, Volume 662, Issue 1, pp 99–106 | Cite as

Molecular evolution of the membrane associated progesterone receptor in the Brachionus plicatilis (Rotifera, Monogononta) species complex

  • Hilary A. Smith
  • David B. Mark Welch
  • Terry W. Snell


Many studies have investigated physiological roles of the membrane associated progesterone receptor (MAPR), but little is known of its evolution. Marked variations in response to exogenous progesterone have been reported for four brachionid rotifer species, suggesting differences in progesterone signaling and reception. Here we report sequence variation for the MAPR gene in the Brachionus plicatilis species complex. Phylogenetic analysis of this receptor is compared with relatedness based on cytochrome c oxidase subunit 1 sequences. Nonsynonymous to synonymous site substitution rate ratios, amino acid divergence, and variations in predicted phosphorylation sites are examined to assess evolution of the MAPR among brachionid clades.


dN/dS Gene tree PGRMC1 Protein structure Signaling Substitution 



National Science Foundation grant BE/GenEn MCB-0412674E to TWS and DMW, and an NSF IGERT fellowship to HAS under DGE 0114400, supported this study. E. García-Roger provided subcultures of B. rotundiformis and B. plicatilis s.s. of Spain. B. Hecox-Lea did 5′-RACE. T. Shearer gave advice. Comments by R.L. Wallace, M. Serra, and two anonymous reviewers improved this manuscript.


  1. Abascal, F., R. Zardoya & D. Posada, 2005. ProtTest: selection of best-fit models of protein evolution. Bioinformatics 21: 2104–2105.CrossRefPubMedGoogle Scholar
  2. Cahill, M. A., 2007. Progesterone receptor membrane component 1: an integrative review. Journal of Steroid Biochemistry and Molecular Biology 105: 16–36.CrossRefPubMedGoogle Scholar
  3. Civetta, A. & R. S. Singh, 1998. Sex-related genes, directional sexual selection, and speciation. Molecular Biology and Evolution 15: 901–909.PubMedGoogle Scholar
  4. de Castro, E., C. J. A. Sigrist, A. Gattiker, V. Bulliard, P. S. Langendijk-Genevaux, E. Gasteiger, A. Bairoch & N. Hulo, 2006. ScanProsite: detection of PROSITE signature matches and ProRule-associated functional and structural residues in proteins. Nucleic Acids Research 34: W362–W365.CrossRefPubMedGoogle Scholar
  5. Ewing, B. & P. Green, 1998. Base-calling of automated sequencer traces using phred. II. Error probabilities. Genome Research 8: 186–194.PubMedGoogle Scholar
  6. Finn, R. D., J. Tate, J. Mistry, P. C. Coggill, J. S. Sammut, H. R. Hotz, G. Ceric, K. Forslund, S. R. Eddy, E. L. Sonnhammer & A. Bateman, 2008. The Pfam protein families database. Nucleic Acids Research 36: D281–D288.CrossRefPubMedGoogle Scholar
  7. Folmer, O., M. Black, W. Hoeh, R. Lutz & R. Vrijenhoek, 1994. DNA primers for amplification of mitochondrial cytochrome c oxidase subunit I form diverse metazoan invertebrates. Molecular Marine Biology and Biotechnology 3: 294–299.PubMedGoogle Scholar
  8. Fontaneto, D., I. Giordani, G. Melone & M. Serra, 2007. Disentangling the morphological stasis in two rotifer species of the Brachionus plicatilis species complex. Hydrobiologia 583: 297–307.CrossRefGoogle Scholar
  9. Frohman, M. A., M. K. Dush & G. R. Martin, 1988. Rapid production of full-length cDNAs from rare transcripts: amplification using a single gene-specific oligonucleotide primer. Proceedings of the National Academy of Sciences of the United States of America 85: 8998–9002.CrossRefPubMedGoogle Scholar
  10. Gelman, A. & D. B. Rubin, 1992. Inference from iterative simulation using multiple sequences. Statistical Science 7: 434–455.Google Scholar
  11. Gibrat, J.-F., T. Madej & S. H. Bryant, 1996. Surprising similarities in structure comparison. Current Opinion in Structural Biology 6: 377–385.CrossRefPubMedGoogle Scholar
  12. Gómez, A., M. Serra, G. R. Carvalho & D. H. Lunt, 2002. Speciation in ancient cryptic species complexes: evidence from the molecular phylogeny of Brachionus plicatilis (Rotifera). Evolution 56: 1431–1444.PubMedGoogle Scholar
  13. Gordon, D., C. Abajian & P. Green, 1998. Consed: a graphical tool for sequence finishing. Genome Research 8: 195–202.PubMedGoogle Scholar
  14. Haag-Liautard, C., N. Coffey, D. Houle, M. Lynch, B. Charlesworth & P. D. Keightley, 2008. Direct estimation of the mitochondrial DNA mutation rate in Drosophila melanogaster. PLoS Biology 6: e204.CrossRefPubMedGoogle Scholar
  15. Hall, T. A., 1999. BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucleic Acids Symposium Series 41: 95–98.Google Scholar
  16. Huelsenbeck, J. P. & F. Ronquist, 2001. MRBAYES: Bayesian inference of phylogenetic trees. Bioinformatics 17: 754–755.CrossRefPubMedGoogle Scholar
  17. Ketterson, E. D. & J. Val Nolan, 1999. Adaptation, exaptation, and constraint: a hormonal perspective. The American Naturalist 154: S4–S25.CrossRefGoogle Scholar
  18. Kishino, H. & M. Hasegawa, 1989. Evaluation of the maximum likelihood estimate of the evolutionary tree topologies from DNA sequence data, and the branching order in Hominoidea. Journal of Molecular Evolution 29: 170–179.CrossRefPubMedGoogle Scholar
  19. Krogh, A., B. Larsson, G. v. Heijne & E. L. L. Sonnhammer, 2001. Predicting transmembrane protein topology with a hidden Markov model: application to complete genomes. Journal of Molecular Biology 305: 567–580.CrossRefPubMedGoogle Scholar
  20. Larkin, M. A., G. Blackshields, N. P. Brown, R. Chenna, P. A. McGettigan, H. McWilliam, F. Valentin, I. M. Wallace, A. Wilm, R. Lopez, J. D. Thompson, T. J. Gibson & D. G. Higgins, 2007. Clustal W and Clustal X version 2.0. Bioinformatics 23: 2947–2948.CrossRefPubMedGoogle Scholar
  21. Li, W.-H., C.-I. Wu & C.-C. Luo, 1984. Nonrandomness of point mutation as reflected in nucleotide substitutions in pseudogenes and its evolutionary implications. Journal of Molecular Evolution 21: 58–71.CrossRefPubMedGoogle Scholar
  22. Mansouri, M. R., J. Schuster, J. Badhai, E.-L. Stattin, R. Lösel, M. Wehling, B. Carlsson, O. Hovatta, P. O. Karlström, I. Golovleva, D. Toniolo, S. Bione, J. Peluso & N. Dahl, 2008. Alterations in the expression, structure and function of progesterone receptor membrane component-1 (PGRMC1) in premature ovarian failure. Human Molecular Genetics 17: 3776–3783.CrossRefPubMedGoogle Scholar
  23. Mifsud, W. & A. Bateman, 2002. Membrane-bound progesterone receptors contain a cytochrome b5-like ligand-binding domain. Genome Biology 3: research0068.0061–research0068.0065.Google Scholar
  24. Notredame, C., D. G. Higgins & J. Heringa, 2000. T-Coffee: a novel method for fast and accurate multiple sequence alignment. Journal of Molecular Biology 302: 205–217.CrossRefPubMedGoogle Scholar
  25. Palmé, A. E., M. Wright & O. Savolainen, 2008. Patterns of divergence among conifer ESTs and polymorphism in Pinus sylvestris identify putative selective sweeps. Molecular Biology and Evolution 25: 2567–2577.CrossRefPubMedGoogle Scholar
  26. Rambaut, A., 2009. FigTree v1.2.2 [available at http://tree.bio.ed.ac.uk/software/figtree/].
  27. Rohe, H. J., I. S. Ahmed, K. E. Twist & R. J. Craven, 2009. PGRMC1 (progesterone receptor membrane component 1): a targetable protein with multiple functions in steroid signaling, P450 activation and drug binding. Pharmacology and Therapeutics 121: 14–19.CrossRefPubMedGoogle Scholar
  28. Schwede, T., J. Kopp, N. Geux & M. C. Peitsch, 2003. SWISS-MODEL: an automated protein homology-modeling server. Nucleic Acids Research 31: 3381–3385.CrossRefPubMedGoogle Scholar
  29. Snell, T. W. & N. J. D. DesRosiers, 2008. Effects of progesterone on sexual reproduction of Brachionus manjavacas (Rotifera). Journal of Experimental Marine Biology and Ecology 363: 104–109.CrossRefGoogle Scholar
  30. Snell, T. W. & C.-P. Stelzer, 2005. Removal of surface glycoproteins and transfer among Brachionus species. Hydrobiologia 546: 267–274.CrossRefGoogle Scholar
  31. Snell, T. W., J. Kubanek, W. Carter, A. B. Payne, J. Kim, M. K. Hicks & C.-P. Stelzer, 2006. A protein signal triggers sexual reproduction in Brachionus plicatilis (Rotifera). Marine Biology 149: 763–773.CrossRefGoogle Scholar
  32. Snell, T. W., T. L. Shearer, H. A. Smith, J. Kubanek, K. E. Gribble & D. B. Mark Welch, 2009. Genetic determinants of mate recognition in Brachionus manjavacas (Rotifera). BMC Biology 7: 60.CrossRefPubMedGoogle Scholar
  33. Suatoni, E., S. Vicario, S. Rice, T. Snell & A. Caccone, 2006. An analysis of species boundaries and biogeographic patterns in a cryptic species complex: the rotifer—Brachionus plicatilis. Molecular Phylogenetics and Evolution 41: 86–98.CrossRefPubMedGoogle Scholar
  34. Wang, Y., L. Y. Geer, C. Chappey, J. A. Kans & S. H. Bryant, 2000. Cn3D: sequence and structure views for Entrez. Trends in Biochemical Sciences 25: 300–302.CrossRefPubMedGoogle Scholar
  35. Yang, Z., 2007. PAML 4: phylogenetic analysis by maximum likelihood. Molecular Biology and Evolution 24: 1586–1591.CrossRefPubMedGoogle Scholar
  36. Yang, Z. & R. Nielsen, 2002. Codon-substitution models for detecting molecular adaptation at individual sites along specific lineages. Molecular Biology and Evolution 19: 908–917.PubMedGoogle Scholar
  37. Zhang, J., R. Nielsen & Z. Yang, 2005. Evaluation of an improved branch-site likelihood method for detecting positive selection at the molecular level. Molecular Biology and Evolution 22: 2472–2479.CrossRefPubMedGoogle Scholar
  38. Zwickl, D. J., 2006. Genetic Algorithm Approaches for the Phylogenetic Analysis of Large Biological Sequence Datasets Under the Maximum Likelihood Criterion. School of Biological Sciences, The University of Texas at Austin, Austin, TX: 115.Google Scholar

Copyright information

© Springer Science+Business Media B.V. 2010

Authors and Affiliations

  • Hilary A. Smith
    • 1
  • David B. Mark Welch
    • 2
  • Terry W. Snell
    • 1
  1. 1.School of BiologyGeorgia Institute of TechnologyAtlantaUSA
  2. 2.Marine Biological LaboratoryJosephine Bay Paul Center for Comparative Molecular Biology and EvolutionWoods HoleUSA

Personalised recommendations