Skip to main content

Advertisement

SpringerLink
Log in

Transcriptomes of Testes at Different Developmental Stages in the Opsariichthys bidens Predict Key Genes for Testis Development and Spermatogenesis

  • Research
  • Published:
Marine Biotechnology Aims and scope Submit manuscript

Abstract

Testis development is a complex process involving multiple genes, and the molecular mechanisms underlying testis development in Opsariichthys bidens remain unclear. We performed transcriptome sequencing analysis on a total of 12 samples of testes from stages II, III, IV, and V of O. bidens and obtained a total of 79.52 Gb clean data, as well as 288,573 transcripts and 116,215 unigenes. Differential expression analysis showed that 22,857 differentially expressed genes (DEGs) were screened in six comparison groups (III vs. II, IV vs. II, V vs. II, IV vs. III, V vs. III, and V vs. IV). Kyoto Encyclopedia of Genes and Genomes enrichment analysis of DEGs showed that six comparison groups were significantly enriched for a total of 20 significantly up- or down-regulated pathways, including six pathways related to signal transduction, three pathways related to energy metabolism, five pathways related to disease, and two pathways related to ribosomes. Furthermore, our investigation revealed that DEGs were enriched in several important functional pathways, such as Huntington’s disease signaling pathway, TGF-β signaling pathway, and ribosome signaling pathway. Protein–protein interaction network analysis of DEGs identified 63 up-regulated hub genes, including 9 kinesin genes and 2 cytoplasmic dynein genes, and 39 down-regulated hub genes, including 13 ribosomal protein genes. This result contributes to the knowledge of spermatogenesis and testis development in O. bidens.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7
Fig. 8
Fig. 9
Fig. 10

Similar content being viewed by others

Data Availability

The data used to support to the findings of this study are available from the corresponding author upon reasonable request.

References

  • Bahamode PA, Mcmaster ME, Servos MR, Martyniuk CJ, Munkittrick KR (2016) Characterizing transcriptional networks in male rainbow darter (Etheostoma caeruleum) that regulate testis development over a complete reproductive cycle. Plos One 11

  • Berrebi P, Retif X, Fang F, Zhang CG (2006) Population structure and systematics of Opsariichthys bidens (Osteichthyes : Cyprinidae) in south-east China using a new nuclear marker: the introns (EPIC-PCR). Biol J Linn Soc 87:155–166

    Article  Google Scholar 

  • Bo L, Dewey CN (2011) RSEM: accurate transcript quantification from RNA-Seq data with or without a reference genome. BMC Bioinformatics 12:323–323

    Article  Google Scholar 

  • Boonanuntanasarn S, Jangprai A, Na-Nakorn U (2020) Transcriptomic analysis of female and male gonads in juvenile snakeskin gourami (Trichopodus pectoralis). Sci Rep 

  • Cai L, Chen J, Johnson D, Tu Z, Huang Y (2020) Effect of body length on swimming capability and vertical slot fishway design. Glob Ecol Conserv 22:e00990 

  • Chen BX, Yi SK, Wang WF, He Y, Huang Y, Gao ZX, Liu H, Wang WM, Wang HL (2017) Transcriptome comparison reveals insights into muscle response to hypoxia in blunt snout bream (Megalobrama amblycephala). Gene 624:6–13

    Article  CAS  PubMed  Google Scholar 

  • Chen H, Zhang J, Yan Y, Zhu C, Wang L, Fu S, Zuo F, Zhang G-W (2022) N6-methyladenosine RNA demethylase ALKBH5 is testis-specifically downregulated in hybrid male sterile dzo and is a target gene of bta-miR-200a. Theriogenology 187:51-57

  • Chen KJ, Tang Y, Liu DZ, Geng B, Liu XY (2020) A comparative study on the nutritional characteristics of male and female chinese hook snout carp (Opsariichthys bidens). Appl Ecol Environ Res 18:3651–3658

    Article  Google Scholar 

  • Chen S, Zhou Y, Chen Y, Gu J (2018a) fastp: an ultra-fast all-in-one FASTQ preprocessor. Bioinformatics 34:884–890

    Article  CAS  Google Scholar 

  • Chen W, Schmidt BV, He S (2018b) The potential colonization histories of Opsariichthys bidens (Cyprinidae) in China using Bayesian binary MCMC analysis. Gene 676:1–8

    Article  CAS  PubMed  Google Scholar 

  • Chin C-H, Chen S-H, Wu H-H et al (2014) cytoHubba: identifying hub objects and sub-networks from complex interactome. BMC Syst Biol 8

  • Coward K, Bromage NR, Hibbitt O, Parrington J (2002) Gamete physiology, fertilization and egg activation in teleost fish. Rev Fish Biol Fish 12:33–58

    Article  Google Scholar 

  • Crespo D, Assis LHC, Furmanek T, Bogerd J, Schulz RW (2016) Expression profiling identifies Sertoli and Leydig cell genes as Fsh targets in adult zebrafish testis. Mol Cell Endocrinol 437:237–251

    Article  CAS  PubMed  Google Scholar 

  • Danilova N, Sakamoto KM, Lin S (2008) Ribosomal protein S19 deficiency in zebrafish leads to developmental abnormalities and defective erythropoiesis through activation of p53 protein family. Blood 112:5228-5237

  • Difiglia M, Sapp E, Chase KO, Davies SW, Bates GP, Vonsattel JP, Aronin N (1997) Aggregation of huntingtin in neuronal intranuclear inclusions and dystrophic neurites in brain. Science 277:1990–1993

    Article  CAS  PubMed  Google Scholar 

  • Ding J, Liu C, Luo S, Zhang Y, Gao X, Wu X, Shen W, Zhu J (2020) Transcriptome and physiology analysis identify key metabolic changes in the liver of the large yellow croaker (Larimichthys crocea) in response to acute hypoxia. Ecotoxicol Environ Saf 189:109957

    Article  CAS  PubMed  Google Scholar 

  • Escudier E, Duquesnoy P, Papon JF, Amselem S (2009) Ciliary defects and genetics of primary ciliary dyskinesia. Paediatr Respir Rev 10:51-54

  • Eswarakumar VP, Lax I, Schlessinger J (2005) Cellular signaling by fibroblast growth factor receptors. Cytokine Growth Factor Rev 16:139–149

    Article  CAS  PubMed  Google Scholar 

  • Fang Y, Zong Q, He Z, Liu C, Wang Y-F (2021) Knockdown of RpL36 in testes impairs spermatogenesis in Drosophila melanogaster. Journal of Experimental Zoology Part B-Molecular and Developmental Evolution 336:417–430

    Article  CAS  PubMed  Google Scholar 

  • Fatima R (2011) Drosophila dynein intermediate chain gene, Dic61B, is required for spermatogenesis. PLoS One 6

  • Fu B, Zhou Y, Liu H, Yu X, Tong J (2021) Updated genome assembly of bighead carp (Hypophthalmichthys nobilis) and its differences between male and female on genomic, transcriptomic, and methylation level. Front genet 12

  • Funabiki H, Murray AW (2000) The Xenopus chromokinesin Xkid is essential for metaphase chromosome alignment and must be degraded to allow anaphase chromosome movement. Cell 102:411–424

    Article  CAS  PubMed  Google Scholar 

  • Gong Z-K, Wang S-J, Huang Y-Q, Zhao R-Q, Zhu Q-F, Lin W-Z (2014) Identification and validation of suitable reference genes for RT-qPCR analysis in mouse testis development. Mol Genet Genomics 289:1157–1169

    Article  CAS  PubMed  Google Scholar 

  • Grabherr MG, Haas BJ, Yassour M, Levin JZ, Thompson DA, Amit I, Adiconis X, Fan L, Raychowdhury R, Zeng Q, Chen Z, Mauceli E, Hacohen N, Gnirke A, Rhind N, Di Palma F, Birren BW, Nusbaum C, Lindblad-Toh K, Friedman N, Regev A (2011) Full-length transcriptome assembly from RNA-Seq data without a reference genome. Nat Biotechnol 29:644-U130

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Gray JP, Davis JW, Gopinathan L, Leas TL, Nugent CA, Vanden Heuvel JP (2006) The ribosomal protein rpL11 associates with and inhibits the transcriptional activity of peroxisome proliferator-activated receptor-alpha. Toxicol Sci 89:535–546

    Article  PubMed  Google Scholar 

  • Greenbaum MP, Iwamori N, Agno JE, Matzuk MM (2009) Mouse TEX14 is required for embryonic germ cell intercellular bridges but not female fertility. Biol Reprod 80:449–457

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Guo Y, Ha Y, Yao C, Chen Z, Hou J, Li Z, He Z (2015) Long-term culture and significant expansion of human Sertoli cells whilst maintaining stable global phenotype and AKT and SMAD1/5 activation. Cell Commun Signal 13

  • Hai Y, Sun M, Niu M, Yuan Q, Guo Y, Li Z, He Z (2015) BMP4 promotes human sertoli cell proliferation via Smad1/5 and ID2/3 pathway and its abnormality is associated with azoospermia. Discov Med 19:311-+

  • Han Y, Chen L, Guan L, He S (2014) Inverse PCR-based method for isolating novel SINEs from genome. Mol Biotechnol 56:296–304

    Article  CAS  PubMed  Google Scholar 

  • Hara-Yokoyama M, Kurihara H, Ichinose S, Matsuda H, Ichinose S, Kurosawa M, Tada N, Iwahara C, Terasawa K, Podyma-Inoue KA, Furukawa K, Iwabuchi K (2019) KIF11 as a potential marker of spermatogenesis within mouse seminiferous tubule cross-sections. J Histochem Cytochem 67:813–824

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hentrich C, Surrey T (2010) Microtubule organization by the antagonistic mitotic motors kinesin-5 and kinesin-14. J Cell Biol 189:465–480

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hong YH, Liu TM, Zhao HB, Xu HY, Wang WJ, Liu R, Chen TS, Deng JR, Gui JF (2004) Establishment of a normal medakafish spermatogonial cell line capable of sperm production in vitro. Proc Natl Acad Sci USA 101:8011–8016

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hu J, Zhang YQ, Liu XP, Wang RA, Jin Y, Xu RJ (2003) Expression and localization of Smad1, Smad2 and Smad4 proteins in rat testis during postnatal development. Asian J Androl 5:51–55

    CAS  PubMed  Google Scholar 

  • Huang Z, Ma A, Yang S, Liu X, Zhao T, Zhang J, Wang X-A, Sun Z, Liu Z, Xu R (2020) Transcriptome analysis and weighted gene co-expression network reveals potential genes responses to heat stress in turbot Scophthalmus maximus. Comp Biochem Physiol 33

  • Imami K, Milek M, Bogdanow B, Yasuda T, Kastelic N, Zauber H, Ishihama Y, Landthaler M, Selbach M (2018) Phosphorylation of the ribosomal protein RPL12/uL11 affects translation during mitosis. Mol Cell 72:84-+

  • Jia Y, Nan P, Zhang W, Wang F, Zhang R, Liang T, Ji X, Du Q, Chang Z (2018) Transcriptome analysis of three critical periods of ovarian development in Yellow River carp (Cyprinus carpio). Theriogenology 105:15–26

    Article  CAS  PubMed  Google Scholar 

  • Jiang H, Tang D, Gao X, Lin C, Feng B, Du C, Jin S, Zhu J (2021) Molecular cloning, characterisation and expression analysis of the vitellogenin genes vtgAo1 and vtgC during ovarian development in Chinese hook snout carp Opsariichthys bidens. Reprod Fertil Dev 33:455–465

    Article  CAS  PubMed  Google Scholar 

  • Johansson F, Radman P, Andersson J (2006) The relationship between ontogeny, morphology, and diet in the Chinese hook snout carp (Opsariichthys bidens). Ichthyol Res 53:63–69

    Article  Google Scholar 

  • Kleppe L, Edvardsen RB, Furmanek T, Andersson E, Skaftnesmo KO, Thyri Segafredo F, Wargelius A (2020) Transcriptomic analysis of dead end knockout testis reveals germ cell and gonadal somatic factors in Atlantic salmon. BMC Genom 21

  • Kubiczkova L, Sedlarikova L, Hajek R, Sevcikova S (2012) TGF-β – an excellent servant but a bad master. J Transl Med. https://doi.org/10.1186/1479-5876-10-183

  • Kuta A, Deng W, El-Kadi AM, Banks GT, Hafezparast M, Pfister KK, Fisher EMC (2010) Mouse cytoplasmic dynein intermediate chains: identification of new isoforms, alternative splicing and tissue distribution of transcripts. PLoS One 5

  • Leal MC, Cardoso ER, Nobrega RH, Batlouni SR, Bogerd J, Franca LR, Schulz RW (2009) Histological and stereological evaluation of zebrafish (Danio rerio) spermatogenesis with an emphasis on spermatogonial generations. Biol Reprod 81:177–187

    Article  CAS  PubMed  Google Scholar 

  • Li X, Ding X, Liu L, Yang P, Yao Z, Lei C, Chen H, Huang Y, Liu W (2021) Copy number variation of bovine DYNC1I2 gene is associated with body conformation traits in chinese beef cattle. Gene 146060–146060

  • Lin C, Tang D, Gao X, Jiang H, Du C, Zhu J (2021a) Molecular characterization, dynamic transcription, and potential function of KIF3A/KIF3B during spermiogenesis in Opsariichthys bidens. Gene 798

  • Lin JC (2015) Impacts of alternative splicing events on the differentiation of adipocytes. Int J Mol Sci 16:22169–22189

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lin X, Zhou D, Zhang X, Li G, Zhang Y, Huang C, Zhang Z, Tian C (2021b) A first insight into the gonad transcriptome of Hong Kong catfish (Clarias fuscus). Animals 11

  • Love MI, Huber W, Anders S (2014) Moderated estimation of fold change and dispersion for RNA-seq data with DESeq2. Genome Biol 15

  • Luo S, Gao X, Ding J, Liu C, Du C, Hou C, Zhu J, Lou B (2019) Transcriptome sequencing reveals the traits of spermatogenesis and testicular development in large yellow croaker (Larimichthys crocea). Genes 10

  • Ma D-D, Wang D-H, Yang W-X (2017) Kinesins in spermatogenesis. Biol Reprod 96:267–276

    Article  PubMed  Google Scholar 

  • Mageeney CM, Ware VC (2019) Specialized eRpL22 paralogue-specific ribosomes regulate specific mRNA translation in spermatogenesis in Drosophila melanogaster. Mol Biol Cell 30:2240–2253

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Makkapan W, Yoshizaki G, Tashiro M, Chotigeat W (2014) Expression profile of ribosomal protein L10a throughout gonadal development in rainbow trout (Oncorhynchus mykiss). Fish Physiol Biochem 40:1069–1081

    Article  CAS  PubMed  Google Scholar 

  • Mangiarini L, Sathasivam K, Seller M, Cozens B, Harper A, Hetherington C, Lawton M, Trottier Y, Lehrach H, Davies SW, Bates GP (1996) Exon 1 of the HD gene with an expanded CAG repeat is sufficient to cause a progressive neurological phenotype in transgenic mice. Cell 87:493–506

    Article  CAS  PubMed  Google Scholar 

  • Manning AL, Ganem NJ, Bakhoum SF, Wagenbach M, Wordeman L, Compton DA (2007) The kinesin-13 proteins Kif2a, Kif2b, and Kif2c/MCAK have distinct roles during mitosis in human cells. Mol Biol Cell 18:2970–2979

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Mazumdar M, Sundareshan S, Misteli T (2004) Human chromokinesin KIF4A functions in chromosome condensation and segregation. J Cell Biol 166:613–620

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Miles DC, Wakeling SI, Stringer JM, Van Den Bergen JA, Wilhelm D, Sinclair AH, Western PS (2013) Signaling through the TGF beta-activin receptors ALK4/5/7 regulates testis formation and male germ cell development. Plos One 8

  • Pangas SA, Li X, Umans L, Zwijsen A, Huylebroeck D, Gutierrez C, Wang D, Martin JF, Jamin SP, Behringer RR, Robertson EJ, Matzuk MM (2008) Conditional deletion of Smad1 and Smad5 in somatic cells of male and female gonads leads to metastatic tumor development in mice. Mol Cell Biol 28:248–257

    Article  CAS  PubMed  Google Scholar 

  • Perdices A, Sayanda D, Coelho MM (2005) Mitochondrial diversity of Opsariichthys bidens (Teleostei, Cyprinidae) in three Chinese drainages. Mol Phylogen Evol 37:920–927

    Article  CAS  Google Scholar 

  • Pertea G, Huang XQ, Liang F, Antonescu V, Sultana R, Karamycheva S, Lee Y, White J, Cheung F, Parvizi B, Tsai J, Quackenbush J (2003) TIGR gene indices clustering tools (TGICL): a software system for fast clustering of large EST datasets. Bioinformatics 19:651–652

    Article  CAS  PubMed  Google Scholar 

  • Rao DS, Chang JC, Kumar PD, Mizukami I, Smithson GM, Bradley SV, Parlow, B.a.F. & Ross, T.S. (2001) Huntingtin interacting protein 1 is a clathrin coat binding protein required for differentiation of late spermatogenic progenitors. Mol Cell Biol 21:7796–7806

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Rim HJ, Kim KH, Joo KH (1996) Classification and host specificity of Metagonimus spp. from Korean freshwater fish. Korean J Parasitol 34:7–14

    Article  CAS  PubMed  Google Scholar 

  • Rizk RS, Bohannon KP, Wetzel LA, Powers J, Shaw SL, Walczak CE (2009) MCAK and paclitaxel have differential effects on spindle microtubule organization and dynamics. Mol Biol Cell 20:1639–1651

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Roy A, Basak R, Rai U (2017) De novo sequencing and comparative analysis of testicular transcriptome from different reproductive phases in freshwater spotted snakehead Channa punctatus. Plos One 12

  • Santos EM, Workman VL, Paull GC, Filby AL, Van Look KJW, Kille P, Tyler CR (2007) Molecular basis of sex and reproductive status in breeding zebrafish. Physiol Genomics 30:111–122

    Article  CAS  PubMed  Google Scholar 

  • Sato Y, Yano S, Ewis AA, Nakahori Y (2011) SRY interacts with ribosomal proteins S7 and L13a in nuclear speckles. Cell Biol Int 35:449–452

    Article  CAS  PubMed  Google Scholar 

  • Schulz RW, De Franca LR, Lareyre J-J, Legac F, Chiarini-Garcia H, Nobrega RH, Miura T (2010) Spermatogenesis in fish. Gen Comp Endocrinol 165:390–411

    Article  CAS  PubMed  Google Scholar 

  • Shannon P, Markiel A, Ozier O, Baliga NS, Wang JT, Ramage D, Amin N, Schwikowski B, Ideker T (2003) Cytoscape: a software environment for integrated models of biomolecular interaction networks. Genome Res 13:2498–2504

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Shen F, Long Y, Li F, Ge G, Song G, Li Q, Qiao Z, Cui Z (2020) De novo transcriptome assembly and sex-biased gene expression in the gonads of Amur catfish (Silurus asotus). Genomics 112:2603–2614

    Article  CAS  PubMed  Google Scholar 

  • Sieff CA, Lodish HF (2007) Pathogenesis of the erythroid failure in diamond blackfan anemia. Blood 110:424

  • Simao FA, Waterhouse RM, Ioannidis P, Kriventseva EV, Zdobnov EM (2015) BUSCO: assessing genome assembly and annotation completeness with single-copy orthologs. Bioinformatics 31:3210–3212

    Article  CAS  PubMed  Google Scholar 

  • Stromqvist M, Tooke N, Brunstrom B (2010) DNA methylation levels in the 5’ flanking region of the vitellogenin I gene in liver and brain of adult zebrafish (Danio rerio)-Sex and tissue differences and effects of 17 alpha-ethinylestradiol exposure. Aquat Toxicol 98:275–281

    Article  CAS  PubMed  Google Scholar 

  • Sui X-Y, Yan Y-Z, Chen Y-F (2012) Age, growth, and reproduction of Opsariichthys bidens (Cyprinidae) from the Qingyi River at Huangshan Mountain, China. Zool Stud 51:476–483

    Google Scholar 

  • Svingen T, Letting H, Hadrup N, Hass U, Vinggaard AM (2015) Selection of reference genes for quantitative RT-PCR (RT-qPCR) analysis of rat tissues under physiological and toxicological conditions. PEERJ 3

  • Tanenbaum ME, Macurek L, Van Der Vaart B, Galli M, Akhmanova A, Medema RH (2011) A complex of Kit18b and MCAK promotes microtubule depolymerization and is negatively regulated by aurora kinases. Curr Biol 21:1356–1365

    Article  CAS  PubMed  Google Scholar 

  • Tang D, Gao X, Lin C, Feng B, Hou C, Zhu J, Wang J (2020) Cytological features of spermatogenesis in Opsariichthys bidens (Teleostei, Cyprinidae). Anim Reprod Sci 222

  • Turner N, Grose R (2010) Fibroblast growth factor signalling: from development to cancer. Nat Rev Cancer 10:116–129. https://doi.org/10.1038/nrc2780

    Article  CAS  PubMed  Google Scholar 

  • Wang C-H, Wang L-K, Wu C-C, Chen M-L, Lee M-C, Lin Y-Y, Tsai F-M (2019) The ribosomal protein RPLP0 mediates PLAAT4-induced cell cycle arrest and cell apoptosis. CELL BIOCHEMISTRY AND BIOPHYSICS 77:253–260

    Article  CAS  Google Scholar 

  • Wang M, Chen X, Wu Y, Zheng Q, Chen W, Yan Y, Luan X, Shen C, Fang J, Zheng B, Yu J (2020) RpS13 controls the homeostasis of germline stem cell niche through Rho1-mediated signals in theDrosophilatestis. Cell Prolif 53

  • Wu J, Xiong S, Jing J, Chen X, Wang W, Gui J-F, Mei J (2015) Comparative transcriptome analysis of differentially expressed genes and signaling pathways between XY and YY testis in yellow catfish. Plos One 10

  • Wurm JP, Meyer B, Bahr U, Held M, Frolow O, Koetter P, Engels JW, Heckel A, Karas M, Entian K-D, Woehnert J (2010) The ribosome assembly factor Nep1 responsible for Bowen-Conradi syndrome is a pseudouridine-N1-specific methyltransferase. Nucleic Acids Res 38:2387–2398

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Xie C, Mao X, Huang J, Ding Y, Wu J, Dong S, Kong L, Gao G, Li C-Y, Wei L (2011) KOBAS 2.0: a web server for annotation and identification of enriched pathways and diseases. Nucleic Acids Res 39:W316–W322

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Yan J, Zhang H, Liu Y, Zhao F, Zhu S, Xie C, Tang T-S, Guo C (2016) Germline deletion of huntingtin causes male infertility and arrested spermiogenesis in mice. J Cell Sci 129:492–501

    Article  CAS  PubMed  Google Scholar 

  • Yang C, Zhang Y, Lin S, Liu Y, Li W (2021) Correction for: suppressing the KIF20A/NUAK1/Nrf2/GPX4 signaling pathway induces ferroptosis and enhances the sensitivity of colorectal cancer to oxaliplatin. Aging, undefined. https://doi.org/10.18632/aging.202774

  • Young MD, Wakefield MJ, Smyth GK, Oshlack A (2010) Gene ontology analysis for RNA-seq: accounting for selection bias. Genome Biol 11:R14–R14

    Article  PubMed  PubMed Central  Google Scholar 

  • Yu J, Luan X, Yan Y, Qiao C, Liu Y, Zhao D, Xie B, Zheng Q, Wang M, Chen W, Shen C, He Z, Hu X, Huang X, Li H, Chen B, Zheng B, Chen X, Fang J (2019) Small ribonucleoprotein particle protein SmD3 governs the homeostasis of germline stem cells and the crosstalk between the spliceosome and ribosome signals in Drosophila. FASEB J 33:8125–8137

    Article  CAS  PubMed  Google Scholar 

  • Zhang DF, Wang W, Liu QF (2017) Length-weight relationships of four fish species from the Niulan River, China. J Appl Ichthyol 33:592–593

    Article  Google Scholar 

  • Zhang Q-Q, Li F-G, Qin B, Chen J, Jiang X-Y, Zou S-M (2015) Functional conservation and divergence of duplicated fibroblast growth factor receptor 1 (fgfr1) genes in blunt snout bream (Megalobrama amblycephala). Gene 573:225–232

    Article  CAS  PubMed  Google Scholar 

  • Zhang Z, Wang Y, Jiang Y, Lin P, Jia X, Zou Z (2007) Ribosomal protein L24 is differentially expressed in ovary and testis of the marine shrimp Marsupenaeus japonicus. Comp Biochem Physiol B-Biochem Mol Biol 147:466–474

    Article  CAS  PubMed  Google Scholar 

  • Zhao X, Yu H, Kong L, Li Q (2016) Gene co-expression network analysis reveals the correlation patterns among genes in euryhaline adaptation of crassostrea gigas. Mar Biotechnol (NY) 18:535–544

    Article  CAS  PubMed  Google Scholar 

  • Zhao Y, Li M-C, Konate MM, Chen L, Das B, Karlovich C, Williams PM, Evrard YA, Doroshow JH, Mcshane LM (2021) TPM, FPKM, or normalized counts? A comparative study of quantification measures for the analysis of RNA-seq data from the NCI patient-derived models repository. J Transl Med 19

  • Zheng Y, Yuan J, Meng S, Chen J, Gu Z (2019) Testicular transcriptome alterations in zebrafish (Danio rerio) exposure to 17 beta-estradiol. Chemosphere 218:14–25

    Article  CAS  PubMed  Google Scholar 

Download references

Funding

This research was funded by the Ningbo Science and Technology Plan Projects (2019C10057), the Science and Technology Planning Programs of Zhejiang Province (2020C02014, 2016C32062), the National Natural Science Foundation of China (NSFC)-Zhejiang Joint Fund for the Integration of Industrialisation and Informatisation (U1809212) and the Collaborative Innovation Center for Zhejiang Marine High-efficiency and Healthy Aquaculture, and was sponsored by the K. C. Wong Magna Fund in Ningbo University.

Author information

Author notes

  1. Jie Ding and Daojun Tang are the co-first authors.

Authors and Affiliations

  1. Key Laboratory of Applied Marine Biotechnology of Ministry of Education, College of Marine Sciences, Ningbo University, Ningbo, 315832, Zhejiang, China

    Jie Ding, Daojun Tang, Yibo Zhang, Xinming Gao, Chen Du, Shan Jin & Junquan Zhu

  2. Ningbo Academy of Oceanology and Fishery, Ningbo, 315103, Zhejiang, China

    Jie Ding, Yibo Zhang & Weiliang Shen

Authors
  1. Jie Ding
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Daojun Tang
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Yibo Zhang
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Xinming Gao
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Chen Du
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Weiliang Shen
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Shan Jin
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Junquan Zhu
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

JQZ conceived and supervised the study. JD and DJT designed and managed the experiments and wrote the manuscript. YBZ performed the analysis and designed the charts and tables. YBZ, JD, CD, WLS, and JQZ conducted the experiments. All authors have read and approved the manuscript.

Corresponding author

Correspondence to Junquan Zhu.

Ethics declarations

Competing interests

The authors declare no competing interests.

Ethics Approval

The principles and procedures of the sampling methods were in strict accordance with the requirements of the Governing Regulation for the Use of Experimental Animals in Zhejiang Province (Zhejiang Provincial Government Order No. 263, released in 17 August 2009, effective from 1 October 2010) and approved by the Animal Care and Use Committee of Ningbo University.

Conflict of Interest

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.

Supplementary Information

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.

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Ding, J., Tang, D., Zhang, Y. et al. Transcriptomes of Testes at Different Developmental Stages in the Opsariichthys bidens Predict Key Genes for Testis Development and Spermatogenesis. Mar Biotechnol 25, 123–139 (2023). https://doi.org/10.1007/s10126-022-10186-0

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10126-022-10186-0

Keywords

Search

Navigation