Skip to main content
SpringerLink
Log in

Identification, Evolution and Expression Analysis of Dmrt Genes in Polychaetes

  • GENERAL GENETICS
  • Published:
Russian Journal of Genetics Aims and scope Submit manuscript

Abstract

The doublesex-mab3-related transcription factor (Dmrt) gene family is a class of crucial transcription factors characterized by one or several DM domains. Dmrt family genes play important roles in sex determination/differentiation. Polychaete annelids are critically important in most marine ecosystems. However, to date, the genome-wide characterization and analysis of Dmrt genes in polychaetes have not been investigated. In this study, the identification and analysis of Dmrt genes were performed in three representative polychaetes, including Capitella teleta, Dimorphilus gyrociliatus, and Owenia fusiformis. A total of 12 Dmrt genes have been found, and the number of Dmrt genes in different polychaetes ranges from 3 to 5. The phylogenetic tree showed that all identified Dmrt genes were classified into 4 classes: Dmrt2/11E, Dmrt3/93B, Dmrt4/5/99B, and DSX. Furthermore, the selection pressure analysis suggested that all the Dmrt genes underwent strong purifying selection pressure. The spatiotemporal expression profile in O. fusiformis suggested that Dmrt genes have diverse functions, and the Dmrt2/11E-like gene may play an important role in the sex determination/differentiation of polychaetes. In general, this study provides a molecular basis for polychaete Dmrt genes and may serve as a reference for in-depth phylogenomics.

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.

Similar content being viewed by others

DATA AVAILABILITY

The datasets used and/or analyzed during the current study are available from the corresponding author on reasonable request.

REFERENCES

  1. Díaz-Castañeda, V. and Reish, D., Polychaetes in environmental studies, Annelids Mod. Biol., 2009, vol. 7, pp. 203—227.

    Article  Google Scholar 

  2. Capa, M. and Hutchings, P., Annelid diversity: historical overview and future perspectives, Diversity, 2021, vol. 13, no. 3, p. 129.

    Article  Google Scholar 

  3. Premoli, M., Sella, G., and Berra, G., Heritable variation of sex ratio in a polychaete worm, J. Evol. Biol., 1996, vol. 9, no. 6, pp. 845—854.

    Article  Google Scholar 

  4. George, J.D. and Hartmann-Schröder, G., Polychaetes: British Amphinomida, Spintherida and Eunicida: keys and notes for the identification of the species, Brill Arch., 1985, vol. 32.

    Book  Google Scholar 

  5. Tosuji, H., Miyamoto, J., Hayata, Y., et al., Karyotyping of female and male Hediste japonica (Polychaeta, Annelida) in comparison with those of two closely related species, H. diadroma and H. atoka, Zool. Sci., 2004, vol. 21, no. 2, pp. 147—152.

    Article  Google Scholar 

  6. Tosuji, H., Togami, K., and Miyamoto, J., Karyotypic analysis of the hermaphroditic viviparous polychaete, Hediste limnicola (Polychaeta: Nereididae): possibility of sex chromosome degeneration, J. Mar. Biol. Assoc. U. K., 2009, vol. 90, no. 3, pp. 613—616.

    Article  Google Scholar 

  7. Kopp, A., Dmrt genes in the development and evolution of sexual dimorphism, Trends Genet., 2012, vol. 28, no. 4, pp. 175—184.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  8. Smith, C.A., Roeszler, K.N., Ohnesorg, T., et al., The avian Z-linked gene DMRT1 is required for male sex determination in the chicken, Nature, 2009, vol. 461, no. 7261, pp. 267—271.

    Article  CAS  PubMed  Google Scholar 

  9. Yoshimoto, S., Okada, E., Umemoto, H., et al., A W‑linked DM-domain gene, DM-W, participates in primary ovary development in Xenopus laevis, Proc. Natl. Acad. Sci. U.S.A., 2008, vol. 105, no. 7, pp. 2469—2474.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  10. Hong, C.-S., Park, B.-Y., and Saint-Jeannet, J.-P., The function of Dmrt genes in vertebrate development: it is not just about sex, Dev. Biol., 2007, vol. 310, no. 1, pp. 1—9.

    Article  CAS  PubMed  Google Scholar 

  11. Wan, H.-F., Zhong, Z.-W., Jiang, Y.-H., et al., Genome-wide investigation of Dmrt gene family in large yellow croaker (Larimichthys crocea), Theriogenology, 2020, vol. 156, pp. 272—282.

    Article  CAS  PubMed  Google Scholar 

  12. Rather, M.A. and Dhandare, B.C., Genome-wide identification of doublesex and Mab-3-related transcription factor (DMRT) genes in Nile tilapia (Oreochromis niloticus), Biotechnol. Rep., 2019, vol. 24, р. e00398.

    Article  Google Scholar 

  13. Simakov, O., Marletaz, F., Cho, S.-J., et al., Insights into bilaterian evolution from three spiralian genomes, Nature, 2013, vol. 493, no. 7433, pp. 526—531.

    Article  CAS  PubMed  Google Scholar 

  14. Martín-Durán, J.M., Vellutini, B.C., Marlétaz, F., et al., Conservative route to genome compaction in a miniature annelid, Nat. Ecol. Evol., 2021, vol. 5, no. 2, pp. 231—242.

    Article  PubMed  Google Scholar 

  15. Martín-Zamora, F.M., Liang, Y., Guynes, K., et al., Annelid functional genomics reveal the origins of bilaterian life cycles, Nature, 2023, pp. 1—6.

  16. Chen, C., Chen, H., Zhang, Y., et al., TBtools: an integrative toolkit developed for interactive analyses of big biological data, Mol. Plant, 2020, vol. 13, no. 8, pp. 1194—1202.

    Article  CAS  PubMed  Google Scholar 

  17. Bailey, T.L., Johnson, J., Grant, C.E., et al., The MEME suite, Nucleic Acids Res., 2015, vol. 43, pp. W39—W49.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  18. Letunic, I. and Bork, P., Interactive Tree Of Life (iTOL) v4: recent updates and new developments, Nucleic Acids Res., 2019, vol. 47, pp. W256—W259.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  19. Kumar, S., Stecher, G., Li, M., et al., MEGA X: molecular evolutionary genetics analysis across computing platforms, Mol. Biol. Evol., 2018, vol. 35, no. 6. pp. 1547—1549. https://doi.org/10.1093/molbev/msy096

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  20. Nguyen, L.-T., Schmidt, H.A., von Haeseler, A., et al., IQ-TREE: a fast and effective stochastic algorithm for estimating maximum-likelihood phylogenies, Mol. Biol. Evol., 2015, vol. 32, no. 1, pp. 268—274.

    Article  CAS  PubMed  Google Scholar 

  21. Letunic, I. and Bork, P., Interactive Tree Of Life (iTOL) v5: an online tool for phylogenetic tree display and annotation, Nucleic Acids Res., 2021, vol. 49, pp. W293—W296.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  22. Gao, F. and Chen, J., EasyCodeML: an interactive visual tool for CodeML analysis, Ecol. Evol., 2016.

  23. Patel, R.K. and Jain, M., NGS QC toolkit: a toolkit for quality control of next generation sequencing data, PLoS One, 2012, vol. 7, no. 2, р. e30619.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  24. Kim, D., Langmead, B., and Salzberg, S.L., HISAT: a fast spliced aligner with low memory requirements, Nat. Methods, 2015, vol. 12, no. 4, pp. 357—360.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  25. Li, H., Handsaker, B., Wysoker, A., et al., The sequence alignment/map format and SAMtools, Bioinformatics, 2009, vol. 25, no. 16, pp. 2078—2079.

    Article  PubMed  PubMed Central  Google Scholar 

  26. Pertea, M., Pertea, G.M., Antonescu, C.M., et al., StringTie enables improved reconstruction of a transcriptome from RNA-seq reads, Nat. Biotechnol., 2015, vol. 33, no. 3, pp. 290—295.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  27. R Core Team, R: A Language and Environment for Statistical Computing, Vienna: R Foundation for Statistical Computing, 2021. https://www.R-project.org.

  28. Zafar, I., Rather, M.A., and Dhandare, B.C., Genome-wide identification of doublesex and Mab-3-related transcription factor (DMRT) genes in Nile tilapia (Oreochromis niloticus), Biotechnol. Rep., 2019, vol. 24, р. e00398.

    Article  Google Scholar 

  29. Xu, S., Zhang, S., Zhang, W., et al., Genome-wide identification, phylogeny, and expression profile of the Dmrt (doublesex and Mab-3 related transcription factor) gene family in channel catfish (Ictalurus punctatus), Front. Genet., 2022, vol. 13, р. 891204.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  30. Panara, V., Budd, G.E., and Janssen, R., Phylogenetic analysis and embryonic expression of panarthropod Dmrt genes, Front. Zool., 2019, vol. 16, р. 23.

    Article  PubMed  PubMed Central  Google Scholar 

  31. Dong, J., Li, J., Hu, J., et al., Comparative genomics studies on the DMRT gene family in fish, Front. Genet., 2020, vol. 11, р. 563947.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  32. Kimura, M., The neutral theory of molecular evolution, Sci. Am., 1979, vol. 241, no. 5, pp. 98—129.

    Article  CAS  PubMed  Google Scholar 

  33. Wei, W.-Y., Huang, J.-H., Yang, Q.-B., et al., Molecular characterization and functional analysis of DMRT11E in black tiger shrimp (Penaeus monodon), Aquac. Rep., 2022, vol. 22, р. 100982.

  34. Yu, F.-F., Wang, M.-F., Zhou, L., et al., Molecular cloning and expression characterization of Dmrt2 in Akoya pearl oysters, Pinctada martensii, J. Shellfish Res., 2011, vol. 30, no. 2, pp. 247—254.

    Article  Google Scholar 

  35. Jönsson, M., Morin, M., Wang, C.K., et al., Sex-specific expression of pheromones and other signals in gravid starfish, BMC Biol., 2022, vol. 20, no. 1, p. 288.

    Article  PubMed  PubMed Central  Google Scholar 

  36. Zhu, H., Zhao, S.D., Ray, A., et al., A comprehensive temporal patterning gene network in Drosophila medulla neuroblasts revealed by single-cell RNA sequencing, Nat. Commun., 2022, vol. 13, no. 1, p. 1247.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

Download references

ACKNOWLEDGMENTS

This work was supported by the High-Performance Computing Platform of Yantai Institute of Coastal Zone Research, Chinese Academy of Sciences.

Funding

This work was supported by the Open Project Program of Key Laboratory of Ecological Warning, Protection and Restoration for Bohai Sea, Ministry of Natural Resources (2022204), Natural Science Foundation of Shandong Province (ZR2021MC151, ZR2021QD158, ZR2022QC234), and Yantai Science and Technology Planning Project (2020MSGY074).

Author information

Authors and Affiliations

  1. Key Laboratory of Ecological Warning, Protection and Restoration for Bohai Sea, Ministry of Natural Resources, 266061, Qingdao, China

    Y. L. Ji & Q. C. Wang

  2. North China Sea Marine Forecasting Center of State Oceanic Administration, 266061, Qingdao, China

    Y. L. Ji

  3. Yantai Institute of China Agricultural University, 264670, Yantai, China

    X. H. Shen

  4. Yantaishan Hospital, 264001, Yantai, China

    S. J. Tian

  5. Yantai Institute of Coastal Zone Research, Chinese Academy of Sciences, 264003, Yantai, China

    H. Liu, T. G. Cao & Q. C. Wang

  6. Yantai Vocational College, 264670, Yantai, China

    Y. Wang

Authors
  1. Y. L. Ji
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. X. H. Shen
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. S. J. Tian
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. H. Liu
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. T. G. Cao
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Q. C. Wang
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Y. Wang
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

Q.W. and Y.W.: Conceptualization, and Methodology. Y.J.: Data curation, Writing—Original draft preparation. X.S. and S.T.: Writing—Reviewing and Editing. H.L.: Data Curation, and Supervision. T.C.: Software, and Validation.

Corresponding authors

Correspondence to Q. C. Wang or Y. Wang.

Ethics declarations

The authors declare that they have no conflicts of interest. This article does not contain any studies involving animals or human participants performed by any of the authors.

Supplementary Information

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Ji, Y.L., Shen, X.H., Tian, S.J. et al. Identification, Evolution and Expression Analysis of Dmrt Genes in Polychaetes. Russ J Genet 59 (Suppl 1), 1–8 (2023). https://doi.org/10.1134/S1022795423130070

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1134/S1022795423130070

Keywords:

Search

Navigation