Skip to main content
SpringerLink
Log in

Identification and Characterization of Gene SpDMRT99B and Its Sex-Biased Expression Profile in the Mud Crab, Scylla paramamosain

  • Published:
Journal of Ocean University of China Aims and scope Submit manuscript

Abstract

The doublesex and mab-3 related transcription factor (DMRT) gene family is conserved from invertebrates to humans. The functions of DMRT are mainly involved in sex development and the formation of many tissues and organs. In this study, a DM (Doublesex/Mab-3)-domain gene was identified in the mud crab Scylla paramamosain, and was named SpDMRT99B because of its many similarities to arthropod DMRT99B and phylogenetically close relationship with arthropod DMRT99B. The cDNA of SpDMRT99B gene is 1249 bp in length, encoding 224 amino acids. From 254 bp to 928 bp there is a conserved DM domain. No transmembrane domain was identified. Through multiple amino acid alignment and phylogenetic tree analysis, the closest gene to SpDMRT99B is Eriocheir sinensis DMRT99B, followed by Macrobrachium rosenbergii and Drosophila melanogaster DMRT99B. The expressions of the gene were characterized in different tissues of female and male crabs during early development period of crab individuals, as well as in different development periods of gonads. The results showed that SpDMRT99B gene is significantly highly expressed in testis than in ovary and other tissues. The expression level of SpDMRT99B in testis at different stages is significantly higher than that in ovary, and it is particularly highly expressed in immature testis. In early developmental stages of larvae, the expressions of SpDMRT99B remain at a low level and reach a peak at zoea stage I when the body segments shape up. It is speculated that SpDMRT99B gene might be involved in the gonadal development process and somitogenesis of S. paramamosain.

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

Similar content being viewed by others

References

  • Abayed, F. A., Manor, R., Aflalo, E. D., and Sagi, A., 2019. Screening for Dmrt genes from embryo to mature Macrobrachium rosenbergii prawns. General and Comparative Endocrinology, 282: 113205.

    Article  Google Scholar 

  • Balciuniene, J., Bardwell, V. J., and Zarkower, D., 2006. Mice mutant in the DM domain gene Dmrt4 are viable and fertile but have polyovular follicles. Molecular and Cellular Biology, 26 (23): 8891–8984.

    Article  Google Scholar 

  • Bellefroid, E. J., Leclere, L., Saulnier, A., Keruzore, M., Sirakov, M., Vervoort, M., et al., 2013. Expanding roles for the evolutionarily conserved Dmrt sex transcriptional regulators during embryogenesis. Cellular and Molecular Life Sciences, 70: 3829–3845.

    Article  Google Scholar 

  • Brunner, B., Hornung, U., Shan, Z., Nanda, I., Kondo, M., Zend-Ajusch, E., et al., 2001. Genomic organization and expression of the doublesex-related gene cluster in vertebrates and detection of putative regulatory regions for DMRT1. Genomics, 77 (1–2): 8–17.

    Article  Google Scholar 

  • Chandler, J. C., Fitzgibbon, Q. P., Smith, G, Elizur, A., and Ventura, T., 2017. Y-linked iDmrt1 paralogue (iDMY) in the Eastern spiny lobster, Sagmariasus verreauxi: The first invertebrate sex-linked Dmrt. Developmental Biology, 430 (2): 337–345.

    Article  Google Scholar 

  • De Clercq, S., Keruzore, M., Desmaris, E., Pollart, C., Assimacopoulos, S., Preillon, J., et al., 2016. DMRT5 together with DMRT3 directly controls hippocampus development and neocortical area map formation. Cerebral Cortex, 28 (2): 493–509.

    Google Scholar 

  • Felsenstein, J., 1985. Confidence limits on phylogenies: An approach using the bootstrap. Evolution, 39: 783–791.

    Article  Google Scholar 

  • Fontana, J. R., and Crews, S. T., 2012. Transcriptome analysis of Drosophila CNS midline cells reveals diverse peptidergic properties and a role for castor in neuronal differentiation. Developmental Biology, 372: 131–142.

    Article  Google Scholar 

  • Galindo-Torres, P., Garcia-Gasca, A., Llera-Herrera, R., Escobedo-Fregoso, C., Abreu-Goodger, C., and Ibarra, A. M., 2018. Sex determination and differentiation genes in a functional hermaphrodite scallop, Nodipecten subnodosus. Marine Genomics, 37: 161–175.

    Article  Google Scholar 

  • Guan, G., Kobayashi, T., and Nagahama, Y., 2000. Sexually dimorphic expression of two types of DM (Doublesex/Mab-3)-domain genes in a teleost fish, the Tilapia (Oreochromis niloticus). Biochemical and Biophysical Research Communications, 272 (3): 662–666.

    Article  Google Scholar 

  • Guo, Y., Li, Q., Gao, S., Zhou, X., He, Y., Shang, X., et al., 2004. Molecular cloning, characterization, and expression in brain and gonad of Dmrt5 of zebrafish. Biochemical and Biophysical Research Communications, 324 (2): 569–575.

    Article  Google Scholar 

  • Henry, G. L., Davis, F. P., Picard, S., and Eddy, S. R., 2012. Cell type-specific genomics of Drosophila neurons. Nucleic Acids Research, 40 (19): 9691–9704.

    Article  Google Scholar 

  • Hong, C. S., Park, B. Y., and Saint-Jeannet, J. P., 2007. The function of Dmrt genes in vertebrate development: It is not just about sex. Developmental Biology, 310 (1): 1–9.

    Article  Google Scholar 

  • Jiang, Q., Lu, B., Wang, G., and Ye, H., 2020. Transcriptional inhibition of Sp-IAG by crustacean female sex hormone in the mud crab, Scylla paramamosain. International Journal of Molecular Sciences, 21 (15): 5300.

    Article  Google Scholar 

  • Jones, D. T., Taylor, W. R., and Thornton, J. M., 1992. The rapid generation of mutation data matrices from protein sequences. Computer Applications in the Biosciences, 8: 275–282.

    Google Scholar 

  • Kasahara, R., Aoki, F., and Suzuki, M. G., 2018. Deficiency in dmrt99B ortholog causes behavioral abnormalities in the silkworm, Bombyx mori. Applied Entomology and Zoology, 53 (3): 381–393.

    Article  Google Scholar 

  • Kato, Y., Kobayashi, K., Oda, S., Colbourn, J. K., Tatarazako, N., Watanabe, H., et al., 2008. Molecular cloning and sexually dimorphic expression of DM-domain genes in Daphnia magna. Genomics, 91 (1): 94–101.

    Article  Google Scholar 

  • Kato, Y., Kobayashi, K., Watanabe, H., and Iguchi, T., 2011. Environmental sex determination in the branchiopod crustacean Daphnia magna: Deep conservation of a doublesex gene in the sex-determining pathway. PLoS Genetics, 7: e1001345.

    Article  Google Scholar 

  • Kim, S., Kettlewell, J. R., Anderson, R. C., Bardwell, V. J., and Zarkower, D., 2003. Sexually dimorphic expression of multiple doublesex-related genes in the embryonic mouse gonad. Gene Expression Patterns, 3 (1): 77–82.

    Article  Google Scholar 

  • Kondo, M., Froschauer, A., Kitano, A., Nanda, I., Hornung, U., Volff, J., et al., 2002. Molecular cloning and characterization of DMRT genes from the medaka Oryzias latipes and the platy-fish Xiphophorus maculatus. Gene, 295 (2): 213–222.

    Article  Google Scholar 

  • Kopp, A., 2012. Dmrt genes in the development and evolution of sexual dimorphism. Trends in Genetics, 28 (4): 175–184.

    Article  Google Scholar 

  • Kumar, S., Stecher, G., and Tamura, K., 2016. MEGA7: Molecular Evolutionary Genetics Analysis version 7.0 for bigger datasets. Molecular Biology and Evolution, 33 (7): 1870–1874.

    Article  Google Scholar 

  • Le Vay, L., Ut, V. N., and Walton, M., 2007. Population ecology of the mud crab Scylla paramamosain (Estampador) in an estuarine mangrove system; a mark-recapture study. Marine Biology, 151 (3): 1127–1135.

    Article  Google Scholar 

  • Li, S., Li, F., Yu, K., and Xiang, J., 2018. Identification and characterization of a doublesex gene which regulates the expression of insulin-like androgenic gland hormone in Fenneropenaeus chinensis. Gene, 649: 1–7.

    Article  Google Scholar 

  • Li, Y. Y., Ai, C. X., and Liu, L. J., 2018. Mud crab, Scylla paramamosain China’s leading maricultured crab. In: Aquaculture in China: Success Stories and Modern Trends. Gui, J. F., et al., eds., Wiley Online Library, 226–233.

  • Lin, J., Yuan, Y., Shi, X., Fang, S., Zhang, Y., Guan, M., et al., 2020. Molecular cloning, characterization and expression profiles of a SoxB2 gene related to gonadal development in mud crab (Scylla paramamosain). Invertebrate Reproduction and Development, 64 (2): 126–136.

    Article  Google Scholar 

  • Livak, K. J., and Schmittgen, T. D., 2001. Analysis of relative gene expression data using real-time quantitative PCR and the 2−ΔΔCT method. Methods, 25 (4): 402–408.

    Article  Google Scholar 

  • Meng, A., Moore, B., Tang, H., Yuan, B., and Lin, S., 1999. A Drosophila doublesex-related gene, terra, is involved in somitogenesis in vertebrates. Development, 126 (6): 1259–1268.

    Article  Google Scholar 

  • Miller, S. W., Hayward, D. C., Bunch, T. A., Miller, D. J., Ball, E. E., Bardwell, V. J., et al., 2003. A DM domain protein from a coral, Acropora millepora, homologous to proteins important for sex determination. Evolution & Development, 5: 251–258.

    Article  Google Scholar 

  • Muralidharan, B., Keruzore, M., Pradhan, S. J., Roy, B., Shetty, A. S., Kinare, V., et al., 2017. Dmrt5, a novel neurogenic factor, reciprocally regulates Lhx2 to control the neuron-glia cell fate switch in the developing hippocampus. The Journal of Neuroscience, 37 (46): 11245–11254.

    Article  Google Scholar 

  • Murphy, M. W., Lee, J. K., Rojo, S., Gearhart, M. D., Kurahashi, K., Banerjee, S., et al., 2015. An ancient protein-DNA interaction underlying metazoan sex determination. Nature Structural & Molecular Biology, 22 (6): 442–451.

    Article  Google Scholar 

  • Ottolenghi, C., Fellous, M., Barbieri, M., and McElreavey, K., 2002. Novel paralogy relations among human chromosomes support a link between the phylogeny of doublesex-related genes and the evolution of sex determination. Genomics, 79 (3): 333–343.

    Article  Google Scholar 

  • Parlier, D., Moers, V., Van Campenhout, C., Preillon, J., Leclère, L., Saulnier, A., et al., 2013. The Xenopus doublesex-related gene Dmrt5 is required for olfactory placode neurogenesis. Developmental Biology, 373 (1): 39–52.

    Article  Google Scholar 

  • Raymond, C. S., Murphy, M. W., Osullivan, M. G., Bardwell, V. J., and Zarkower, D., 2000. Dmrt1, a gene related to worm and fly sexual regulators, is required for mammalian testis differentiation. Genes & Development, 14 (20): 2587–2595.

    Article  Google Scholar 

  • Raymond, C. S., Parker, E. D., Kettlewell, J. R., Brown, L. G., Page, D. C., Kusz, K., et al., 1999. A region of human chromosome 9p required for testis development contains two genes related to known sexual regulators. Human Molecular Genetics, 8 (6): 989–996.

    Article  Google Scholar 

  • Raymond, C. S., Shamu, C. E., Shen, M. M., Seifert, K. J., Hirsch, B., Hodgkin, J., et al., 1998. Evidence for evolutionary conservation of sex-determining genes. Nature, 391: 691.

    Article  Google Scholar 

  • Rideout, E. J., Dornan, A. J., Neville, M. C., Eadie, S., and Goodwin, S. F., 2010. Control of sexual differentiation and behavior by the doublesex gene in Drosophila melanogaster. Nature Neuroscience, 13 (4): 458–466.

    Article  Google Scholar 

  • Sato, T., Rocancourt, D., Marques, L., Thorsteinsdóttir, S., and Buckingham, M., 2010. A Pax3/Dmrt2/Myf5 regulatory cascade functions at the onset of myogenesis. PLoS Genetics, 6 (4): e1000897.

    Article  Google Scholar 

  • Toyota, K., Kato, Y., Sato, M., Sugiura, N., Miyagawa, S., Miyakawa, H., et al., 2013. Molecular cloning of doublesex genes of four cladocera (water flea) species. BMC Genomics, 14: 239.

    Article  Google Scholar 

  • Urquhart, J. E., Beaman, G. M., Byers, H., Roberts, N. A., Chervinsky, E., Osullivan, J., et al., 2016. DMRTA2 (DMRT5) is mutated in a novel cortical brain malformation. Clinical Genetics, 89 (6): 724–727.

    Article  Google Scholar 

  • Veith, A. M., Schafer, M., Kluver, N., Schmidt, C., Schultheis, C., Schartl, M., et al., 2006. Tissue-specific expression of dmrt genes in embryos and adults of the platyfish Xiphophorus maculatus. Zebrafish, 3 (3): 325–337.

    Article  Google Scholar 

  • Volff, J., Zarkower, D., Bardwell, V. J., and Schartl, M., 2003. Evolutionary dynamics of the DM domain gene family in metazoans. Journal of Molecular Evolution, 57 (1): S241–S249.

    Article  Google Scholar 

  • Wang, M., Xie, X., Xu, D., Wang, Z., Yu, G., Jin, Z., et al., 2020. Molecular characterization of the sex-lethal gene in mud crab Scylla paramamosain and its potential role in sexual development. Comparative Biochemistry and Physiology Part B: Biochemistry and Molecular Biology, 250: 110486.

    Article  Google Scholar 

  • Wang, Y., Jin, S., Fu, H., Qiao, H., Sun, S., Zhang, W., et al., 2019. Identification and characterization of the DMRT11E gene in the oriental river prawn Macrobrachium nipponense. International Journal of Molecular Sciences, 20 (7): 1734.

    Article  Google Scholar 

  • Wexler, J. R., Plachetzki, D. C., and Kopp, A., 2014. Pan-metazoan phylogeny of the DMRT gene family: A framework for functional studies. Development Genes and Evolution, 224 (3): 175–181.

    Article  Google Scholar 

  • Williams, M. J., and Primavera, J. H., 2001. Choosing tropical portunid species for culture, domestication and stock enhancement in the Indo-Pacific. Asian Fisheries Science, 14 (2): 121–142.

    Article  Google Scholar 

  • Winkler, C., Hornung, U., Kondo, M., Neuner, C., Duschl, J., Shima, A., et al., 2004. Developmentally regulated and non-sex-specific expression of autosomal dmrt genes in embryos of the Medaka fish (Oryzias latipes). Mechanisms of Development, 121 (7): 997–1005.

    Article  Google Scholar 

  • Wu, Q., Waiho, K., Huang, Z., Li, S., Zheng, H., Zhang, Y., et al., 2020. Growth traits and biochemical composition dynamics of ovary, hepatopancreas and muscle tissues at different ovarian maturation stages of female mud crab, Scylla paramamosain. Aquaculture, 515: 734560.

    Article  Google Scholar 

  • Yang, X., Ikhwanuddin, M., Li, X., Lin, F., Wu, Q., Zhang, Y., et al., 2018. Comparative transcriptome analysis provides insights into differentially expressed genes and long non-coding RNAs between ovary and testis of the mud crab (Scylla paramamosain). Marine Biotechnology, 20 (1): 20–34.

    Article  Google Scholar 

  • Yoshizawa, A., Nakahara, Y., Izawa, T., Ishitani, T., Tsutsumi, M., Kuroiwa, A., et al., 2011. Zebrafish Dmrta2 regulates neurogenesis in the telencephalon. Genes Cells, 16 (11): 1097–1109.

    Article  Google Scholar 

  • Yu, Y., Ma, W., Zeng, Q., Qian, Y., Yang, J., and Yang, W., 2014. Molecular cloning and sexually dimorphic expression of two Dmrt genes in the giant freshwater prawn, Macrobrachium rosenbergii. Agricultural Research, 3 (2): 181–191.

    Article  Google Scholar 

  • Yu, Y., Zhang, X., Yuan, J., Li, F., Chen, X., Zhao, Y., et al., 2015. Genome survey and high-density genetic map construction provide genomic and genetic resources for the Pacific White Shrimp Litopenaeus vannamei. Scientific Reports, 5: 15612.

    Article  Google Scholar 

  • Yu, Y., Zhang, X., Yuan, J., Wang, Q., Li, S., Huang, H., et al., 2017. Identification of sex-determining loci in Pacific White Shrimp Litopeneaus vannamei using linkage and association analysis. Marine Biotechnology, 19 (3): 277–286.

    Article  Google Scholar 

  • Zhang, E., and Qiu, G., 2010. A novel Dmrt gene is specifically expressed in the testis of Chinese mitten crab, Eriocheir sinensis. Development Genes & Evolution, 220 (5): 151–159.

    Article  Google Scholar 

  • Zhang, T., and Zarkower, D., 2017. DMRT proteins and coordination of mammalian spermatogenesis. Stem Cell Research, 24: 195–202.

    Article  Google Scholar 

  • Zhong, P., Zhou, T., Zhang, Y., Chen, Y., Yi, J., Lin, W., et al., 2019. Potential involvement of a DMRT family member (MrDsx) in the regulation of sexual differentiation and moulting in the giant river prawn Macrobrachium rosenbergii. Aquaculture Research, 50 (10): 3037–3049.

    Article  Google Scholar 

  • Zhu, L., Wilken, J., Phillips, N. B., Narendra, U., Chan, G., Stratton, S. M., et al., 2000. Sexual dimorphism in diverse metazoans is regulated by a novel class of intertwined zinc fingers. Genes & Development, 14 (14): 1750–1764.

    Article  Google Scholar 

  • Zwarts, L., Broeck, L. V., Cappuyns, E., Ayroles, J. F., Magwire, M. M., Vulsteke, V., et al., 2015. The genetic basis of natural variation in mushroom body size in Drosophila melanogaster. Nature Communications, 6 (1): 10115–10115.

    Article  Google Scholar 

Download references

Acknowledgements

This study was funded by the National Natural Science Foundation of China (No. 31772837), the National Key Research & Development Program of China (No. 2018YF D0900201), the Science and Technology Project of Guangdong Province (No. 2018A050506080), the Shantou University Scientific Research Foundation for Talents (No. NTF17006), and the Program for Innovation and Enhancement of School of Department of Education of Guangdong Province (No. 2017KCXTD014).

Author information

Authors and Affiliations

  1. Guangdong Provincial Key Laboratory of Marine Biotechnology, Institute of Marine Sciences, Shantou University, Shantou, 515063, China

    Yin Zhang, Shaobin Fang, Fei Lin, Shengkang Li, Huaiping Zheng, Yueling Zhang & Hongyu Ma

  2. STU-UMT Joint Shellfish Research Laboratory, Shantou University, Shantou, 515063, China

    Yin Zhang, Shaobin Fang, Fei Lin, Shengkang Li, Huaiping Zheng, Yueling Zhang, Mhd Ikhwanuddin & Hongyu Ma

  3. Institute of Tropical Aquaculture, Universiti Malaysia Terengganu, Kuala Terengganu, 21030, Malaysia

    Mhd Ikhwanuddin & Hongyu Ma

Authors
  1. Yin Zhang
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Shaobin Fang
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Fei Lin
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Shengkang Li
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Huaiping Zheng
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Yueling Zhang
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Mhd Ikhwanuddin
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Hongyu Ma
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Hongyu Ma.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Zhang, Y., Fang, S., Lin, F. et al. Identification and Characterization of Gene SpDMRT99B and Its Sex-Biased Expression Profile in the Mud Crab, Scylla paramamosain. J. Ocean Univ. China 20, 1495–1504 (2021). https://doi.org/10.1007/s11802-021-4765-5

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11802-021-4765-5

Key words

Search

Navigation