H (1999) Human 60-kDa heat-shock protein: a danger signal to the innate immune system. J Immunol 162:3212–3219
Chi W, Gao Y, Hu Q, Guo W, Li D (2017) Genome-wide analysis of brain and gonad transcripts reveals changes of key sex reversal-related genes expression and signaling pathways in three stages of Monopterus albus. PLoS ONE 12:1–19
FAO (2019) FishStatJ, a tool for fishery statistics analysis, Release: 3.5.0, Universal Software for Fishery Statistical Time Series. Global aquaculture production: Quantity 1950–2017; Value 1950–2017; Global capture production. Rome, Italy: FAO 1950–2017
FAO (2020) Statistics – Introduction. Food and Agriculture Organization of the United Nations. Retrieved from http://www.FAO.org/fishery/statistics/en
Grabherr MG, Haas BJ, Yassour M, Levin JZ, Thompson DA, Amit I, Regev A (2011) Full-length transcriptome assemble from RNA-seq data without a reference genome. Nat Biotechnol 29:644–652
Halder G, Johnson RL (2011) Hippo signaling: growth control and beyond. Development 138:9–22
He Y, Shang X, Sun J, Zhang L, Zhao W, Tian Y, Cheng H, Zhou R (2010) Gonadal apoptosis during sex reversal of the rice field eel: implications for an evolutionarily conserved role of the molecular chaperone heat shock protein 10. J Exp Zool Part B 314:257–266
Hong CP, Lee SJ, Park JY, Plaha P, Park YS, Lee YK, Choi JE, Kim KY, Lee JH, Lee J, Jin H, Choi SR, Lim YP (2004) Construction of a BAC library of Korean ginseng and initial analysis of BAC-end sequences. Mol Gen Genet 271:709–716
Jiang K, Fang X, Li Y, Qiu GF (2023) Genome-wide identification, phylogeny, expression and eyestalk neuroendocrine regulation of vitellogenin gene family in the freshwater giant prawn Macrobrachium rosenbergii. Gen Comp Endocrinol 340:114306
Kong HJ, Cho HK, Park EM, Hong GE, Kim YO, Nam BH, Kim WJ, Lee SJ, Han HS, Jang IK, Lee CH (2009) Molecular cloning of Kazal-type proteinase inhibitor of the shrimp Fenneropenaeus chinensis. Fish Shellfish Immunol 26:109–114
Langmead B, Salzberg SL (2012) Fast gapped-read alignment with bowtie 2. Nat Methods 9:357–359
Lin KM, Lin B, Lian IY, Mestril R, Scheffler IE, Dillmann WH (2001) Combined and individual mitochondrial HSP60 and HSP10 expression in cardiac myocytes protects mitochondrial function and prevents apoptotic cell deaths induced by simulated ischemia-reoxygenation. Circulation 103:1787–1792
Ling J, Zhao K, Cui YG, Li Y, Wang X, Li M, Xue K, Ma X, Liu JY (2011) Heat shock protein 10 regulated apoptosis of mouse ovarian granulosa cells. Gynecol Endocrinol 27:63–71
Love MI, Huber W, Anders S (2014) Moderated estimation of fold change and dispersion for RNA-seq data with DESeq2. Genome Biol 15:1–21
Manfrin C, Tom M, Avian M, Battistella S, Pallavicini A, Giulianini PG (2021) Characterization and gene expression of vitellogenesis-related transcripts in the hepatopancreas and ovary of the red swamp crayfish, Procambarus clarkii (Girard, 1852), during reproductive cycle. Diversity 13:445
Misra JR, Irvine KD (2018) The hippo signaling network and its biological functions. Annu Rev Genet 52:65–87
Morton H, Hegh V, Clunie G (1974) Immunosuppression detected in pregnant mice by rosette inhibition test. Nature 249:459–460
Pace MC, Thomas P (2005) Steroid-induced oocyte maturation in Atlantic croaker (Micropogonias undulatus) is dependent on activation of the phosphatidylinositol 3- kinase/Akt signal transduction pathway. Biol Reprod 73:988–996
Patel RK, Jain M (2012) NGS QC toolkit: a toolkit for quality control of next generation sequencing data. PLoS ONE 7:e30619
Pertea G, Huang X, Liang F, Antonescu V, Sultana R, Karamycheva S, Quackenbush J (2003) TIGR gene indices clustering tools (TGICL): a software system for fast clustering of large EST datasets. Bioinformatics 19:651–652
Rosen O, Manor R, Weil S, Gafni O, Linial A, Aflalo ED, Ventura T, Sagi A (2010) A sexual shift induced by silencing of a single insulin-like gene in crayfish: Ovarian upregulation and testicular degeneration. PLoS One e15281
Roth Z, Weil S, Aflalo ED, Manor R, Sagi A, Khalaila I (2013) Identification of receptor-interacting regions of vitellogenin within evolutionarily conserved beta- sheet structures by using a peptide array. ChemBioChem 14:1116–1122
Sagi A, Manor R, Ventura T (2013) Gene silencing in crustaceans: from basic research to biotechnologies. Genes 4:620–645
Sasu S, LaVerda D, Qureshi N, Golenbock DT, Beasley D (2001) Chlamydia pneumoniae and chlamydial heat shock protein 60 stimulate proliferation of human vascular smooth muscle cells via Toll-like receptor 4 and p44/p42 mitogen-activated protein kinase activation. Circ Res 89:244–250
Schlesinger MJ (1990) Heat shock proteins. J Biol Chem 265:12111–12114
Schmittgen TD, Livak KJ (2018) Analyzing real-time PCR data by the comparative CT method. Nat Protoc 3:1101
Staley BK, Irvine KD (2012) Hippo signaling in Drosophila: recent advances and insights. Dev Dyn 241:3–15
Su B, Wang X, Dunham RA (2023) The application of genetic and genomic biotechnology in aquaculture. Biology 12:127
Sugumaran M (2002) Comparative biochemistry of eumelanogenesis and the protective roles of phenoloxidase and melanin in insects. Pigm Cell Res 15:2e9
Tacon AG (2020) Trends in global aquaculture and aquafeed production: 2000–2017. Rev Fish Sci Aquacult 28:43–56
Takada A, Takada Y, Urano T (1994) The physiological aspects of fibrinolysis. Thromb Res 76:1e31
Tan KA, Khor WH, Tan KS, Qiao Y, Lim LS, Yang X, Wen YL, Xu P, Peng Y, Ma X, Kwan KY (2023) Silencing of novel TtVtg6-like induced ovarian cell apoptosis in ancient chelicerate Tachypleus tridentatus. Biochem Biophys Res Commun 679:66–74
Tan K, Yu JY, Liao SL, Huang JR, Li M, Wang WM (2022) Transcriptomic profiling and novel insights into the effect of AG ablation on gonad development in Macrobrachium rosenbergii. Aquaculture 556:738224
Tan KA, Zhou M, Jiang H, Jiang D, Li YH, Wang WM (2020a) siRNA-mediated MrIAG silencing induces sex reversal in Macrobrachium rosenbergii. Mar Biotech 22:456–466
Tan KA, Li YH, Zhou M, Wang WM (2020b) siRNA knockdown of MrIR induces sex reversal in Macrobrachium rosenbergii. Aquaculture 523:735172
Thongbuakaew T, Siangcham S, Suwansa-Ard S, Elizur A, Cummins SF, Sobhon P, Sretarugsa P (2016) Steroids and genes related to steroid biosynthesis in the female giant freshwater prawn, Macrobrachium rosenbergii. Steroids 107:149–160
Tiu SH, Hui HL, Tsukimura B, Tobe SS, He JG, Chan SM (2009) Cloning and expression study of the lobster (Homarus americanus) vitellogenin: conservation in gene structure among decapods. Gen Comp Endocrinol 160:36–46
Wang S, Xie Y (2014) China species red list, vol 1. Higher Education Press, Beijing, China, pp 189–224
Xie C, Mao X, Huang J, Ding Y, Wu J, Dong S, Wei L (2011) KOBAS 2.0: a web server for annotation and identification of enriched pathways and diseases. Nucleic Acids Res 39:316–322
Xu Y, Huang Y, Cai S (2017) Characterization and function analysis of interleukin-1 receptor-associated kinase-1 (IRAK-1) from Fenneropenaeus penicillatus. Fish Shellfish Immunol 61:111–119
Ye J, Fang L, Zheng H, Zhang Y, Chen J, Zhang Z, Wang J, Li S, Li R, Bolund L, Wang J (2006) WEGO: a web toll for plotting GO annotations. Nucleic Acids Res 34:W293–W297
Young MD, Wakefield MJ, Smyth GK, Oshlack A (2010) Gene ontology analysis for RNA-seq: accounting for selection bias. Genome Biol 11:R14
Zhao JC, Wang W, Wang CG, Shi LL, Wang G, Sun CB, Chan SF (2021) The presence of multiple copies of the vitellogenin gene in Fenneropenaeus merguiensis (De Man, 1888) (Decapoda: Dendrobranchiata: Penaeidae): evidence for gene expansion and functional diversification in shrimps. J Crustac Biol 41:ruaa100
Funding
This research was financially supported by a research grant from the National Natural Science Foundation of China (42366006); High-level Talent Scientific Research Start-Up Fund Project of Beibu Gulf University (2022KYQD10); ASEAN Talented Young Scientist Program of Guangxi (ATYSP2022008); Marine Science Program for Guangxi First-Class Discipline, Beibu Gulf University (DRA002, TRA001).
Author information
Authors and Affiliations
Contributions
Kianann Tan: methodology, writing — original draft, funding acquisition, conceptualization, resources. Yaxin Dong: investigation, formal analysis. Karsoon Tan: investigation, supervision. Leong-Seng Lim: writing — review and editing, visualization. Khor Waiho: methodology, conceptualization. Jing Chen: formal analysis, visualization. Peng Xu: project administration, supervision, conceptualization. Kit Yue Kwan: funding acquisition, resources, writing — review and editing.
Corresponding authors
Ethics declarations
Ethics Approval
All experiments in this study were conducted under a protocol approved by the Institutional Animal Care and Use Committee (IACUC, China).
Competing Interests
The authors declare no competing interests.
Additional information
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Rights and permissions
Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.
About this article
Cite this article
Tan, K., Dong, Y., Tan, K. et al. siRNA Silencing of FpVtg Induces Ovarian Cell Apoptosis in Redtail Prawn, Fenneropenaeus penicillatus. Mar Biotechnol 25, 1176–1190 (2023). https://doi.org/10.1007/s10126-023-10269-6
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10126-023-10269-6