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Development Genes and Evolution

, Volume 224, Issue 3, pp 175–181 | Cite as

Pan-metazoan phylogeny of the DMRT gene family: a framework for functional studies

  • Judith R. WexlerEmail author
  • David C. Plachetzki
  • Artyom Kopp
Sequence Corner

Abstract

The family of Doublesex-Mab-3 Related Transcription factors (DMRTs) includes key regulators of sexual differentiation and neurogenesis. To help understand the functional diversification of this gene family, we examined DMRT gene complements from the whole genome sequences and predicted gene models of 32 animal species representing 12 different phyla and from several non-metazoan outgroups. DMRTs are present in all animals except the sponge Amphimedon queenslandica, but are not found in any of the outgroups, indicating that this gene family is specific to animals and has an ancient pre-eumetazoan origin. Our analyses suggest that DMRT genes diversified independently in bilaterian and non-bilaterian animals. Most clades in the DMRT gene tree, including those containing the well-characterized DMRT1 and doublesex genes, have phylogenetically limited distributions.

Keywords

Doublesex-mab-3 related transcription factor Gene tree Phylogenetics Sex determination Evolution 

Notes

Acknowledgments

This work was supported by the National Institutes of Health (R01 GM082843 to A.K.); the Howard Hughes Medical Institute Life Sciences Research Foundation postdoctoral fellowship (to D.P.); and the UC—Davis Population Biology Graduate Group (to J.W.). We also thank two anonymous reviewers for their comments on the manuscript.

Supplementary material

427_2014_473_MOESM1_ESM.pdf (430 kb)
Supplementary Figures Summary of phylogenetic results, includes Figs. S1–S11 (PDF 429 kb)

References

  1. Abascal F, Zardoya R, Posada D (2005) ProtTest: selection of best-fit models of protein evolution. Bioinformatics 21:2104–2105CrossRefPubMedGoogle Scholar
  2. Altschul SF, Madden TL, Schaffer AA, Zhang J, Zhang Z, Miller W, Lipman DJ (1997) Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res 25:3389–3402CrossRefPubMedCentralPubMedGoogle Scholar
  3. Burtis KC, Baker BS (1989) Drosophila doublesex gene controls somatic sexual differentiation by producing alternatively spliced mRNAs encoding related sex-specific polypeptides. Cell 56:997–1010CrossRefPubMedGoogle Scholar
  4. Capella-Gutierrez S, Silla-Martinez JM, Gabaldon T (2009) trimAl: a tool for automated alignment trimming in large-scale phylogenetic analyses. Bioinformatics 25:1972–1973CrossRefPubMedCentralPubMedGoogle Scholar
  5. Coschigano KT, Wensink PC (1993) Sex-specific transcriptional regulation by the male and female doublesex proteins of Drosophila. Genes Dev 7:42–54CrossRefPubMedGoogle Scholar
  6. Katoh K, Misawa K, Kuma K, Miyata T (2002) MAFFT a novel method for rapid multiple sequence alignment based on fast Fourier transform. Nucleic Acids Res 30:3059–3066CrossRefPubMedCentralPubMedGoogle Scholar
  7. Kato Y, Kobayashi K, Watanabe H, Iguchi T (2011) Environmental sex determination in the branchiopod crustacean Daphnia magna: deep conservation of a Doublesex gene in the sex-determining pathway. PLoS Genet 7:e1001345CrossRefPubMedCentralPubMedGoogle Scholar
  8. Kim J, Kim Y, Lee S, Kwak K, Chung WJ, Choi K (2011) Determination of mRNA expression of DMRT93B, vitellogenin, and cuticle 12 in Daphnia magna and their biomarker potential for endocrine disruption. Ecotoxicology 20:1741–1748CrossRefPubMedGoogle Scholar
  9. Kopp A (2012) Dmrt genes in the development and evolution of sexual dimorphism. Trends Genet 28:175–184CrossRefPubMedCentralPubMedGoogle Scholar
  10. Mason DA, Rabinowitz JS, Portman DS (2008) dmd-3, a doublesex-related gene regulated by tra-1, governs sex-specific morphogenesis in C. elegans. Development 135:2373–2382CrossRefPubMedGoogle Scholar
  11. Matson CK, Murphy MW, Sarver AL, Griswold MD, Bardwell VJ, Zarkower D (2011) DMRT1 prevents female reprogramming in the postnatal mammalian testis. Nature 476:101–104CrossRefPubMedCentralPubMedGoogle Scholar
  12. Matsuda M et al (2007) DMY gene induces male development in genetically female (XX) medaka fish. Proc Natl Acad Sci 104:3865–3870CrossRefPubMedCentralPubMedGoogle Scholar
  13. Meng A, Moore B, Tang H, Yuan B, Lin S (1999) A Drosophila doublesex-related gene, terra, is involved in somitogenesis in vertebrates. Development 126:1259–1268PubMedGoogle Scholar
  14. Miller SW, Hayward DC, Bunch TA, Miller DJ, Ball EE, Bardwell VJ, Zarkower D, Brower DL (2003) A DM domain protein from a coral, Acropora millepora, homologous to proteins important for sex determination. Evol Dev 5:251–258CrossRefPubMedGoogle Scholar
  15. Parlier D, Moers V, Van Campenhout C, Preillon J, Lecière L, Saulnier A, Sirakov M, Busgendal H, Kricha S, Marine JC, Rentzch F, Bellefroid EJ (2013) The Xenopus doublesex-related gene Dmrt5 is required for olfactory placode neurogenesis. Dev Biol 373:39–52CrossRefPubMedGoogle Scholar
  16. Raymond CS, Kettlewell JR, Hirsch B, Bardwell VJ, Zarkower D (1999) Expression of Dmrt1 in the genital ridge of mouse and chicken embryos suggests a role in vertebrate sexual development. Dev Biol 215:208–220CrossRefPubMedGoogle Scholar
  17. Ronquist F, Teslenko M, van der Mark P, Ayres DL, Darling A, Hohna S, Larget B, Liu L, Suchard MA, Huelsenbeck JP (2012) MrBayes 3.2: efficient Bayesian phylogenetic inference and model choice across a large model space. Syst Biol 61:539–542CrossRefPubMedCentralPubMedGoogle Scholar
  18. Saude L, Lourenco R, Goncalves A, Palmeirim I (2005) terra is a left-right asymmetry gene required for left-right synchronization of the segmentation clock. Nat Cell Biol 7:918–920CrossRefPubMedGoogle Scholar
  19. Stamatakis A (2006) RAxML-VI-HPC: maximum likelihood-based phylogenetic analyses with thousands of taxa and mixed models. Bioinformatics 22:2688–2690CrossRefPubMedGoogle Scholar
  20. Toyota K, Kato Y, Sato M, Sugiura N, Miyagawa S, Miyakawa H, Watanabe H, Oda S, Ogino Y, Hiruta C, Mizutani T, Tatarazako N, Paland S, Jackson C, Colbourne J, Iguchi T (2013) Molecular cloning of doublesex genes of four cladocera (water flea) species. BMC Genomics 14:239CrossRefPubMedCentralPubMedGoogle Scholar
  21. Tresser J, Chiba S, Veeman M, El-Nachef D, Newman-Smith E, Horie T, Tsuda M, Smith WC (2010) doublesex/mab3 related-1 (dmrt1) is essential for development of anterior neural plate derivatives in Ciona. Development 137:2197–2203CrossRefPubMedCentralPubMedGoogle Scholar
  22. Volff JN, Zarkower D, Bardwell VJ, Schartl M (2003) Evolutionary dynamics of the DM domain gene family in metazoans. J Mol Evol 57(Suppl 1):S241–S249CrossRefPubMedGoogle Scholar
  23. Yu F-F, Wang M-F, Zhou L, Gui J-F, Yu X-Y (2011) Molecular cloning and expression characterization of Dmrt2 in Akoya Pearl Oysters, Pinctada martensii. J Shellfish Res 30:247–254CrossRefGoogle Scholar
  24. Zarkower D (2013) DMRT genes in vertebrate gametogenesis. Curr Top Dev Biol 102:327–356CrossRefPubMedGoogle Scholar
  25. Zhu L, Wilken J, Phillips NB, Narendra U, Chan G, Stratton S, Kent S, Weiss M (2000) Sexual dimorphism in diverse metazoans is regulated by a novel class of intertwined zinc fingers. Gene Dev 14:1750–1764CrossRefPubMedCentralPubMedGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2014

Authors and Affiliations

  • Judith R. Wexler
    • 1
    Email author
  • David C. Plachetzki
    • 2
  • Artyom Kopp
    • 1
  1. 1.Center for Population Biology, Department of Evolution and EcologyUniversity of CaliforniaDavisUSA
  2. 2.Department of Molecular, Cellular, & Biomedical SciencesUniversity of New HampshireDurhamUSA

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