Skip to main content
SpringerLink
Log in

Full-length gonad transcriptome analysis of Amur sturgeon Dmrt family genes: identification, characterization, and expression patterns during gonadal differentiation

  • Published:
Fish Physiology and Biochemistry Aims and scope Submit manuscript

Abstract

The regulatory mechanisms that govern sex differentiation in sturgeon are still poorly understood. The doublesex and Mab-3-related transcription factor (Dmrt) gene family is known for its extensive roles in sex determination and differentiation across vertebrates. This study aimed to identify new members of sturgeon Dmrt family genes and core actors in the gonadal differentiation of Amur sturgeon. A full-length gonad transcriptome database was exploited to identify Dmrt gene orthologs. Analyses of phylogenetic relationships and selection pressure were performed, and tissue expression profiles and spatiotemporal expression patterns in gonads were then analyzed using real-time PCR. In total, five Dmrt family genes were identified from the full-length gonad transcriptome, including Dmrt2, DmrtA1, DmrtA2, DmrtB1a, and DmrtB1b. Phylogenetic analysis showed that these genes were clustered into clades corresponding to the doublesex/Mav-3 (DM) genes of vertebrates. Furthermore, the analysis of evolutionary selective pressure indicated that DmrtB1a and DmrtB1b were subject to positive selection, suggesting the existence of adaptive evolution in sturgeon. The extensive tissue expression profiling of each Dmrt family gene revealed typical characteristics. Remarkably, according to a spatiotemporal expression pattern analysis, in later stages, DmrtB1b expression increased in testes and was significantly higher in testes than in ovaries at 24 months after hatching (M) and 36 M. This study provides a genetic resource of full-length Dmrt family genes and increases the understanding of Dmrt functions in sex differentiation in sturgeon.

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

Similar content being viewed by others

Data availability

All data generated or analyzed during this study are included in this published article and its supplementary files.

Code availability

Not applicable.

Abbreviations

Dmrt:

Doublesex and Mab-3-related transcription factor

DM:

Doublesex/Mab-3

ORF:

Open reading frame

CDS:

Coding sequences

UG:

Undifferentiated gonad

M:

Months after hatching

Ka:

Nonsynonymous substitutions

Ks:

Synonymous substitutions

HE:

Hematoxylin and eosin staining

References

  • Bemis WE, Findeis EK, Grande L (1997) An overview of Acipenseriformes. In: Birstein VJ, Waldman JR, Bemis WE (eds) Sturgeon Biodiversity and Conservation. Springer, Dordrecht, pp 25–71

    Google Scholar 

  • Burtis KC, Baker BS (1989) Drosophila doublesex gene controls somatic sexual differentiation by producing alternatively spliced mRNAs encoding related sex-specific polypeptides. Cell 56:997–1010

    Article  CAS  Google Scholar 

  • Cheng P, Huang Y, Lv Y et al (2021) The American paddlefish genome provides novel insights into chromosomal evolution and bone mineralization in early vertebrates. Mol Biol Evol 38:1595–1607

    Article  CAS  Google Scholar 

  • Dong J, Li J, Hu J et al (2020) Comparative genomics studies on the dmrt gene family in fish. Front Genet 11:563947

    Article  CAS  Google Scholar 

  • Du K, Stöck M (2020) The sterlet sturgeon genome sequence and the mechanisms of segmental rediploidization. Nat Ecol Evol 4(6):841–852

    Article  Google Scholar 

  • Erdman SE, Burtis KC (1993) The Drosophila doublesex proteins share a novel zinc finger related DNA binding domain. Embo J 12:527–535

    Article  CAS  Google Scholar 

  • Hildreth PE (1965) Doublesex, recessive gene that transforms both males and females of Drosophila into intersexes. Genetics 51:659–678

    Article  CAS  Google Scholar 

  • Hoegg S, Brinkmann H, Taylor JS et al (2004) Phylogenetic timing of the fish-specific genome duplication correlates with the diversification of teleost fish. J Mol Evol 59:190–203

    Article  CAS  Google Scholar 

  • Johnsen H, Andersen Ø (2012) Sex dimorphic expression of five dmrt genes identified in the Atlantic cod genome. The fish-specific dmrt2b diverged from dmrt2a before the fish whole-genome duplication. Gene 505:221–232

    Article  CAS  Google Scholar 

  • Kato Y, Kobayashi K, Watanabe H et al (2011) Environmental sex determination in the branchiopod crustacean Daphnia magna: deep conservation of a Doublesex gene in the sex-determining pathway. PLoS Genet 7:e1001345

    Article  CAS  Google Scholar 

  • Lebeda I, Ráb P, Majtánová Z et al (2020) Artificial whole genome duplication in paleopolyploid sturgeons yields highest documented chromosome number in vertebrates. Sci Rep 10:19705

    Article  CAS  Google Scholar 

  • Ludwig A, Belfiore NM, Pitra C et al (2001) Genome duplication events and functional reduction of ploidy levels in sturgeon (Acipenser, Huso and Scaphirhynchus). Genetics 158:1203–1215

    Article  CAS  Google Scholar 

  • Lyu Q, Hu J, Yang X et al (2019) Expression profiles of dmrts and foxls during gonadal development and sex reversal induced by 17α-methyltestosterone in the orange-spotted grouper. Gen Comp Endocrinol 274:26–36

    Article  CAS  Google Scholar 

  • Matson CK, Murphy MW, Griswold MD et al (2010) The mammalian doublesex homolog DMRT1 is a transcriptional gatekeeper that controls the mitosis versus meiosis decision in male germ cells. Dev Cell 19:612–624

    Article  CAS  Google Scholar 

  • Matsuda M, Shinomiya A, Kinoshita M et al (2007) DMY gene induces male development in genetically female (XX) medaka fish. Proc Natl Acad SciU S A 104:3865–3870

    Article  CAS  Google Scholar 

  • Okada H, Hagihara S, Yamashita K et al (2017) Expression pattern of foxl2 and dmrt1 in gonad of Amur sturgeon Acipenser schrenckii in relation to sex differentiation. Aquaculture 479:712–720

    Article  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Panchy N, Lehti-Shiu M (2016) Evolution of gene duplication in plants. Plant Physiol 171:2294–2316

    Article  CAS  Google Scholar 

  • Poulain M, Frydman N, Tourpin S et al (2014) Involvement of doublesex and mab-3-related transcription factors in human female germ cell development demonstrated by xenograft and interference RNA strategies. Mol Hum Reprod 20:960–971

    Article  CAS  Google Scholar 

  • Saito T, Psenicka M, Goto R et al (2014) The origin and migration of primordial germ cells in sturgeons. PLoS ONE 9:e86861

    Article  Google Scholar 

  • Sheng Y, Chen B, Zhang L et al (2014) Identification of Dmrt genes and their up-regulation during gonad transformation in the swamp eel (Monopterus albus). Mol Biol Rep 41:1237–1245

    Article  CAS  Google Scholar 

  • Smith CA, Roeszler KN, Ohnesorg T et al (2009) The avian Z-linked gene DMRT1 is required for male sex determination in the chicken. Nature 461:267–271

    Article  CAS  Google Scholar 

  • Veith AM, Klattig J, Dettai A et al (2006) Male-biased expression of X-chromosomal DM domain-less Dmrt8 genes in the mouse. Genomics 88:185–195

    Article  CAS  Google Scholar 

  • Veith AM, Schäfer M, Klüver N et al (2006) Tissue-specific expression of dmrt genes in embryos and adults of the platyfish Xiphophorus maculatus. Zebrafish 3:325–337

    Article  CAS  Google Scholar 

  • Volff JN, Zarkower D, Bardwell VJ et al (2003) Evolutionary dynamics of the DM domain gene family in metazoans. Ej Mol Evol 57:S241-249

    Article  CAS  Google Scholar 

  • Wang D, Zhang Y, Zhang Z et al (2010) KaKs_Calculator 2.0: a toolkit incorporating gamma-series methods and sliding window strategies. Genom Proteomics Bioinfo 8:77–80

    Article  CAS  Google Scholar 

  • Wang W, Zhu H, Dong Y et al (2019) Identification and dimorphic expression of sex-related genes during gonadal differentiation in sterlet Acipenser ruthenus, a primitive fish species. Aquaculture 500:178–187

    Article  CAS  Google Scholar 

  • Webster KA, Schach U, Ordaz A et al (2017) Dmrt1 is necessary for male sexual development in zebrafish. Dev Biol 422:33–46

    Article  CAS  Google Scholar 

  • Xu S, Xia W, Zohar Y et al (2013) Zebrafish dmrta2 regulates the expression of cdkn2c in spermatogenesis in the adult testis. BiolReprod 88:14

    Google Scholar 

  • Yamaguchi A, Lee KH, Fujimoto H et al (2006) Expression of the DMRT gene and its roles in early gonadal development of the Japanese pufferfish Takifugu rubripes. Comp Biochem Physiol Part D Genomics Proteomics 1:59–68

    Article  Google Scholar 

  • Yoshimoto S, Okada E, Umemoto H et al (2008) A W-linked DM-domain gene, DM-W, participates in primary ovary development in Xenopus laevis. Proc Natl Acad Sci U S A 105:2469–2474

    Article  CAS  Google Scholar 

  • Zafar I, Rather MA, Dhandare BC (2019) Genome-wide identification of doublesex and Mab-3-related transcription factor (DMRT) genes in Nile tilapia (Oreochromis niloticus). Biotechnol Rep 24:e00398

    Article  Google Scholar 

  • Zhang T, Murphy MW, Gearhart MD et al (2014) The mammalian Doublesex homolog DMRT6 coordinates the transition between mitotic and meiotic developmental programs during spermatogenesis. Development 141:3662–3671

    Article  CAS  Google Scholar 

  • Zhang X, Wang H, Li M et al (2014) Isolation of doublesex- and mab-3-related transcription factor 6 and its involvement in spermatogenesis in tilapia. Biol Reprod 91:136

    PubMed  Google Scholar 

  • Zhang X, Li G, Jiang H et al (2019) Full-length transcriptome analysis of Litopenaeus vannamei reveals transcript variants involved in the innate immune system. Fish Shellfish Immunol 87:346–359

    Article  CAS  Google Scholar 

  • Zhang X, Zhou J, Li L et al (2020) Full-length transcriptome sequencing and comparative transcriptomic analysis to uncover genes involved in early gametogenesis in the gonads of Amur sturgeon (Acipenser schrenckii). Front Zool 17:11

    Article  Google Scholar 

  • Zhou X, Li Q, Lu H et al (2008) Fish specific duplication of Dmrt2: characterization of zebrafish Dmrt2b. Biochimie 90:878–887

    Article  CAS  Google Scholar 

  • Zhu L, Wilken J, Phillips NB et al (2000) Sexual dimorphism in diverse metazoans is regulated by a novel class of intertwined zinc fingers. Genes Dev 14:1750–1764

    Article  CAS  Google Scholar 

  • Zhu Y, Cui Z, Yang Y et al (2019) Expression analysis and characterization of dmrt2 in Chinese tongue sole (Cynoglossus semilaevis). Theriogenology 138:1–8

    Article  Google Scholar 

Download references

Acknowledgements

We thank Mr. Wenhua Wu for the help with sturgeon sampling.

Funding

This work was supported by the GDAS’ Project of Science and Technology Development (2020GDASYL-20200104026), the National Natural Science Fund of China (31802279), and the Key Laboratory Fund of Animal Protection and Resource Utilization of Guangdong Province (GIABR-KF201704).

Author information

Author notes

  1. Xiujuan Zhang and Guanyu Li contributed equally.

Authors and Affiliations

  1. Guangdong Key Laboratory of Animal Conservation and Resource Utilization, Guangdong Public Laboratory of Wild Animal Conservation and Utilization, Institute of Zoology, Guangdong Academy of Sciences, Guangzhou, Guangdong, China

    Xiujuan Zhang, Guanyu Li, Jiabin Zhou, Mei Lv, Linmiao Li & Jinping Chen

  2. South China Botanical Garden, Chinese Academy of Sciences, Guangzhou, Guangdong, China

    Guanyu Li

Authors
  1. Xiujuan Zhang
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Guanyu Li
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Jiabin Zhou
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Mei Lv
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Linmiao Li
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Jinping Chen
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

X. J. Zhang and J. P. Chen conceived and designed the study. X. J. Zhang, G. Y. Li, J. B. Zhou, M. Lv, and L. M. Li performed the experiments. X. J. Zhang and G. Y. Li analyzed the sequence data. X. J. Zhang contributed to the writing of the manuscript. All authors read and approved the final manuscript.

Corresponding author

Correspondence to Jinping Chen.

Ethics declarations

Ethics approval

All experimental animal procedures followed the principles of Guide for Care and Use of Laboratory Animal and were approved by the Ethics Committee of Laboratory Animal of Institute of Zoology, Guangdong Academy of Science (No: GIZ20200828).

Consent to participate

Consent was obtained from individual participants.

Consent for publication

All authors have approved the final manuscript.

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

Below is the link to the electronic supplementary material.

Supplementary file1 (RAR 6733 KB)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Zhang, X., Li, G., Zhou, J. et al. Full-length gonad transcriptome analysis of Amur sturgeon Dmrt family genes: identification, characterization, and expression patterns during gonadal differentiation. Fish Physiol Biochem 48, 839–852 (2022). https://doi.org/10.1007/s10695-022-01087-z

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10695-022-01087-z

Keywords

Search

Navigation