Molecular evolution of candidate male reproductive genes in the brown algal model Ectocarpus.

Agnieszka P Lipinska, Els J M Van Damme, Olivier De Clerck
Author Information
  1. Agnieszka P Lipinska: Phycology Research Group and Center for Molecular Phylogenetics and Evolution, Ghent University, Krijgslaan 281, Building S8, 9000, Ghent, Belgium. ap.lipinska@gmail.com.
  2. Els J M Van Damme: Department of Molecular Biotechnology, Laboratory of Biochemistry and Glycobiology, Ghent University, Coupure Links 653, 9000, Ghent, Belgium. ElsJM.VanDamme@UGent.be.
  3. Olivier De Clerck: Phycology Research Group and Center for Molecular Phylogenetics and Evolution, Ghent University, Krijgslaan 281, Building S8, 9000, Ghent, Belgium. olivier.declerck@ugent.be.

Abstract

BACKGROUND: Evolutionary studies of genes that mediate recognition between sperm and egg contribute to our understanding of reproductive isolation and speciation. Surface receptors involved in fertilization are targets of sexual selection, reinforcement, and other evolutionary forces including positive selection. This observation was made across different lineages of the eukaryotic tree from land plants to mammals, and is particularly evident in free-spawning animals. Here we use the brown algal model species Ectocarpus (Phaeophyceae) to investigate the evolution of candidate gamete recognition proteins in a distant major phylogenetic group of eukaryotes.
RESULTS: Male gamete specific genes were identified by comparing transcriptome data covering different stages of the Ectocarpus life cycle and screened for characteristics expected from gamete recognition receptors. Selected genes were sequenced in a representative number of strains from distant geographical locations and varying stages of reproductive isolation, to search for signatures of adaptive evolution. One of the genes (Esi0130_0068) showed evidence of selective pressure. Interestingly, that gene displayed domain similarities to the receptor for egg jelly (REJ) protein involved in sperm-egg recognition in sea urchins.
CONCLUSIONS: We have identified a male gamete specific gene with similarity to known gamete recognition receptors and signatures of adaptation. Altogether, this gene could contribute to gamete interaction during reproduction as well as reproductive isolation in Ectocarpus and is therefore a good candidate for further functional evaluation.

References

  1. BMC Bioinformatics. 2008;9:393 [PMID: 18811941]
  2. Heredity (Edinb). 2009 Jan;102(1):66-76 [PMID: 19018273]
  3. Nat Protoc. 2009;4(3):363-71 [PMID: 19247286]
  4. Biol Lett. 2009 Jun 23;5(3):409-12 [PMID: 19433612]
  5. Mol Biol Evol. 2007 Aug;24(8):1586-91 [PMID: 17483113]
  6. Nat Rev Genet. 2007 Sep;8(9):689-98 [PMID: 17680007]
  7. Bioinformatics. 2007 Nov 1;23(21):2947-8 [PMID: 17846036]
  8. Mol Biol Evol. 2007 Dec;24(12):2698-706 [PMID: 17893399]
  9. Dev Growth Differ. 2008 Jun;50 Suppl 1:S221-38 [PMID: 18494705]
  10. Int J Dev Biol. 2008;52(5-6):769-80 [PMID: 18649289]
  11. Syst Biol. 2008 Oct;57(5):758-71 [PMID: 18853362]
  12. J Mol Evol. 1981;17(6):368-76 [PMID: 7288891]
  13. Proc Natl Acad Sci U S A. 1986 Dec;83(23):9055-9 [PMID: 3466177]
  14. Mol Biol Evol. 1995 Mar;12(2):231-8 [PMID: 7700151]
  15. J Mol Evol. 1995 Dec;41(6):1085-95 [PMID: 8587107]
  16. Mol Biol Evol. 1996 Feb;13(2):397-406 [PMID: 8587504]
  17. J Cell Biol. 1996 May;133(4):809-17 [PMID: 8666666]
  18. Proc Natl Acad Sci U S A. 1997 Aug 5;94(16):8634-9 [PMID: 9238029]
  19. Nucleic Acids Res. 1997 Sep 1;25(17):3389-402 [PMID: 9254694]
  20. Dev Biol. 1997 Dec 1;192(1):125-35 [PMID: 9405102]
  21. Mol Biol Evol. 1998 May;15(5):568-73 [PMID: 9580986]
  22. Mol Biol Evol. 1998 Jul;15(7):901-9 [PMID: 9656489]
  23. Science. 1998 Jul 31;281(5377):710-2 [PMID: 9685267]
  24. Proc Natl Acad Sci U S A. 2001 Feb 27;98(5):2509-14 [PMID: 11226269]
  25. Appl Environ Microbiol. 2001 Aug;67(8):3501-13 [PMID: 11472926]
  26. Proc Natl Acad Sci U S A. 2002 Dec 24;99(26):16981-6 [PMID: 12482949]
  27. Proc Natl Acad Sci U S A. 2003 Apr 15;100(8):4639-43 [PMID: 12676995]
  28. Mol Biol Evol. 2003 Aug;20(8):1326-8 [PMID: 12777506]
  29. Science. 2004 Feb 13;303(5660):971-5 [PMID: 14963320]
  30. J Cell Sci. 1979 Apr;36:19-30 [PMID: 457806]
  31. J Cell Sci. 1980 Jun;43:209-24 [PMID: 7191429]
  32. Proc Int Conf Intell Syst Mol Biol. 1998;6:175-82 [PMID: 9783223]
  33. Hum Mol Genet. 1999 Mar;8(3):543-9 [PMID: 9949214]
  34. Mol Biol Evol. 1999 Jun;16(6):839-48 [PMID: 10368961]
  35. Appl Environ Microbiol. 1999 Jul;65(7):3121-8 [PMID: 10388712]
  36. Mol Biol Evol. 2005 Mar;22(3):533-41 [PMID: 15525699]
  37. Bioinformatics. 2005 Mar 1;21(5):676-9 [PMID: 15509596]
  38. Bioinformatics. 2005 Sep 15;21(18):3674-6 [PMID: 16081474]
  39. PLoS Genet. 2009 Jul;5(7):e1000570 [PMID: 19629160]
  40. Nature. 2010 Jun 3;465(7298):617-21 [PMID: 20520714]
  41. New Phytol. 2010 Oct;188(1):1-4 [PMID: 20840144]
  42. Bioinformatics. 2010 Oct 1;26(19):2455-7 [PMID: 20671151]
  43. Protist. 2011 Jan;162(1):100-14 [PMID: 20663714]
  44. BMC Evol Biol. 2011;11:18 [PMID: 21247489]
  45. Proc Natl Acad Sci U S A. 2011 Aug 16;108(33):13624-9 [PMID: 21810989]
  46. Cold Spring Harb Perspect Biol. 2011 Nov;3(11):a002931 [PMID: 21730046]
  47. Mol Ecol. 2012 Jan;21(1):130-44 [PMID: 21981354]
  48. Cold Spring Harb Protoc. 2012 Feb;2012(2):193-8 [PMID: 22301644]
  49. Syst Biol. 2012 May;61(3):539-42 [PMID: 22357727]
  50. Evolution. 2012 Jun;66(6):1675-80 [PMID: 22671538]
  51. PLoS Genet. 2012;8(7):e1002764 [PMID: 22807683]
  52. Nucleic Acids Res. 2012 Aug;40(15):e115 [PMID: 22730293]
  53. Nat Methods. 2012 Nov;9(11):1041 [PMID: 23132114]
  54. Mol Biol Evol. 2013 Dec;30(12):2725-9 [PMID: 24132122]
  55. BMC Genomics. 2013;14:909 [PMID: 24359479]
  56. Mol Biol Evol. 2014 Jan;31(1):212-31 [PMID: 24129904]
  57. Mol Biol Evol. 2014 Mar;31(3):574-83 [PMID: 24273323]
  58. Evolution. 2014 May;68(5):1294-305 [PMID: 24410379]
  59. Mol Hum Reprod. 2014 Dec;20(12):1190-7 [PMID: 25323969]
  60. Mol Biol Evol. 2015 Jun;32(6):1581-97 [PMID: 25725430]
  61. Genetics. 2000 May;155(1):431-49 [PMID: 10790415]
  62. J Mol Evol. 2000 Nov;51(5):423-32 [PMID: 11080365]
  63. J Mol Biol. 2001 Jan 19;305(3):567-80 [PMID: 11152613]
  64. Plant Physiol. 2001 Feb;125(2):1012-22 [PMID: 11161057]
  65. Reproduction. 2006 Jan;131(1):11-22 [PMID: 16388004]
  66. PLoS Genet. 2005 Sep;1(3):e35 [PMID: 16170411]
  67. J Mol Evol. 2006 Aug;63(2):231-9 [PMID: 16830090]
  68. Curr Biol. 2006 Sep 5;16(17):R744-54 [PMID: 16950101]
  69. Protist. 2007 Jan;158(1):77-88 [PMID: 17126076]
  70. Bioinformatics. 2007 May 15;23(10):1289-91 [PMID: 17379693]
  71. Am J Hum Genet. 2007 Jul;81(1):44-52 [PMID: 17564962]
  72. BMC Genomics. 2007;8:235 [PMID: 17629917]

MeSH Term

Biological Evolution
Evolution, Molecular
Fertilization
Ovule
Phaeophyceae
Phylogeny
Pollen
Selection, Genetic

Word Cloud

Created with Highcharts 10.0.0gametegenesrecognitionreproductiveEctocarpusisolationreceptorsevolutioncandidategeneeggcontributeinvolvedselectiondifferentbrownalgalmodeldistantspecificidentifiedstagessignaturesmaleBACKGROUND:EvolutionarystudiesmediatespermunderstandingspeciationSurfacefertilizationtargetssexualreinforcementevolutionaryforcesincludingpositiveobservationmadeacrosslineageseukaryotictreelandplantsmammalsparticularlyevidentfree-spawninganimalsusespeciesPhaeophyceaeinvestigateproteinsmajorphylogeneticgroupeukaryotesRESULTS:MalecomparingtranscriptomedatacoveringlifecyclescreenedcharacteristicsexpectedSelectedsequencedrepresentativenumberstrainsgeographicallocationsvaryingsearchadaptiveOneEsi0130_0068showedevidenceselectivepressureInterestinglydisplayeddomainsimilaritiesreceptorjellyREJproteinsperm-eggseaurchinsCONCLUSIONS:similarityknownadaptationAltogetherinteractionreproductionwellthereforegoodfunctionalevaluationMolecular

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