Perspectives on Gene Regulatory Network Evolution.

Marc S Halfon
Author Information
  1. Marc S Halfon: Department of Biochemistry, University at Buffalo - State University of New York, Buffalo, NY, USA; NY State Center of Excellence in Bioinformatics and Life Sciences, Buffalo, NY, USA; Department of Biological Sciences, University at Buffalo - State University of New York, Buffalo, NY, USA; Department of Biomedical Informatics, University at Buffalo - State University of New York, Buffalo, NY, USA; Department of Molecular and Cellular Biology and Program in Cancer Genetics, Roswell Park Cancer Institute, Buffalo, NY, USA. Electronic address: mshalfon@buffalo.edu.

Abstract

Animal development proceeds through the activity of genes and their cis-regulatory modules (CRMs) working together in sets of gene regulatory networks (GRNs). The emergence of species-specific traits and novel structures results from evolutionary changes in GRNs. Recent work in a wide variety of animal models, and particularly in insects, has started to reveal the modes and mechanisms of GRN evolution. I discuss here various aspects of GRN evolution and argue that developmental system drift (DSD), in which conserved phenotype is nevertheless a result of changed genetic interactions, should regularly be viewed from the perspective of GRN evolution. Advances in methods to discover related CRMs in diverse insect species, a critical requirement for detailed GRN characterization, are also described.

Keywords

References

  1. Genesis. 2014 Mar;52(3):193-207 [PMID: 24549884]
  2. Nature. 2009 Apr 9;458(7239):719-24 [PMID: 19360079]
  3. Nature. 2005 Feb 3;433(7025):481-7 [PMID: 15690032]
  4. Philos Trans R Soc Lond B Biol Sci. 2013 Nov 11;368(1632):20130020 [PMID: 24218633]
  5. Nature. 2010 Dec 16;468(7326):911-20 [PMID: 21164479]
  6. Nature. 2007 Jun 14;447(7146):799-816 [PMID: 17571346]
  7. Dev Cell. 2015 Sep 14;34(5):520-31 [PMID: 26343453]
  8. Genome Res. 2007 Jun;17(6):877-85 [PMID: 17179217]
  9. Dev Biol. 2006 Mar 15;291(2):356-67 [PMID: 16414040]
  10. Nat Rev Genet. 2009 Feb;10(2):141-8 [PMID: 19139764]
  11. Theor Popul Biol. 2000 May;57(3):187-95 [PMID: 10828213]
  12. Nucleic Acids Res. 2011 Jan;39(Database issue):D118-23 [PMID: 20965965]
  13. Evol Dev. 2008 May-Jun;10(3):360-74 [PMID: 18460097]
  14. Birth Defects Res C Embryo Today. 2009 Jun;87(2):123-30 [PMID: 19530131]
  15. Dev Biol. 2016 Aug 15;416(2):402-13 [PMID: 27341759]
  16. Dev Biol. 2007 Feb 15;302(2):717-27 [PMID: 17174297]
  17. Nature. 2005 Feb 10;433(7026):643-7 [PMID: 15703749]
  18. Cell. 2015 Jan 29;160(3):554-66 [PMID: 25635462]
  19. Science. 2010 Jan 15;327(5963):302-5 [PMID: 20007865]
  20. Nature. 2006 Apr 20;440(7087):1050-3 [PMID: 16625197]
  21. Science. 1975 Apr 11;188(4184):107-16 [PMID: 1090005]
  22. Science. 2014 Nov 7;346(6210):763-7 [PMID: 25378627]
  23. Annu Rev Pathol. 2015;10:25-50 [PMID: 25340638]
  24. Curr Opin Insect Sci. 2017 Feb;19:1-7 [PMID: 28521937]
  25. Nat Genet. 2010 Mar;42(3):255-9 [PMID: 20118932]
  26. PLoS Biol. 2011 Jul;9(7):e1001110 [PMID: 21814488]
  27. Dev Biol. 2014 Jun 15;390(2):261-72 [PMID: 24680932]
  28. Genome Res. 2014 Oct;24(10):1595-602 [PMID: 25035418]
  29. Nucleic Acids Res. 2014 Jun;42(10):6128-45 [PMID: 24682824]
  30. Cell. 2008 Aug 22;134(4):610-23 [PMID: 18724934]
  31. BMC Genomics. 2011 Nov 25;12:578 [PMID: 22115527]
  32. Proc Natl Acad Sci U S A. 2013 Oct 15;110(42):16951-6 [PMID: 24085843]
  33. Curr Biol. 2016 Sep 26;26(18):2423-2433 [PMID: 27546578]
  34. Dev Cell. 2009 Oct;17(4):568-79 [PMID: 19853570]
  35. Nucleic Acids Res. 2015 Jan;43(Database issue):D714-9 [PMID: 25332403]
  36. Proc Natl Acad Sci U S A. 2005 Apr 5;102(14):4936-42 [PMID: 15788537]
  37. Curr Opin Insect Sci. 2017 Feb;19:8-15 [PMID: 28521947]
  38. Science. 2010 Dec 24;330(6012):1787-97 [PMID: 21177974]
  39. Nucleic Acids Res. 2007 Jan;35(Database issue):D88-92 [PMID: 17130149]
  40. Nucleic Acids Res. 2016 Jan 4;44(D1):D801-7 [PMID: 26578584]
  41. Science. 2002 Jul 12;297(5579):249-52 [PMID: 12114626]
  42. Cell. 2006 Jun 30;125(7):1387-99 [PMID: 16814723]
  43. J Exp Zool B Mol Dev Evol. 2013 Mar;320(2):74-83 [PMID: 23225600]
  44. Bioinformatics. 2012 Feb 15;28(4):581-3 [PMID: 22199387]
  45. Annu Rev Genet. 2005;39:95-119 [PMID: 16285854]
  46. Curr Biol. 2016 Sep 26;26(18):2412-2422 [PMID: 27546577]
  47. Annu Rev Genomics Hum Genet. 2015;16:103-31 [PMID: 26079281]
  48. Wiley Interdiscip Rev Dev Biol. 2015 Mar-Apr;4(2):59-84 [PMID: 25704908]
  49. Curr Opin Genet Dev. 2009 Dec;19(6):535-40 [PMID: 19913405]
  50. Development. 2016 Oct 15;143(20):3723-3732 [PMID: 27802137]
  51. Curr Biol. 2009 Dec 29;19(24):2057-65 [PMID: 20005109]
  52. Cell. 2008 Mar 7;132(5):783-93 [PMID: 18329365]
  53. Database (Oxford). 2016 Feb 17;2016:null [PMID: 26888907]
  54. Proc Natl Acad Sci U S A. 2011 Feb 15;108(7):2855-60 [PMID: 21282633]
  55. Genome Biol Evol. 2014 Sep;6(9):2301-20 [PMID: 25173756]
  56. Proc Natl Acad Sci U S A. 2012 Dec 18;109(51):20975-9 [PMID: 23197832]
  57. Genes Dev. 1998 May 15;12(10):1474-82 [PMID: 9585507]
  58. Nat Methods. 2013 Dec;10(12):1213-8 [PMID: 24097267]
  59. Nucleic Acids Res. 2011 Dec;39(22):9463-72 [PMID: 21821659]
  60. Evol Dev. 2001 Mar-Apr;3(2):109-19 [PMID: 11341673]
  61. Dev Biol. 2010 Apr 15;340(2):200-8 [PMID: 19941847]
  62. J Hered. 2013 Sep-Oct;104(5):595-600 [PMID: 23940263]

Grants

  1. R21 AI125918/NIAID NIH HHS

MeSH Term

Animals
Gene Regulatory Networks
Genome
Insecta
Phenotype

Word Cloud

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