Skip to main content

Advertisement

SpringerLink
Log in

Genetic regulation of male sexual development in the oriental river prawn Macrobrachium nipponense during reproductive vs. non-reproductive season

  • Published:
Aquaculture International Aims and scope Submit manuscript

Abstract

Rapid gonad development is an important concern in the Macrobrachium nipponense aquaculture industry. The process of sexual differentiation and development is influenced by environmental factors, including water temperature and illumination time. In this study, we aimed to identify the key metabolites and genes from the androgenic gland, in response to different water temperatures and illumination times based on the integrated metabolomic and transcriptomic analysis of the androgenic gland during the reproductive vs. non-reproductive seasons. Histological observations revealed that the division of the androgenic gland in the reproductive season is more active than that in the non-reproductive season. The metabolic profiling analysis revealed that glycerophospholipid metabolism and sphingolipid metabolism represented the most enriched metabolic pathways of differentially expressed metabolites (DEMs). Transcriptome profiling analysis revealed that phagosome, spliceosome, RNA degradation, ribosome biogenesis in eukaryotes, and oxidative phosphorylation represented the main enriched metabolic pathways of differentially expressed genes (DEGs). A total of 14 DEGs from these metabolic pathways were considered as strong candidate genes involved in the male sexual development in M. nipponense, based on the expression difference between the reproductive vs. non-reproductive seasons. qPCR verifications of these 14 DEGs indicate the accuracy of the RNA-Seq. In addition, eight genes out of 14 DEGs showed high expression levels in the testis or/and androgenic gland. Predicting these eight genes may play an essential role in male sexual development of M. nipponense. The results of this study contribute to our knowledge of sexual development in male M. nipponense, as well as other crustacean species.

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.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7

Similar content being viewed by others

Data availability

The reads of M. nipponense transcriptome were submitted to NCBI with the accession number of SRX5805440-SRX5805445. The data of M. nipponense were submitted to MetaboLights with the accession number of MTBLS1025.

Code availability

Not applicable.

References

  • Ashburner M, Ball CA, Blake JA et al (2000) Gene ontology: tool for the unification of biology. Nat Genet 25(1):25–29

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Beggs JD (1993) Yeast protein factors involved in pre-mRNA splicing. Mol Biol Rep 18:99–103

    Article  CAS  PubMed  Google Scholar 

  • Bell AA, Stipanovic RD, O’Brien DH, Fryxellc PA (1978) Sesquiterpenoid aldehyde quinones and derivatives in pigment glands of Gossypium. Phytochemistry 17(8):1297–1305

    Article  CAS  Google Scholar 

  • Benjamini Y, Drai D, Elmer G et al (2001) Controlling the false discovery rate in behavior genetics research. Behav Brain Res 125(1–2):279–284

    Article  CAS  PubMed  Google Scholar 

  • Bjork P, Bauren G, Jin S et al (2002) A novel conserved RNA-binding domain protein, RBD-1, is essential for ribosome biogenesis. Mol Biol Cell 13:3683–3695

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Blomberg LA, Schreier LL, Talbot NC (2007) Expression analysis of pluripotency factors in the undifferentiated porcine inner cell mass and epiblast during in vitro culture. Mol Reprod Dev 75(3):450–463

    Article  CAS  Google Scholar 

  • Cheng D, Côté J, Shaaban S, Bedford MT (2007) The arginine methyltransferase CARM1 regulates the coupling of transcription and mRNA processing. Mol Cell 25:71–83

    Article  CAS  PubMed  Google Scholar 

  • Coiras M, Montes M, Montanuy I et al (2013) Transcription elongation regulator 1 (TCERG1) regulates competent RNA polymerase II-mediated elongation of HIV-1 transcription and facilitates efficient viral replication. Retrovirology 10:124

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Defronzo RA, Hissa MN, Garber AJ et al (2009) The efficacy and safety of saxagliptin when added to metformin therapy in patients with inadequately controlled Type 2 diabetes with metformin alone. Diabetes Care 32(9):1649–1655

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Dennis EA, Rhee SG, Billah MM, Hannun YA (1991) Role of phospholipase in generating lipid second messengers in signal transduction. FASEB J 5:2068–2077

    Article  CAS  PubMed  Google Scholar 

  • Dimroth P, Kaim G, Matthey U (2000) Crucial role of the membrane potential for ATP synthesis by F(1)F(o) ATP synthases. J Exp Biol 203:51–59

    Article  CAS  PubMed  Google Scholar 

  • Dixon WL, ap Rees T (1980) Identification of the regulatory steps in glycolysis in potato tubers. Phytochemistry 19:1297–1301

    Article  CAS  Google Scholar 

  • Exton JH (1994) Phosphatidylcholine breakdown and signal transduction. Biochim Biophys Acta 1212:26–42

    Article  CAS  PubMed  Google Scholar 

  • Fu XD, Tom M (1990) Factor required for mammalian spliceosome assembly is localized to discrete regions in the nucleus. Nature 343:437–441

    Article  CAS  PubMed  Google Scholar 

  • Fu HT, Jiang SF, Xiong YW (2012) Current status and prospects of farming the giant river prawn (Macrobrachium rosenbergii) and the oriental river prawn (Macrobrachium nipponense) in china. Aquac Res 43:993–998

    Article  Google Scholar 

  • Goldstrohm AC, Greenleaf AL, Garcia-Blanco MA (2001) Co-transcriptional splicing of pre-messenger RNAs: considerations for the mechanism of alternative splicing. Gene 277:31–47

    Article  CAS  PubMed  Google Scholar 

  • Good JA, Ziegler WH, Parekh DB et al (1998) Protein kinase C isotypes controlled by phosphoinositide 3-kinase through the protein kinase PDK1. Science 281(5385):2042–2045

    Article  PubMed  Google Scholar 

  • Grabherr MG, Haas BJ, Yassour M et al (2011) Trinity: reconstructing a full-lengthtranscriptome without a genome from RNA-Seq data. Nat Biotechnol 29(7):644–652

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Guthrie C (1991) Messenger RNA splicing in yeast: clues as to why the spliceosome is a ribonucleoprotein. Science 253:157–163

    Article  CAS  PubMed  Google Scholar 

  • Hampton MB, Kettle AJ, Winterbourn CC (1998) Inside the neutrophil phagosome: oxidants, myeloperoxidase, and bacterial killing. Blood 92(9):3007–3017

    Article  CAS  PubMed  Google Scholar 

  • Houseley J, Tollervey D (2009) The many pathways of RNA degradation. Cell 136(4):763–776

    Article  CAS  PubMed  Google Scholar 

  • Hsu CL, Stevens A (1993) Yeast cells lacking 5’ 3’ exoribonuclease 1 contain mRNA species that are poly(A) deficient and partially lack the 5’ cap structure. Mol Cell Biol 13:4826–4835

    CAS  PubMed  PubMed Central  Google Scholar 

  • Hu YN, Fu HT, Qiao H et al (2018) Validation and evaluation of reference genes for Quantitative real-time PCR in Macrobrachium nipponense. Int J Mol Sci 19(8):2258

    Article  CAS  PubMed Central  Google Scholar 

  • Huang XS, Ye HH, Huang HY et al (2014) An insulin-like androgenic gland hormone gene in the mud crab, Scylla paramamosain, extensively expressed and involved in the processes of growth and female reproduction. Gen Comp Endocrinol 204:229–238

    Article  CAS  PubMed  Google Scholar 

  • Inoguchi T, Li P, Umeda F (2000) High glucose level and free fatty acid stimulate reactive oxygen species production through protein kinase C-dependent activation of NAD(P)H Oxidase in Culutred Vascular Cells. Diabetes 49(11):1939–1945

    Article  CAS  PubMed  Google Scholar 

  • Jin SB, Fu HT, Zhou Q et al (2013) Transcriptome analysis of androgenic gland for discovery of novel genes from the oriental river prawn, Macrobrachium nipponense, using Illumina Hiseq 2000. PLoS ONE 8:e76840

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Jin SB, Fu HT, Sun SM et al (2018) iTRAQ-based quantitative proteomic analysis of the androgenic glands of the oriental river prawn, Macrobrachium nipponense, during nonreproductive and reproductive seasons. Comp Biochem Physiol Part D Genomics Proteomics 26:50–57

    Article  CAS  PubMed  Google Scholar 

  • Jin SB, Hu YN, Fu HT et al (2019a) Potential functions of Gem-associated protein 2-like isoform X1 in the oriental river prawn Macrobrachium nipponense: cloning, qPCR, in situ hybridization, and RNAi analysis. Int J Mol Sci 20:3995

    Article  CAS  PubMed Central  Google Scholar 

  • Jin SB, Hu YN, Fu HT et al (2019b) Identification of potentially novel functions of DNA polymerase zeta catalytic subunit in oriental river prawn, Macrobrachium nipoponense: Cloning, qPCR, in situ hybridization and RNAi analysis. 3Biotech 9:330

    Google Scholar 

  • Jin SB, Hu YN, Fu HT et al (2020) Analysis of testis metabolome and transcriptome from the oriental river prawn (Macrobrachium nipponense) in response to different temperatures and illumination times. Comp Biochem Physiol Part D Genomics Proteomics 34:100662

    Article  CAS  PubMed  Google Scholar 

  • Jin SB, Hu YN, Fu HT et al (2021a) Identification and characterization of the succinate dehydrogenase complex iron sulfur subunit B gene in the oriental river prawn Macrobrachium Nipponense. Front Genet 12:698318

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Jin SB, Fu Y, Hu YN et al (2021b) Identification of candidate genes from androgenic gland in Macrobrachium nipponense regulated by eyestalk ablation. Sci Rep 11:1985

    Article  CAS  Google Scholar 

  • Jin SB, Fu Y, Hu YN et al (2021c) Transcriptome profiling analysis of the testis after eyestalk ablation for selection of the candidate genes involved in the male sexual development in Macrobrachium nipponense. Front Genet 12:675928

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Jin SB, Zhao J, Bjork P et al (2002) Mrd1p is required for processing of pre-rRNA and for maintenance of steady-state levels of 40 S ribosomal subunits in yeast. J Biol Chem 277:18431–18439

    Article  CAS  PubMed  Google Scholar 

  • Kanehisa M, Araki M, Goto S et al (2008) KEGG for linking genomes to life and the environment. Nucleic Acids Res 36:480–484

    Article  CAS  Google Scholar 

  • Kobr MJ, Beevers H (1971) Gluconeogenesis in the castor bean endosperm. Plant Physiol 47:48–52

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lacava J, Houseley J, Saveanu C et al (2005) RNA degradation by the exosome is promoted by a nuclear polyadenylation complex. Cell 121(5):713–724

    Article  CAS  PubMed  Google Scholar 

  • Leslie LH, Valentine AA (2015) 5-DMRT1 and the road to masculinity. Sertoli Cell Biology. Second edn. Academic Press pp 123–174

  • Li SH, Li FH, Sun Z, Xiang JH (2012) Two spliced variants of insulin-like androgenic gland hormone gene in the Chinese shrimp Fenneropenaeus Chinensis. Gen Comp Endocrinol 177(2):246–255

    Article  CAS  PubMed  Google Scholar 

  • Lin KT, Lu RM, Tarn WY (2004) The WW domain-containing proteins interact with the early spliceosome and participate in pre-mRNA splicing in vivo. Mol Cell Biol 24:9176–9185

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Liu F, Shi W, Ye H et al (2021) RNAi reveals role of insulin-like androgenic gland hormone 2 (IAG2) in sexual differentiation and growth in Hermaphrodite Shrimp. Front Mar Sci 8:666763

    Article  Google Scholar 

  • Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2−∆∆CT method. Methods 25:402–408

    Article  CAS  PubMed  Google Scholar 

  • Lunt DH, Zhang DX, Szymura JM, Hewitt GM (2019) The insect cytochrome oxidase I gene: evolutionary patterns and conserved primers for phylogenetic studies. Insect Mol Biol 5(3):153–165

    Article  Google Scholar 

  • Ma XK, Liu XZ, Wen HS et al (2006) Histological observation on gonadal sex differentiation in Cynoglossus semilaevis Günther. Mar Fish Res 27(2):55–61

    Google Scholar 

  • Ma KY, Li JL, Qiu GF (2016) Identification of putative regulatory region of insulin-like androgenic gland hormone gene (IAG) in the prawn Macrobrachium nipponense and proteins that interact with IAG by using yeast two-hybrid system. Gen Comp Endocrinol 229:112–118

    Article  CAS  PubMed  Google Scholar 

  • Meagher EA, Fitzgerald GA (1993) The molecular basis of eicosanoid action. Hypertens Pregnancy 12:439–451

    Article  CAS  Google Scholar 

  • Morales A, Lee H, Goñi FM et al (2007) Sphingolipids and cell death. Apoptosis 12(5):923–939

    Article  CAS  PubMed  Google Scholar 

  • Moser MJ, Holley WR, Chatterjee A, Mian IS (1998) The proofreading domain of Escherichia coli DNA polymerase I and other DNA and/or RNA exonuclease domains. Nucleic Acids Res 25(24):5110–5118

    Article  Google Scholar 

  • Om AD, Sharif S, Jasmani S, Sung YY, Bolong AA (2015) Molecular characteristic ofgiant grouper (Epinephelus Lanceolatus) Vitellogenin. J Aquac Res Development 6(9):1000360

    Google Scholar 

  • Ortiz-Villanueva E, Navarro-Martín L, Jaumot J, et al (2017) Metabolic disruption of zebrafish (Danio rerio) embryos by bisphenol A. An integrated metabolomic and transcriptomic approach. Environ Pollut 231(Pt1): 22–36

  • Pearson JL, Robinson TJ, Muñoz MJ et al (2008) Identification of the cellular targets of the transcription factor TCERG1 reveals a prevalent role in mRNA processing. J Biol Chem 283:7949–7961

    Article  CAS  PubMed  Google Scholar 

  • Rosen O, Manor R, Weil S et al (2010) A sexual shift induced by silencing of a single insulin-like gene in crayfish: ovarian upregulation and testicular degeneration. PLoS ONE 5:e15281

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Rosenstock J, Aguilar-Salinas C, Klein E et al (2009) Effect of saxagliptin monotherapy in treatment-naïve patients with type 2 diabetes. Curr Med Res Opin 25(10):2401–2411

    Article  CAS  PubMed  Google Scholar 

  • Ruby SW, Abelson J (1991) Pre-mRNA splicing in yeast. Trends Genet 7:79–85

    Article  CAS  PubMed  Google Scholar 

  • Ruffner HP, Hawker JS (1977) Control of glycolysis in Vitis vinifera. Phytochemistry 16:1171–1175

    Article  CAS  Google Scholar 

  • Sagi A, Cohen D, Wax Y (1986) Production of Macrobrachium rosenbetgii in momosex population: yield characterises under intensive monoculture conditions in cages. Aquaculture 51(3–4):265–275

    Article  Google Scholar 

  • Sagi A, Cohen D, Milner Y (1990) Effect of androgenic gland ablation on morphotypic differentiation and sexual characteristics of male freshwater prawns, Macrobrachium rosenbergii. Gen Comp Endocr 77:15–22

    Article  CAS  PubMed  Google Scholar 

  • Saijou E, Fujiwara T, Suzaki T et al (2004) RBD-1, a nucleolar RNA-binding protein, is essential for Caenorhabditis elegans early development through 18S ribosomal RNA processing. Nucleic Acids Res 32:1028–1036

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sánchez-Alvarez M, Goldstrohm AC, Garcia-Blanco MA, Suñé C (2006) Human transcription elongation factor CA150 localizes to splicing factor-rich nuclear speckles and assembles transcription and splicing components into complexes through its amino and carboxyl regions. Mol Cell Biol 26:4998–5014

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sánchez-Alvarez M, Montes M, Sánchez-Hernández N et al (2010) Differential effects of sumoylation on transcription and alternative splicing by transcription elongation regulator 1 (TCERG1). J Biol Chem 285:15220–15233

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • ShangGuan BM, Liu ZZ, Li SQ (1991) Histological studies on ovarian development in Scylla serrata. J Fish China 15(2):96–103

    Google Scholar 

  • Spiegel S, Merrill AH (1996) Sphingolipid metabolism 622 and cell growth regulation. FASEB J 10(12):1388–1397

    Article  CAS  PubMed  Google Scholar 

  • Sunnucks P, Hales DF (1996) Numerous transposed sequences of mitochondrial cytochrome oxidase I-II in aphids of the genus Sitobion (Hemiptera: Aphididae). Mol Biol Evol 13(3):510–524

    Article  CAS  PubMed  Google Scholar 

  • Supriya B, Praveen B, Rajeeb S (2015) Nucleolar protein 4-like has a complex expression pattern in zebrafish embryos. Int J Dev Biol 52:1–3

    Google Scholar 

  • Tatusov RL, Fedorova ND, Jackson JD et al (2003) The COG database: an updated version includes eukaryotes. BMC Bioinformatics 4(1):41

    Article  PubMed  PubMed Central  Google Scholar 

  • Taylor SKB, Minhas MH, Tong J et al (2021) C. elegans electrotaxis behavior is modulated by heat shock response and unfolded protein response signaling pathways. Sci Rep 11:3115

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ventura T, Manor R, Aflalo ED et al (2009) Temporal silencing of an androgenic gland-specific insulin-like gene affecting phenotypical gender differences and spermatogenesis. Endocrinology 150:1278–1286

    Article  CAS  PubMed  Google Scholar 

  • Ventura T, Manor R, Aflalo ED et al (2011) Expression of an androgenic gland-specific insulin-like peptide during the course of prawn sexual and morphotypic differentiation. ISRN Endocrinol 2011:476283

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ventura T, Manor R, Aflalo ED et al (2012) Timing sexual differentiation: full functional sex reversal achieved through silencing of a single insulin-like gene in the prawn Macrobrachium Rosenbergii. Biol Reprod 86:90

    Article  CAS  PubMed  Google Scholar 

  • Vijayraghavan U, Company M, Abelson J (1989) Isolation and characterization of pre-mRNA splicing mutants of S. cerevisiae. Genes Dev 3:1206–1216

    Article  CAS  PubMed  Google Scholar 

  • Wedekind C (2017) Demographic and genetic consequences of disturbed sex determination. Philos Trans R Soc Lond B Biol Sci 372(1729):20160326

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Will CL, Lührmann R (2011) Spliceosome structure and function. Csh Perspect Biol 3(7):21441581

    Google Scholar 

  • Zhang YP, Fu HT, Qiao H et al (2013) Molecular cloning and expression analysis of transformer-2 gene during development in Macrobrachium nipponense (de Haan 1849). J World Aquacult Soc 44(3):338–349

    Article  CAS  Google Scholar 

  • Zhang XL, Cui LF, Li SM et al (2020) Bureau of Fisheries, Ministry of Agriculture, P.R.C. Fisheries economic statistics. In: China Fishery Yearbook. China Fishery Statistical Yearbook. Beijing China Agricultural Press 24.

  • Zhou TT, Wang W, Wang CG et al (2021) Insulin-like androgenic gland hormone from the shrimp Fenneropenaeus merguiensis: expression, gene organization and transcript variants. Gene 782:145529

    Article  CAS  PubMed  Google Scholar 

Download references

Funding

This research was supported by grants from the National Key R&D Program of China (2018YFD0900201); Central Public-interest Scientific Institution Basal Research Fund CAFS (2021JBFM02; 2020TD36); Jiangsu Agricultural Industry Technology System; the China Agriculture Research System-48 (CARS-48); the New cultivar breeding Major Project of Jiangsu province (PZCZ201745). Thank you for the Jiangsu Province Platform for the Conservation and Utilization of Agricultural Germplasm.

Author information

Authors and Affiliations

  1. Key Laboratory of Freshwater Fisheries and Germplasm Resources Utilization, Ministry of Agriculture and Rural Affairs, Freshwater Fisheries Research Center, Chinese Academy of Fishery Sciences, Wuxi, 214081, People’s Republic of China

    Shubo Jin, Wenyi Zhang, Yiwei Xiong, Sufei Jiang, Hui Qiao, Yongsheng Gong, Yan Wu & Hongtuo Fu

Authors
  1. Shubo Jin
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Wenyi Zhang
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Yiwei Xiong
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Sufei Jiang
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Hui Qiao
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Yongsheng Gong
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Yan Wu
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Hongtuo Fu
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

S.J. designed and wrote the manuscript. W.Z. performed the qPCR analysis. S.J. and Y.X. provided the experimental prawns. H.Q. selected the differentially expressed metabolites. Y.G. selected the differentially expressed genes. Y.W. performed the histological observations. H.F. supervised the experiment.

Corresponding author

Correspondence to Hongtuo Fu.

Ethics declarations

Ethics approval

Permission was obtained from the Tai Lake Fishery Management Council and the committee of Freshwater Fisheries Research Center during the experimental programs. All experiments were performed in accordance with relevant guidelines and regulations.

Conflict of interest

The authors declare no competing interests.

Additional information

Handling Editor: Gavin Burnell

Publisher's note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Jin, S., Zhang, W., Xiong, Y. et al. Genetic regulation of male sexual development in the oriental river prawn Macrobrachium nipponense during reproductive vs. non-reproductive season. Aquacult Int 30, 2059–2079 (2022). https://doi.org/10.1007/s10499-022-00887-7

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10499-022-00887-7

Keywords

Search

Navigation