Display options
Share it on

Evodevo. 2015 Sep 16;6:27. doi: 10.1186/s13227-015-0022-6. eCollection 2015.

Differential expression of the aryl hydrocarbon receptor pathway associates with craniofacial polymorphism in sympatric Arctic charr.

EvoDevo

Ehsan Pashay Ahi, Sophie S Steinhäuser, Arnar Pálsson, Sigrídur Rut Franzdóttir, Sigurdur S Snorrason, Valerie H Maier, Zophonías O Jónsson

Affiliations

  1. Institute of Life and Environmental Sciences, University of Iceland, Sturlugata 7, 101 Reykjavik, Iceland.
  2. Biomedical Center, University of Iceland, Vatnsmýrarvegur 16, 101 Reykjavik, Iceland.
  3. Institute of Life and Environmental Sciences, University of Iceland, Sturlugata 7, 101 Reykjavik, Iceland ; Biomedical Center, University of Iceland, Vatnsmýrarvegur 16, 101 Reykjavik, Iceland.

PMID: 26388986 PMCID: PMC4574265 DOI: 10.1186/s13227-015-0022-6

Abstract

BACKGROUND: The developmental basis of craniofacial morphology hinges on interactions of numerous signalling systems. Extensive craniofacial variation in the polymorphic Arctic charr, a member of the salmonid family, from Lake Thingvallavatn (Iceland), offers opportunities to find and study such signalling pathways and their key regulators, thereby shedding light on the developmental pathways, and the genetics of trophic divergence.

RESULTS: To identify genes involved in the craniofacial differences between benthic and limnetic Arctic charr, we used transcriptome data from different morphs, spanning early development, together with data on craniofacial expression patterns and skeletogenesis in model vertebrate species. Out of 20 genes identified, 7 showed lower gene expression in benthic than in limnetic charr morphs. We had previously identified a conserved gene network involved in extracellular matrix (ECM) organization and skeletogenesis, showing higher expression in developing craniofacial elements of benthic than in limnetic Arctic charr morphs. The present study adds a second set of genes constituting an expanded gene network with strong, benthic-limnetic differential expression. To identify putative upstream regulators, we performed knowledge-based motif enrichment analyses on the regulatory sequences of the identified genes which yielded potential binding sites for a set of known transcription factors (TFs). Of the 8 TFs that we examined using qPCR, two (Ahr2b and Ap2) were found to be differentially expressed between benthic and limnetic charr. Expression analysis of several known AhR targets indicated higher activity of the AhR pathway during craniofacial development in benthic charr morphotypes.

CONCLUSION: These results suggest a key role of the aryl hydrocarbon receptor (AhR) pathway in the observed craniofacial differences between distinct charr morphotypes.

References

  1. Nat Rev Genet. 2007 Jun;8(6):450-61 - PubMed
  2. Am J Hum Genet. 2014 Jan 2;94(1):62-72 - PubMed
  3. Evol Dev. 2010 May-Jun;12(3):246-57 - PubMed
  4. Chem Res Toxicol. 2010 Mar 15;23(3):480-7 - PubMed
  5. Proc Natl Acad Sci U S A. 2005 Nov 8;102(45):16287-92 - PubMed
  6. Biochem Biophys Res Commun. 2002 Mar 15;291(5):1194-200 - PubMed
  7. Science. 2015 Feb 6;347(6222):664-7 - PubMed
  8. Am J Hum Genet. 2012 Feb 10;90(2):369-77 - PubMed
  9. Crit Rev Oral Biol Med. 2002;13(4):308-22 - PubMed
  10. Chem Biol. 2014 Apr 24;21(4):488-501 - PubMed
  11. Evodevo. 2014 Nov 03;5(1):40 - PubMed
  12. Mol Cell Biol. 2006 Oct;26(19):7201-10 - PubMed
  13. Dev Biol. 2014 Dec 1;396(1):94-106 - PubMed
  14. Blood Cells Mol Dis. 2010 Apr 15;44(4):199-206 - PubMed
  15. Mol Ecol. 2014 Sep;23(18):4511-26 - PubMed
  16. Toxicology. 2011 Jan 11;279(1-3):146-54 - PubMed
  17. F1000Res. 2015 Jun 01;4:136 - PubMed
  18. Chem Res Toxicol. 2008 Jan;21(1):102-16 - PubMed
  19. PLoS One. 2010 Sep 08;5(9):e12626 - PubMed
  20. Nature. 2004 Apr 15;428(6984):717-23 - PubMed
  21. Proc Natl Acad Sci U S A. 2014 Jun 10;111(23):8530-4 - PubMed
  22. Mech Dev. 2006 Dec;123(12):925-40 - PubMed
  23. Nucleic Acids Res. 2013 Jul;41(Web Server issue):W77-83 - PubMed
  24. Trends Genet. 2013 Jun;29(6):358-66 - PubMed
  25. Int J Dev Biol. 2009;53(7):1097-104 - PubMed
  26. Proc Natl Acad Sci U S A. 2005 Apr 5;102(14):4936-42 - PubMed
  27. Methods. 2010 Apr;50(4):323-35 - PubMed
  28. Cell. 1986 Sep 26;46(7):1063-73 - PubMed
  29. BMC Evol Biol. 2010 Jan 06;10:4 - PubMed
  30. Mol Ecol. 2013 Feb;22(3):650-69 - PubMed
  31. Toxicol Pathol. 2008 Dec;36(7):1006-13 - PubMed
  32. Development. 2010 Aug;137(16):2723-31 - PubMed
  33. PLoS One. 2013 Jul 24;8(7):e69402 - PubMed
  34. Nat Commun. 2014 Apr 03;5:3629 - PubMed
  35. Biochem Biophys Res Commun. 2010 Nov 12;402(2):335-9 - PubMed
  36. Mol Biol Evol. 2013 Jun;30(6):1384-96 - PubMed
  37. BMC Genomics. 2014 Feb 19;15:141 - PubMed
  38. J Bone Miner Res. 2013 Sep;28(9):1950-61 - PubMed
  39. Dev Biol. 2006 Aug 1;296(1):83-93 - PubMed
  40. PLoS One. 2013;8(1):e54363 - PubMed
  41. Aquat Toxicol. 2008 Jan 31;86(2):121-30 - PubMed
  42. Mol Pharmacol. 2004 Dec;66(6):1557-72 - PubMed
  43. Mol Cell Biol. 2001 Mar;21(5):1475-83 - PubMed
  44. Nature. 2014 Aug 28;512(7515):387-92 - PubMed
  45. Dev Dyn. 2015 Sep;244(9):1168-1178 - PubMed
  46. Dev Biol. 2007 Feb 15;302(2):427-37 - PubMed
  47. Dev Biol. 2013 Oct 1;382(1):57-69 - PubMed
  48. Mol Biol Cell. 2008 Aug;19(8):3263-71 - PubMed
  49. Gen Comp Endocrinol. 2013 Sep 15;191:45-58 - PubMed
  50. Biochem Pharmacol. 2009 Feb 15;77(4):536-46 - PubMed
  51. Mol Biol Evol. 2014 Dec;31(12):3113-24 - PubMed
  52. Toxicol Sci. 2003 Nov;76(1):138-50 - PubMed
  53. Chemosphere. 2012 Apr;87(4):369-75 - PubMed
  54. Environ Health Perspect. 2009 Jul;117(7):1139-46 - PubMed
  55. Development. 2005 Mar;132(5):851-61 - PubMed
  56. Biochem Pharmacol. 2013 May 15;85(10):1405-16 - PubMed
  57. J Bone Miner Res. 2004 Feb;19(2):245-55 - PubMed
  58. Development. 2006 Aug;133(16):3127-37 - PubMed
  59. J Fish Biol. 2011 Sep;79(3):561-74 - PubMed
  60. Dev Biol. 2005 May 15;281(2):227-39 - PubMed
  61. PLoS Biol. 2009 Feb 10;7(2):e31 - PubMed
  62. Heredity (Edinb). 2011 Mar;106(3):472-87 - PubMed
  63. Curr Biol. 2000 Oct 5;10(19):1217-20 - PubMed
  64. PLoS Genet. 2013;9(8):e1003661 - PubMed
  65. Blood. 2011 Apr 14;117(15):3996-4007 - PubMed
  66. Nucleic Acids Res. 2001 May 1;29(9):e45 - PubMed
  67. Evodevo. 2015 Jun 28;6:25 - PubMed
  68. Mol Pharmacol. 2008 Dec;74(6):1544-53 - PubMed
  69. Proc Jpn Acad Ser B Phys Biol Sci. 2010;86(1):40-53 - PubMed
  70. Development. 2005 Jul;132(13):3127-38 - PubMed
  71. Heredity (Edinb). 2006 Sep;97(3):211-21 - PubMed
  72. Cell. 1998 Sep 18;94(6):727-37 - PubMed
  73. Biochem Biophys Res Commun. 2000 Apr 29;271(1):130-7 - PubMed
  74. PLoS One. 2014 Jul 02;9(7):e100910 - PubMed
  75. Mol Pharmacol. 2004 Sep;66(3):512-21 - PubMed
  76. PLoS One. 2013 Jun 13;8(6):e66389 - PubMed
  77. Stem Cells. 2011 Jul;29(7):1112-25 - PubMed
  78. Proc Natl Acad Sci U S A. 2011 Aug 9;108(32):13194-9 - PubMed
  79. Nucleic Acids Res. 2011 Jan;39(Database issue):D1016-22 - PubMed
  80. Database (Oxford). 2011 Nov 26;2011:bar050 - PubMed
  81. J Biol Chem. 2004 Jul 9;279(28):29013-22 - PubMed
  82. PLoS One. 2012;7(1):e29346 - PubMed
  83. Science. 2003 Oct 10;302(5643):249-55 - PubMed
  84. Evodevo. 2014 Feb 05;5(1):8 - PubMed
  85. Dev Genes Evol. 2008 Jan;218(1):1-14 - PubMed
  86. J Exp Zool B Mol Dev Evol. 2015 Jun;324(4):316-41 - PubMed
  87. Cell. 2007 Mar 23;128(6):1077-88 - PubMed
  88. J Exp Zool B Mol Dev Evol. 2011 Nov 15;316(7):526-46 - PubMed
  89. FEBS Lett. 2007 Jul 31;581(19):3608-15 - PubMed
  90. Dev Dyn. 2006 Oct;235(10):2722-35 - PubMed
  91. Cell Death Differ. 2013 Nov;20(11):1510-20 - PubMed
  92. Dev Dyn. 2007 Oct;236(10):2943-51 - PubMed
  93. Zebrafish. 2005;2(4):243-57 - PubMed
  94. Heredity (Edinb). 2011 Jul;107(1):1-15 - PubMed
  95. Mol Ecol. 2013 Sep;22(17):4516-31 - PubMed
  96. Neurosci Lett. 2003 Mar 13;339(1):62-6 - PubMed

Publication Types