Abstract
Schizothorax oconnori (S. oconnori) is an economically important fish in Tibet. Oocyte maturation is a physiological process that is of great significance to reproduction and seed production in S. oconnori, yet little is currently known regarding the molecular mechanisms of oocyte development in this species. To identify candidate genes involved in reproduction of female fish, a combination of PacBio and Illumina HiSeq technologies was employed to provide deep coverage of the oocyte transcriptome. Transcriptome analysis revealed several candidate genes that are potentially involved in the regulation of oocyte maturation in S. oconnori, including GIRK1, CHRM3, NPY2R, GABRA3, GnRH3, mGluR1α, GPER1, GDF9, HSP90, and ESR2. Genes that are significantly expressed during oocyte maturation mainly contribute to the GPCR signaling pathway and the estrogen signaling pathway. Neurotransmitter (Ach, NPY, and GABA) and peptide hormone (GnRH3) binding to G protein-coupled receptors (GPCRs) frees G-protein βγ subunits to interact with the G protein-gated inward rectifier K+ channel 1 (GIRK1). This process helps release K+ from granulosa cells to maturing oocytes, allowing yolk globule fusion. This mechanism may play an important role in oocyte maturation in S. oconnori. In conclusion, this study provides a valuable basis for deciphering the reproductive system in S. oconnori during the oocyte maturation process.
Similar content being viewed by others
Data Availability
The datasets used and analysed during the current study have been deposited to Biotechnology Information (NCBI) Sequence Read Archive (SRA) under accession number: PRJNA527715 (https://www.ncbi.nlm.nih.gov/search/all/?term=PRJNA527715) and PRJNA527627 (https://www.ncbi.nlm.nih.gov/search/all/?term=PRJNA527627).
References
Bao-Shan MA, Cong-Xin X, Bin H, University HA (2014) Life history pattern and exploitation status of a population of schizothorax o'connori in the yarlung zangbo river. Resources and Environment in the Yangtze Basin 23(11):1558–1565
Bolamba, D, Pati?O, R, Yoshizaki, G, Thomas, P (2003) Changes in homologous and heterologous gap junction contacts during maturation-inducing hormone-dependent meiotic resumption in ovarian follicles of Atlantic croaker. General Comparative Endocrinol 131, 291-295 https://doi.org/10.1016/S0016-6480(03)00015-7
Briguglio, M, Dell'osso, B, Panzica, G, Malgaroli, A, Banfi, G, Zanaboni Dina, C, et al. (2018) Dietary Neurotransmitters: A Narrative Review on Current Knowledge. Nutrients 10. https://doi.org/10.3390/nu10050591
Cerda JL, Petrino TR, Wallace RA (1993) Functional heterologous gap junctions in Fundulus ovarian follicles maintain meiotic arrest and permit hydration during oocyte maturation. Dev Biol 160:228–235. https://doi.org/10.1006/dbio.1993.1300
Cerda J, Zapater C, Chauvigne F, Finn RN (2013) Water homeostasis in the fish oocyte: new insights into the role and molecular regulation of a teleost-specific aquaporin. Fish Physiol Biochem 39:19–27. https://doi.org/10.1007/s10695-012-9608-2
Chapman RW, Reading BJ, Sullivan CV (2014) Ovary transcriptome profiling via artificial intelligence reveals a transcriptomic fingerprint predicting egg quality in striped bass. Morone Saxatilis Plos One 9:e96818. https://doi.org/10.1371/journal.pone.0096818
Chen Y, Cheng Q, Qiao H, Chen W, Zhu Y (2013) The complete mitochondrial genome structure of Schizothorax oconnori (Cypriniformes: Cyprinidae). Mitochondrial DNA 24. 24(6):630–2
Cheol, Young, Choi, Takashima, and Fumio (2000) Molecular cloning and hormonal control in the ovary of connexin 31.5 mRNA and correlation with. J Experiment Biol 203(Pt 21):3299–306
Dascal N (2001) Ion-channel regulation by G proteins. Trends Endocrinol Metab 12:391–398. https://doi.org/10.1016/s1043-2760(01)00475-1
Deloffre LA, Andrade A, Filipe AI, Canario AV (2012) Reference genes to quantify gene expression during oogenesis in a teleost fish. Gene 506:69–75. https://doi.org/10.1016/j.gene.2012.06.047
Fabra M, Raldúa D, Power DM, Deen PMT, Cerdà J (2005) Marine fish egg hydration is aquaporin-mediated. Science 307:545–545
Fabra M, Raldua D, Bozzo MG, Deen PM, Lubzens E, Cerda J (2006) Yolk proteolysis and aquaporin-1o play essential roles to regulate fish oocyte hydration during meiosis resumption. Dev Biol 295:250–262. https://doi.org/10.1016/j.ydbio.2006.03.034
Fan Z, You F, Wang L, Weng S, Wu Z, Hu J et al (2014) Gonadal transcriptome analysis of male and female olive flounder (Paralichthys olivaceus). Biomed Res Int 2014:291067. https://doi.org/10.1155/2014/291067
Farrants H, Gutzeit VA, Acosta-Ruiz A, Trauner D, Johnsson K, Levitz J et al (2018) SNAP-Tagged Nanobodies Enable Reversible Optical Control of a G Protein-Coupled Receptor via a Remotely Tethered Photoswitchable Ligand. ACS Chem Biol 13:2682–2688. https://doi.org/10.1021/acschembio.8b00628
Finn RN, Ostby GC, Norberg B, Fyhn HJ (2002) In vivo oocyte hydration in Atlantic halibut (Hippoglossus hippoglossus); proteolytic liberation of free amino acids, and ion transport, are driving forces for osmotic water influx. J Exp Biol 205:211–224
Fisher DL, Mandart E, Dorée M (2000) Hsp90 is required for c-Mos activation and biphasic MAP kinase activation in Xenopus oocytes. EMBO J 19(7):1516–1524
Halm S, Ibañez AJ, Tyler CR, Prat F (2008) Molecular characterisation of growth differentiation factor 9 (gdf9) and bone morphogenetic protein 15 (bmp15) and their patterns of gene expression during the ovarian reproductive cycle in the European sea bass. Mol Cell Endocrinol 291:95–103
Khristi V, Chakravarthi VP, Singh P, Ghosh S, Pramanik A, Ratri A et al (2018) ESR2 regulates granulosa cell genes essential for follicle maturation and ovulation. Mol Cell Endocrinol 474:214–226. https://doi.org/10.1016/j.mce.2018.03.012
Kollonitsch J, Patchett AA, Marburg S, Maycock AL, Perkins LM, Doldouras GA et al (1978) Selective inhibitors of biosynthesis of aminergic neurotransmitters. Nature 274:906–908
Li B, Dewey CN (2011) RSEM: accurate transcript quantification from RNA-Seq data with or without a reference genome. BMC Bioinformatics 12:323
Li Y, Chia JM, Bartfai R, Christoffels A, Yue GH, Ding K et al (2004) Comparative analysis of the testis and ovary transcriptomes in zebrafish by combining experimental and computational tools. Comp Funct Genomics 5:403–418. https://doi.org/10.1002/cfg.418
Liang-Song Z (2011) Study on the large scale artificial propagation of Schizothorax o′connori. Freshwater Fisheries 41(05):88–91+95
Lubzens E, Young G, Bobe J, Cerdà J (2010) Oogenesis in teleosts: How fish eggs are formed. Gen Comp Endocrinol 165:367–389
Nishida M, Mackinnon R (2002) Structural basis of inward rectification: cytoplasmic pore of the G protein-gated inward rectifier GIRK1 at 1.8 A resolution. Cell 111:957–965. https://doi.org/10.1016/s0092-8674(02)01227-8
Norman AW, Mizwicki MT, Norman DP (2004) Steroid-hormone rapid actions, membrane receptors and a conformational ensemble model. Nat Rev Drug Discov 3:27–41. https://doi.org/10.1038/nrd1283
Selman K, Wallace RA, Cerdà J (2010) Bafilomycin A1 inhibits proteolytic cleavage and hydration but not yolk crystal disassembly or meiosis during maturation of sea bass oocytes. J Experiment Zoology 290(3):265–78
Sharpe RM, Millar MR, Maddocks S, Clegg J (1996) Regulatory mechanisms of oocyte maturation and ovulation[M]. The fish oocyte: From basic studies to biotechnological applications. Dordrecht: Springer Netherlands, p 323–347
Singh VK, Mangalam AK, Dwivedi S, Naik S (1998) Primer premier: program for design of degenerate primers from a protein sequence. Biotechniques 24:318–319. https://doi.org/10.2144/98242pf02
Stitzel ML, Seydoux G (2007) Regulation of the oocyte-to-zygote transition. Science 316:407–408. https://doi.org/10.1126/science.1138236
Suwa, K, Yamashita, M (2007) Regulatory mechanisms of oocyte maturation and ovulation. Fish Oocyte, 323–347
Tabak G, Keren Raifman T, Tsemakhovich V, Dascal N (2018) Ggamma Assists Gbeta to Activate GIRK1 by Relaxing Inhibitory Constraint. Biophys J 114:377a–378a
Tanaka T, Yamashita M (1995) Pre-MPF is absent in immature oocytes of fishes and amphibians except Xenopus. Dev Growth Different 37(4):387–393
Tao W, Yuan J, Zhou L, Sun L, Sun Y, Yang S et al (2013) Characterization of gonadal transcriptomes from Nile tilapia (Oreochromis niloticus) reveals differentially expressed genes. PLoS ONE 8:e63604. https://doi.org/10.1371/journal.pone.0063604
Wagner J, Coupland P, Browne HP, Lawley TD, Francis SC, Parkhill J (2016) Evaluation of PacBio sequencing for full-length bacterial 16S rRNA gene classification. BMC Microbiol 16:274. https://doi.org/10.1186/s12866-016-0891-4
Wallace RA, Greeley MS Jr, Mcpherson R (1992) Analytical and experimental studies on the relationship between Na+, K+, and water uptake during volume increases associated with Fundulus oocyte maturation in vitro. J Comp Physiol B 162:241–248. https://doi.org/10.1007/BF00357530
Wallace, RA, Kelly, S (1981) Cellular and Dynamic Aspects of Oocyte Growth in Teleosts. Am Zool, 325–343. https://doi.org/10.1093/icb/21.2.325
Watanabe WO, Kuo CM (2010) Water and ion balance in hydrating oocytes of the grey mullet, Mugil cephalus (L.), during hormone-induced final maturation. J Fish Biol 28:425–437
Wickman K, Clapham DE (1995) Ion channel regulation by G proteins. Physiol Rev 75:865–885. https://doi.org/10.1152/physrev.1995.75.4.865
Wu J, Xiong S, Jing J, Chen X, Wang W, Gui JF et al (2015) Comparative Transcriptome Analysis of Differentially Expressed Genes and Signaling Pathways between XY and YY Testis in Yellow Catfish. PLoS One 10(8):e0134626
Xiaotian, Chang, And, Reynaldo, Patiño And et al (2000) Hormonal Regulation and Cellular Distribution of Connexin 32.2 and Connexin 32.7 RNAs in the Ovary of Atlantic Croaker. General Comparative Endocrinol 120(2):146–156
Xie C, Mao X, Huang J, Ding Y, Wu J, Dong S et al (2011) KOBAS 2.0: a web server for annotation and identification of enriched pathways and diseases. Nucleic Acids Res 39:W316-322. https://doi.org/10.1093/nar/gkr483
Yamashita and Masakane (2000) Toward Modeling of a General Mechanism of MPF Formation during Oocyte Maturation in Vertebrates. Zoological Ence 17:841–851
Yoshizaki, G, Pati?O, R, Thomas, P, Bolamba, D, Chang, X (2001) Effects of Maturation-Inducing Hormone on Heterologous Gap Junctional Coupling in Ovarian Follicles of Atlantic Croaker. Gen Comparative Endocrinol 124, 359-366 https://doi.org/10.1006/gcen.2001.7726
Young MD, Wakefield MJ, Smyth GK, Oshlack A (2010) Gene ontology analysis for RNA-seq: accounting for selection bias. Genome Biol 11:R14. https://doi.org/10.1186/gb-2010-11-2-r14
Zhou W, Zhang Y, Wen Y, Ji W, Zhou Y, Ji Y et al (2015) Analysis of the transcriptomic profilings of Mandarin fish (Siniperca chuatsi) infected with Flavobacterium columnare with an emphasis on immune responses. Fish Shellfish Immunol 43:111–119. https://doi.org/10.1016/j.fsi.2014.12.006
Funding
This research was funded by the China Agriculture Research System of Specialty Freshwater Fish (CARS-46), Key Research and Development Plan of Tibet of China (Grant Number: XZ202101ZY0003N) and the Special Fund for Agro-Scientific Research in the Public Interest of China (Grant Number: 201403012). The funding bodies had no roles in the design of the study, collection, analysis, and interpretation of data, nor in writing the manuscript.
Author information
Authors and Affiliations
Contributions
JSZ, ML and ZCL conceived and designed the experiments. RTL and SJS performed the experiments. ZCL, JSZ and HFX analyzed the data. JSZ wrote the paper. All authors read and approved the final manuscript.
Corresponding authors
Ethics declarations
Ethical Approval
All animal experiments were performed according to protocols and guidelines approved by the Institutional Animal Care and Use Committee of Tibet Academy of Agricultural and Animal Husbandry Sciences, China.
Competing interests
The authors declare that they have no competing interests.
Additional information
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Supplementary Information
Below is the link to the electronic supplementary material.
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
Zhou, J., Sun, S., Li, R. et al. Transcriptome analysis of Schizothorax oconnori (Cypriniformes: Cyprinidae) oocytes: The role of K+ in promoting yolk globule fusion and regulating oocyte maturation. Fish Physiol Biochem 50, 435–448 (2024). https://doi.org/10.1007/s10695-023-01272-8
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10695-023-01272-8