Journal of Molecular Evolution

, Volume 77, Issue 3, pp 119–129 | Cite as

Lineage-Specific Duplications of Muroidea Faim and Spag6 Genes and Atypical Accelerated Evolution of the Parental Spag6 Gene

  • Huan Qiu
  • Aniela Gołas
  • Paweł Grzmil
  • Leszek Wojnowski
Original Article

Abstract

Gene duplications restricted to single lineage combined with an asymmetric evolution of the resulting genes may play particularly important roles in this lineage’s biology. We searched and identified asymmetrical evolution in nine gene families that duplicated exclusively in rodents and are present as single-copies in human, dog, cow, elephant, opossum, chicken, lizard, and Western clawed frog. Among those nine gene families are Fas apoptosis inhibitory molecule (Faim), implicated in apoptosis, and Sperm antigen 6 (Spag6), implicated in sperm mobility. Both genes were duplicated in or before the Muroidea ancestor. Due to the highly asymmetric evolution of the resulting paralogs, the existence of these duplications had been previously overlooked. Interestingly, Spag6, previously regarded and characterized as a single-copy ortholog of human Spag6, turns out to be a Muroidea-specific paralog. Conversely, the newly identified, highly divergent Spag6-BC061194 is in fact the parental gene. In consequence, this gene represents a rare exception from the general rule of rapid evolution of derived rather than parental genes following gene duplication. Unusual genes such as murine Spag6 may help to understand which mechanisms are responsible for this rule.

Keywords

Gene duplication Asymmetric evolution Faim Spag6 Positive selection 

Notes

Acknowledgments

This study was partly supported by Jagiellonian University, Institute of Zoology Grant (K/ZDS/003254). We acknowledge the release and sharing of whole-genome sequences of guinea pig, squirrel, rabbit and elephant prior to publication by the Broad Institute, Cambridge, MA, USA. We thank the editor and the two anonymous reviewers for constructive suggestions for improving the paper.

Conflict of interest

The authors declare that they have no conflict of interest.

Supplementary material

239_2013_9585_MOESM1_ESM.docx (1.6 mb)
Supplementary material 1 (DOCX 1,665 kb)

References

  1. Benson DA, Karsch-Mizrachi I, Clark K, Lipman DJ, Ostell J, Sayers EW (2012) GenBank. Nucleic Acids Res 40:D48–D53PubMedCentralCrossRefPubMedGoogle Scholar
  2. Blanco-Rodriguez J (1998) A matter of death and life: the significance of germ cell death during spermatogenesis. Int J Androl 21:236–248CrossRefPubMedGoogle Scholar
  3. Boguski MS, Lowe TM, Tolstoshev CM (1993) dbEST—database for “expressed sequence tags”. Nat Genet 4:332–333CrossRefPubMedGoogle Scholar
  4. Castillo-Davis CI, Kondrashov FA, Hartl DL, Kulathinal RJ (2004) The functional genomic distribution of protein divergence in two animal phyla: coevolution, genomic conflict, and constraint. Genome Res 14:802–811PubMedCentralCrossRefPubMedGoogle Scholar
  5. Church DM, Goodstadt L, Hillier LW, Zody MC, Goldstein S, She X, Bult CJ, Agarwala R, Cherry JL, DiCuccio M, Hlavina W, Kapustin Y, Meric P, Maglott D, Birtle Z et al (2009) Lineage-specific biology revealed by a finished genome assembly of the mouse. PLoS Biol 7:e1000112PubMedCentralCrossRefPubMedGoogle Scholar
  6. Ciccarelli FD, von Mering C, Suyama M, Harrington ED, Izaurralde E, Bork P (2005) Complex genomic rearrangements lead to novel primate gene function. Genome Res 15:343–351PubMedCentralCrossRefPubMedGoogle Scholar
  7. Clark NL, Aagaard JE, Swanson WJ (2006) Evolution of reproductive proteins from animals and plants. Reproduction 131:11–22CrossRefPubMedGoogle Scholar
  8. Conant GC, Wagner A (2003) Asymmetric sequence divergence of duplicate genes. Genome Res 13:2052–2058PubMedCentralCrossRefPubMedGoogle Scholar
  9. Conrad B, Antonarakis SE (2007) Gene duplication: a drive for phenotypic diversity and cause of human disease. Annu Rev Genomics Hum Genet 8:17–35CrossRefPubMedGoogle Scholar
  10. Cusack BP, Wolfe KH (2007) Not born equal: increased rate asymmetry in relocated and retrotransposed rodent gene duplicates. Mol Biol Evol 24:679–686CrossRefPubMedGoogle Scholar
  11. Elsik CG, Tellam RL, Worley KC, Gibbs RA, Muzny DM, Weinstock GM, Adelson DL, Eichler EE, Elnitski L, Guigo R, Hamernik DL, Kappes SM, Lewin HA, Lynn DJ, Nicholas FW et al (2009) The genome sequence of taurine cattle: a window to ruminant biology and evolution. Science 324:522–528PubMedCentralCrossRefPubMedGoogle Scholar
  12. Fletcher W, Yang Z (2010) The effect of insertions, deletions, and alignment errors on the branch-site test of positive selection. Mol Biol Evol 27:2257–2267CrossRefPubMedGoogle Scholar
  13. Friedman R, Hughes AL (2007) Likelihood-ratio tests for positive selection of human and mouse duplicate genes reveal nonconservative and anomalous properties of widely used methods. Mol Phylogenet Evol 42:388–393CrossRefPubMedGoogle Scholar
  14. Goodstadt L, Ponting CP (2006) Phylogenetic reconstruction of orthology, paralogy, and conserved synteny for dog and human. PLoS Comput Biol 2:e133PubMedCentralCrossRefPubMedGoogle Scholar
  15. Guindon S, Dufayard JF, Lefort V, Anisimova M, Hordijk W, Gascuel O (2010) New algorithms and methods to estimate maximum-likelihood phylogenies: assessing the performance of PhyML 3.0. Syst Biol 59:307–321CrossRefPubMedGoogle Scholar
  16. Haider S, Ballester B, Smedley D, Zhang J, Rice P, Kasprzyk A (2009) BioMart central portal—unified access to biological data. Nucleic Acids Res 37:W23–W27PubMedCentralCrossRefPubMedGoogle Scholar
  17. Han MV, Demuth JP, McGrath CL, Casola C, Hahn MW (2009) Adaptive evolution of young gene duplicates in mammals. Genome Res 19:859–867PubMedCentralCrossRefPubMedGoogle Scholar
  18. He X, Zhang J (2005) Rapid subfunctionalization accompanied by prolonged and substantial neofunctionalization in duplicate gene evolution. Genetics 169:1157–1164PubMedCentralCrossRefPubMedGoogle Scholar
  19. Hemond M, Rothstein TL, Wagner G (2009) Fas apoptosis inhibitory molecule contains a novel beta-sandwich in contact with a partially ordered domain. J Mol Biol 386:1024–1037PubMedCentralCrossRefPubMedGoogle Scholar
  20. Huo J, Xu S, Guo K, Zeng Q, Lam KP (2009) Genetic deletion of Faim reveals its role in modulating c-FLIP expression during CD95-mediated apoptosis of lymphocytes and hepatocytes. Cell Death Differ 16:1062–1070CrossRefPubMedGoogle Scholar
  21. Jun J, Ryvkin P, Hemphill E, Nelson C (2009) Duplication mechanism and disruptions in flanking regions determine the fate of Mammalian gene duplicates. J Comput Biol 16:1253–1266CrossRefPubMedGoogle Scholar
  22. Kaessmann H, Vinckenbosch N, Long M (2009) RNA-based gene duplication: mechanistic and evolutionary insights. Nat Rev Genet 10:19–31PubMedCentralCrossRefPubMedGoogle Scholar
  23. 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 30:3059–3066PubMedCentralCrossRefPubMedGoogle Scholar
  24. Krasnov AN, Kurshakova MM, Ramensky VE, Mardanov PV, Nabirochkina EN, Georgieva SG (2005) A retrocopy of a gene can functionally displace the source gene in evolution. Nucleic Acids Res 33:6654–6661PubMedCentralCrossRefPubMedGoogle Scholar
  25. Lander ES, Linton LM, Birren B, Nusbaum C, Zody MC, Baldwin J, Devon K, Dewar K, Doyle M, FitzHugh W, Funke R, Gage D, Harris K, Heaford A, Howland J et al (2001) Initial sequencing and analysis of the human genome. Nature 409:860–921CrossRefPubMedGoogle Scholar
  26. Liao BY, Scott NM, Zhang J (2006) Impacts of gene essentiality, expression pattern, and gene compactness on the evolutionary rate of mammalian proteins. Mol Biol Evol 23:2072–2080CrossRefPubMedGoogle Scholar
  27. Lynch M (2002) Genomics. Gene duplication and evolution. Science 297:945–947CrossRefPubMedGoogle Scholar
  28. Nozawa M, Suzuki Y, Nei M (2009) Reliabilities of identifying positive selection by the branch-site and the site-prediction methods. Proc Natl Acad Sci USA 106:6700–6705PubMedCentralCrossRefPubMedGoogle Scholar
  29. Panhuis TM, Clark NL, Swanson WJ (2006) Rapid evolution of reproductive proteins in abalone and Drosophila. Philos Trans R Soc Lond B Biol Sci 361:261–268PubMedCentralCrossRefPubMedGoogle Scholar
  30. Pegueroles C, Laurie S, Alba MM (2013) Accelerated evolution after gene duplication: a time-dependent process affecting just one copy. Mol Biol Evol 30:1830–1842CrossRefPubMedGoogle Scholar
  31. Pohl AA, Sugnet CW, Clark TA, Smith K, Fujita PA, Cline MS (2009) Affy exon tissues: exon levels in normal tissues in human, mouse and rat. Bioinformatics 25:2442–2443PubMedCentralCrossRefPubMedGoogle Scholar
  32. Pond SL, Frost SD, Muse SV (2005) HyPhy: hypothesis testing using phylogenies. Bioinformatics 21:676–679CrossRefPubMedGoogle Scholar
  33. Prasad AB, Allard MW, Green ED (2008) Confirming the phylogeny of mammals by use of large comparative sequence data sets. Mol Biol Evol 25:1795–1808PubMedCentralCrossRefPubMedGoogle Scholar
  34. Rothstein TL, Zhong X, Schram BR, Negm RS, Donohoe TJ, Cabral DS, Foote LC, Schneider TJ (2000) Receptor-specific regulation of B-cell susceptibility to Fas-mediated apoptosis and a novel Fas apoptosis inhibitory molecule. Immunol Rev 176:116–133CrossRefPubMedGoogle Scholar
  35. Sanborn JZ, Benz SC, Craft B, Szeto C, Kober KM, Meyer L, Vaske CJ, Goldman M, Smith KE, Kuhn RM, Karolchik D, Kent WJ, Stuart JM, Haussler D, Zhu J (2011) The UCSC Cancer Genomics Browser: update 2011. Nucleic Acids Res 39:D951–D959PubMedCentralCrossRefPubMedGoogle Scholar
  36. Sapiro R, Tarantino LM, Velazquez F, Kiriakidou M, Hecht NB, Bucan M, Strauss JF 3rd (2000) Sperm antigen 6 is the murine homologue of the Chlamydomonas reinhardtii central apparatus protein encoded by the PF16 locus. Biol Reprod 62:511–518CrossRefPubMedGoogle Scholar
  37. Sapiro R, Kostetskii I, Olds-Clarke P, Gerton GL, Radice GL, Strauss IJ (2002) Male infertility, impaired sperm motility, and hydrocephalus in mice deficient in sperm-associated antigen 6. Mol Cell Biol 22:6298–6305PubMedCentralCrossRefPubMedGoogle Scholar
  38. Sawyer S (1989) Statistical tests for detecting gene conversion. Mol Biol Evol 6:526–538PubMedGoogle Scholar
  39. Schwartz S, Kent WJ, Smit A, Zhang Z, Baertsch R, Hardison RC, Haussler D, Miller W (2003) Human-mouse alignments with BLASTZ. Genome Res 13:103–107PubMedCentralCrossRefPubMedGoogle Scholar
  40. Segura MF, Sole C, Pascual M, Moubarak RS, Perez-Garcia MJ, Gozzelino R, Iglesias V, Badiola N, Bayascas JR, Llecha N, Rodriguez-Alvarez J, Soriano E, Yuste VJ, Comella JX (2007) The long form of Fas apoptotic inhibitory molecule is expressed specifically in neurons and protects them against death receptor-triggered apoptosis. J Neurosci 27:11228–11241CrossRefPubMedGoogle Scholar
  41. Su AI, Wiltshire T, Batalov S, Lapp H, Ching KA, Block D, Zhang J, Soden R, Hayakawa M, Kreiman G, Cooke MP, Walker JR, Hogenesch JB (2004) A gene atlas of the mouse and human protein-encoding transcriptomes. Proc Natl Acad Sci USA 101:6062–6067PubMedCentralCrossRefPubMedGoogle Scholar
  42. Talavera G, Castresana J (2007) Improvement of phylogenies after removing divergent and ambiguously aligned blocks from protein sequence alignments. Syst Biol 56:564–577CrossRefPubMedGoogle Scholar
  43. Tamura K, Peterson D, Peterson N, Stecher G, Nei M, Kumar S (2011) MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Mol Biol Evol 28:2731–2739PubMedCentralCrossRefPubMedGoogle Scholar
  44. Taylor JS, Van de Peer Y, Meyer A (2001) Genome duplication, divergent resolution and speciation. Trends Genet 17:299–301CrossRefPubMedGoogle Scholar
  45. Vilella AJ, Severin J, Ureta-Vidal A, Heng L, Durbin R, Birney E (2009) EnsemblCompara GeneTrees: complete, duplication-aware phylogenetic trees in vertebrates. Genome Res 19:327–335PubMedCentralCrossRefPubMedGoogle Scholar
  46. Wu C, Orozco C, Boyer J, Leglise M, Goodale J, Batalov S, Hodge CL, Haase J, Janes J, Huss JW 3rd, Su AI (2009) BioGPS: an extensible and customizable portal for querying and organizing gene annotation resources. Genome Biol 10:R130PubMedCentralCrossRefPubMedGoogle Scholar
  47. Xu X, Nagarajan H, Lewis NE, Pan S, Cai Z, Liu X, Chen W, Xie M, Wang W, Hammond S, Andersen MR, Neff N, Passarelli B, Koh W, Fan HC et al (2011) The genomic sequence of the Chinese hamster ovary (CHO)-K1 cell line. Nat Biotechnol 29:735–741PubMedCentralCrossRefPubMedGoogle Scholar
  48. Yang Z (2007) PAML 4: phylogenetic analysis by maximum likelihood. Mol Biol Evol 24:1586–1591CrossRefPubMedGoogle Scholar
  49. Yang Z, dos Reis M (2011) Statistical properties of the branch-site test of positive selection. Mol Biol Evol 28:1217–1228CrossRefPubMedGoogle Scholar
  50. Yang Z, Nielsen R, Goldman N, Pedersen AM (2000) Codon-substitution models for heterogeneous selection pressure at amino acid sites. Genetics 155:431–449PubMedCentralPubMedGoogle Scholar
  51. Yang Z, Wong WS, Nielsen R (2005) Bayes empirical bayes inference of amino acid sites under positive selection. Mol Biol Evol 22:1107–1118CrossRefPubMedGoogle Scholar
  52. Zhai W, Nielsen R, Goldman N, Yang Z (2012) Looking for darwin in genomic sequences–validity and success of statistical methods. Mol Biol Evol 29:2889–2893CrossRefPubMedGoogle Scholar
  53. Zhang J (2003) Evolution by gene duplication: an update. Trends Ecol Evol 18:292–298CrossRefGoogle Scholar
  54. Zhang J, Nielsen R, Yang Z (2005) Evaluation of an improved branch-site likelihood method for detecting positive selection at the molecular level. Mol Biol Evol 22:2472–2479CrossRefPubMedGoogle Scholar
  55. Zhong X, Schneider TJ, Cabral DS, Donohoe TJ, Rothstein TL (2001) An alternatively spliced long form of Fas apoptosis inhibitory molecule (FAIM) with tissue-specific expression in the brain. Mol Immunol 38:65–72CrossRefPubMedGoogle Scholar

Copyright information

© Springer Science+Business Media New York 2013

Authors and Affiliations

  • Huan Qiu
    • 1
    • 3
  • Aniela Gołas
    • 2
  • Paweł Grzmil
    • 2
  • Leszek Wojnowski
    • 1
  1. 1.Department of PharmacologyUniversity Medical Center of the Johannes Gutenberg University MainzMainzGermany
  2. 2.Department of Genetics and Evolution, Institute of ZoologyJagiellonian UniversityKrakówPoland
  3. 3.Department of Ecology, Evolution and Natural ResourcesRutgers UniversityNew BrunswickUSA

Personalised recommendations