Rhodopsin gene copies in Japanese eel originated in a teleost-specific genome duplication.

Yoji Nakamura, Motoshige Yasuike, Miyuki Mekuchi, Yuki Iwasaki, Nobuhiko Ojima, Atushi Fujiwara, Seinen Chow, Kenji Saitoh
Author Information
  1. Yoji Nakamura: Research Center for Bioinformatics and Biosciences, National Research Institute of Fisheries Science, Japan Fisheries Research and Education Agency, 2-12-4 Fukuura, Kanazawa, Yokohama, Kanagawa 236-8648 Japan. ORCID
  2. Motoshige Yasuike: Research Center for Bioinformatics and Biosciences, National Research Institute of Fisheries Science, Japan Fisheries Research and Education Agency, 2-12-4 Fukuura, Kanazawa, Yokohama, Kanagawa 236-8648 Japan.
  3. Miyuki Mekuchi: Research Center for Bioinformatics and Biosciences, National Research Institute of Fisheries Science, Japan Fisheries Research and Education Agency, 2-12-4 Fukuura, Kanazawa, Yokohama, Kanagawa 236-8648 Japan.
  4. Yuki Iwasaki: Research Center for Bioinformatics and Biosciences, National Research Institute of Fisheries Science, Japan Fisheries Research and Education Agency, 2-12-4 Fukuura, Kanazawa, Yokohama, Kanagawa 236-8648 Japan.
  5. Nobuhiko Ojima: Research Center for Bioinformatics and Biosciences, National Research Institute of Fisheries Science, Japan Fisheries Research and Education Agency, 2-12-4 Fukuura, Kanazawa, Yokohama, Kanagawa 236-8648 Japan.
  6. Atushi Fujiwara: Research Center for Bioinformatics and Biosciences, National Research Institute of Fisheries Science, Japan Fisheries Research and Education Agency, 2-12-4 Fukuura, Kanazawa, Yokohama, Kanagawa 236-8648 Japan.
  7. Seinen Chow: Research Center for Bioinformatics and Biosciences, National Research Institute of Fisheries Science, Japan Fisheries Research and Education Agency, 2-12-4 Fukuura, Kanazawa, Yokohama, Kanagawa 236-8648 Japan.
  8. Kenji Saitoh: Research Center for Bioinformatics and Biosciences, National Research Institute of Fisheries Science, Japan Fisheries Research and Education Agency, 2-12-4 Fukuura, Kanazawa, Yokohama, Kanagawa 236-8648 Japan.

Abstract

BACKGROUND: Gene duplication is considered important to increasing the genetic diversity in animals. In fish, visual pigment genes are often independently duplicated, and the evolutionary significance of such duplications has long been of interest. Eels have two rhodopsin genes (), one of which (freshwater type, ) functions in freshwater and the other (deep-sea type, ) in marine environments. Hence, switching of expression in retinal cells is tightly linked with eels' unique life cycle, in which they migrate from rivers or lakes to the sea. These genes are apparently paralogous, but the timing of their duplication is unclear due to the deep-branching phylogeny. The aim of the present study is to elucidate the evolutionary origin of the two copies in eels using comparative genomics methods.
RESULTS: In the present study, we sequenced the genome of Japanese eel and reconstructed two regions containing by de novo assembly. We found a single corresponding region in a non-teleostean primitive ray-finned fish (spotted gar) and two regions in a primitive teleost (Asian arowana). The order of and the neighboring genes was highly conserved among the three species. With respect to , which was lost in Asian arowana, the neighboring genes were also syntenic between Japanese eel and Asian arowana. In particular, the pattern of gene losses in and regions was the same as that in Asian arowana, and no discrepancy was found in any of the teleost genomes examined. Phylogenetic analysis supports mutual monophyly of these two teleostean synteny groups, which correspond to the and regions.
CONCLUSIONS: Syntenic and phylogenetic analyses suggest that the duplication of rhodopsin gene in Japanese eel predated the divergence of eel (Elopomorpha) and arowana (Osteoglossomorpha). Thus, based on the principle of parsimony, it is most likely that the rhodopsin paralogs were generated through a whole genome duplication in the ancestor of teleosts, and have remained till the present in eels with distinct functional roles. Our result indicates, for the first time, that teleost-specific genome duplication may have contributed to a gene innovation involved in eel-specific migratory life cycle.

Keywords

References

  1. Biophysics (Oxf). 2010 Jan 1;6:67-68 [PMID: 21297892]
  2. Proc Natl Acad Sci U S A. 2013 Jul 2;110(27):11061-6 [PMID: 23781100]
  3. Genome Res. 2003 Sep;13(9):2178-89 [PMID: 12952885]
  4. J Exp Zool B Mol Dev Evol. 2010 Mar 15;314(2):135-47 [PMID: 19670462]
  5. Mol Phylogenet Evol. 2015 Aug;89:205-18 [PMID: 25899306]
  6. Bioinformatics. 2011 Mar 15;27(6):764-70 [PMID: 21217122]
  7. Proc Natl Acad Sci U S A. 2016 Oct 11;113(41):11531-11536 [PMID: 27671652]
  8. Proc Natl Acad Sci U S A. 2004 Feb 10;101(6):1638-43 [PMID: 14757817]
  9. Folia Biol (Krakow). 2003;51 Suppl:101-5 [PMID: 15303348]
  10. Nucleic Acids Res. 2016 Jan 4;44(D1):D710-6 [PMID: 26687719]
  11. Methods Mol Biol. 2009;537:39-64 [PMID: 19378139]
  12. Bioinformatics. 2001 Dec;17(12):1246-7 [PMID: 11751242]
  13. Mol Phylogenet Evol. 2012 Mar;62(3):986-1008 [PMID: 22178363]
  14. BMC Evol Biol. 2013 Nov 02;13:238 [PMID: 24180662]
  15. Dev Suppl. 1994;:125-33 [PMID: 7579513]
  16. Gen Comp Endocrinol. 2016 Sep 1;235:177-191 [PMID: 26654744]
  17. Proc Natl Acad Sci U S A. 1999 Aug 31;96(18):10267-71 [PMID: 10468597]
  18. PLoS One. 2017 Feb 27;12(2):e0173053 [PMID: 28241055]
  19. Bioinformatics. 2011 Feb 15;27(4):578-9 [PMID: 21149342]
  20. Biodivers Data J. 2016 Sep 01;(4):e10356 [PMID: 27660524]
  21. Mol Phylogenet Evol. 2001 Aug;20(2):275-85 [PMID: 11476635]
  22. Science. 2000 Nov 10;290(5494):1151-5 [PMID: 11073452]
  23. Nat Biotechnol. 2010 May;28(5):511-5 [PMID: 20436464]
  24. Bioinformatics. 2008 Mar 1;24(5):637-44 [PMID: 18218656]
  25. Genome Biol. 2004;5(2):R12 [PMID: 14759262]
  26. Bioinformatics. 2014 May 1;30(9):1236-40 [PMID: 24451626]
  27. BMC Bioinformatics. 2005 Feb 15;6:31 [PMID: 15713233]
  28. Mol Biol Evol. 2009 Jan;26(1):47-59 [PMID: 18842688]
  29. Brain Res Mol Brain Res. 1999 Nov 10;73(1-2):110-8 [PMID: 10581404]
  30. PLoS Curr. 2013 Apr 16;5: [PMID: 23788273]
  31. Nat Commun. 2011 Feb 01;2: [PMID: 21285957]
  32. PLoS One. 2014 Jul 28;9(7):e102089 [PMID: 25069045]
  33. Proc Natl Acad Sci U S A. 2015 Dec 1;112(48):14918-23 [PMID: 26578810]
  34. Sci Adv. 2016 Sep 05;2(10):e1501694 [PMID: 27713924]
  35. PLoS One. 2012;7(2):e32231 [PMID: 22384188]
  36. PLoS Biol. 2005 Oct;3(10):e314 [PMID: 16128622]
  37. Sci Data. 2016 Dec 06;3:160105 [PMID: 27922628]
  38. Trends Genet. 2009 May;25(5):198-202 [PMID: 19362746]
  39. Mol Biol Evol. 2007 Aug;24(8):1586-91 [PMID: 17483113]
  40. In Vitro Cell Dev Biol Anim. 2012 Sep;48(8):507-17 [PMID: 22956044]
  41. BMC Genomics. 2014 Mar 26;15:233 [PMID: 24669946]
  42. Sci Rep. 2017 Aug 3;7(1):7213 [PMID: 28775309]
  43. J Comp Physiol A. 1985 Oct;157(3):323-33 [PMID: 3837092]
  44. J Exp Biol. 2007 Aug;210(Pt 16):2829-35 [PMID: 17690230]
  45. Philos Trans R Soc Lond B Biol Sci. 2001 Oct 29;356(1414):1661-79 [PMID: 11604130]
  46. Mol Genet Genomics. 2014 Dec;289(6):1045-60 [PMID: 25092473]
  47. Genome Biol. 2012 Jun 25;13(6):R56 [PMID: 22731987]
  48. Mol Phylogenet Evol. 2013 Dec;69(3):884-94 [PMID: 23831455]
  49. Comp Biochem Physiol A Mol Integr Physiol. 2017 Jan;203:91-99 [PMID: 27590411]
  50. BMC Bioinformatics. 2010 May 27;11:284 [PMID: 20507581]
  51. Mol Phylogenet Evol. 2014 Jan;70:152-61 [PMID: 24041936]
  52. Genome Biol. 2017 Jun 14;18(1):111 [PMID: 28615063]
  53. Mol Biol Evol. 2013 Dec;30(12):2725-9 [PMID: 24132122]
  54. J Mol Evol. 2004 Aug;59(2):190-203 [PMID: 15486693]
  55. Nat Methods. 2012 Mar 04;9(4):357-9 [PMID: 22388286]
  56. Genes Genet Syst. 1999 Oct;74(5):211-7 [PMID: 10734603]
  57. Proc Biol Sci. 1995 Dec 22;262(1365):289-95 [PMID: 8587887]
  58. Proc Biol Sci. 1998 May 22;265(1399):869-74 [PMID: 9633112]
  59. Mol Phylogenet Evol. 2003 Feb;26(2):262-88 [PMID: 12565036]
  60. FEBS Lett. 2000 Mar 3;469(1):39-43 [PMID: 10708752]
  61. Nucleic Acids Res. 1997 Sep 1;25(17):3389-402 [PMID: 9254694]
  62. Proc Natl Acad Sci U S A. 2008 Sep 9;105(36):13480-5 [PMID: 18768804]
  63. J Exp Biol. 2017 Jan 15;220(Pt 2):294-303 [PMID: 27811293]
  64. BMC Evol Biol. 2008 Dec 18;8:336 [PMID: 19094205]
  65. Genome Biol. 2013 Apr 25;14(4):R36 [PMID: 23618408]
  66. J Exp Biol. 2008 Dec;211(Pt 24):3879-88 [PMID: 19043060]
  67. Nat Protoc. 2013 Aug;8(8):1494-512 [PMID: 23845962]
  68. Mol Biol Evol. 2016 Jan;33(1):228-44 [PMID: 26507457]
  69. Vis Neurosci. 2011 Jul;28(4):325-35 [PMID: 21447259]
  70. Biol Lett. 2010 Jun 23;6(3):363-6 [PMID: 20053660]

Word Cloud

Created with Highcharts 10.0.0duplicationgenestwogenomeeelarowanaJapaneseregionsAsiangenerhodopsinpresentGenefishevolutionaryfreshwatertypelifecyclestudycopieseelsfoundprimitiveteleostneighboringparalogsteleost-specificRhodopsinBACKGROUND:consideredimportantincreasinggeneticdiversityanimalsvisualpigmentoftenindependentlyduplicatedsignificanceduplicationslonginterestEelsonefunctionsdeep-seamarineenvironmentsHenceswitchingexpressionretinalcellstightlylinkedeels'uniquemigrateriverslakesseaapparentlyparalogoustimingunclearduedeep-branchingphylogenyaimelucidateoriginusingcomparativegenomicsmethodsRESULTS:sequencedreconstructedcontainingdenovoassemblysinglecorrespondingregionnon-teleosteanray-finnedspottedgarorderhighlyconservedamongthreespeciesrespectlostalsosyntenicparticularpatternlossesdiscrepancygenomesexaminedPhylogeneticanalysissupportsmutualmonophylyteleosteansyntenygroupscorrespondCONCLUSIONS:SyntenicphylogeneticanalysessuggestpredateddivergenceElopomorphaOsteoglossomorphaThusbasedprincipleparsimonylikelygeneratedwholeancestorteleostsremainedtilldistinctfunctionalrolesresultindicatesfirsttimemaycontributedinnovationinvolvedeel-specificmigratoryoriginatedAnguillalossPhylogenomicsSyntenyTeleosteiVisualadaptationWhole

Similar Articles

Cited By