Dynamics of DNA methylomes underlie oyster development.

Guillaume Riviere, Yan He, Samuele Tecchio, Elizabeth Crowell, Michaël Gras, Pascal Sourdaine, Ximing Guo, Pascal Favrel
Author Information
  1. Guillaume Riviere: Normandy University, Caen, France. ORCID
  2. Yan He: Ministry of Education Key Laboratory of Marine Genetics and Breeding, College of Marine Life Sciences, Ocean University of China, Qingdao, Shandong, China.
  3. Samuele Tecchio: Normandy University, Caen, France.
  4. Elizabeth Crowell: Normandy University, Caen, France. ORCID
  5. Michaël Gras: Normandy University, Caen, France. ORCID
  6. Pascal Sourdaine: Normandy University, Caen, France.
  7. Ximing Guo: Haskin Shellfish Research Laboratory, Department of Marine and Coastal Sciences, Rutgers University, Port Norris, NJ, United States of America.
  8. Pascal Favrel: Normandy University, Caen, France.

Abstract

DNA methylation is a critical epigenetic regulator of development in mammals and social insects, but its significance in development outside these groups is not understood. Here we investigated the genome-wide dynamics of DNA methylation in a mollusc model, the oyster Crassostrea gigas, from the egg to the completion of organogenesis. Large-scale methylation maps reveal that the oyster genome displays a succession of methylated and non methylated regions, which persist throughout development. Differentially methylated regions (DMRs) are strongly regulated during cleavage and metamorphosis. The distribution and levels of methylated DNA within genomic features (exons, introns, promoters, repeats and transposons) show different developmental lansdscapes marked by a strong increase in the methylation of exons against introns after metamorphosis. Kinetics of methylation in gene-bodies correlate to their transcription regulation and to distinct functional gene clusters, and DMRs at cleavage and metamorphosis bear the genes functionally related to these steps, respectively. This study shows that DNA methylome dynamics underlie development through transcription regulation in the oyster, a lophotrochozoan species. To our knowledge, this is the first demonstration of such epigenetic regulation outside vertebrates and ecdysozoan models, bringing new insights into the evolution and the epigenetic regulation of developmental processes.

References

  1. Sci Rep. 2016 Feb 10;6:20796 [PMID: 26861843]
  2. Brief Funct Genomics. 2014 May;13(3):217-22 [PMID: 24397979]
  3. BMC Genomics. 2014 Dec 16;15:1119 [PMID: 25514978]
  4. Curr Top Dev Biol. 2016;116:273-97 [PMID: 26970624]
  5. Nat Genet. 2011 Oct 02;43(11):1091-7 [PMID: 21964573]
  6. Development. 2016 Jun 1;143(11):1833-7 [PMID: 27246709]
  7. Epigenetics Chromatin. 2013 Nov 11;6(1):38 [PMID: 24279449]
  8. Trends Genet. 1997 Aug;13(8):335-40 [PMID: 9260521]
  9. Development. 2013 Oct;140(19):3951-63 [PMID: 24046316]
  10. Parasit Vectors. 2013 Jun 06;6:167 [PMID: 23742053]
  11. PLoS Genet. 2013;9(10):e1003872 [PMID: 24130511]
  12. Dev Biol. 1991 Jul;146(1):12-23 [PMID: 2060698]
  13. Insect Mol Biol. 2012 Feb;21(1):129-38 [PMID: 22122805]
  14. FEBS Lett. 2015 Jun 4;589(13):1459-66 [PMID: 25943713]
  15. Nat Cell Biol. 2006 Feb;8(2):188-94 [PMID: 16415856]
  16. Science. 2001 Dec 21;294(5551):2536-9 [PMID: 11719692]
  17. Cell. 1999 Oct 29;99(3):247-57 [PMID: 10555141]
  18. Curr Biol. 2012 Oct 9;22(19):1755-64 [PMID: 22885060]
  19. PeerJ. 2013 Nov 21;1:e215 [PMID: 24282674]
  20. Development. 2014 Jul;141(13):2568-80 [PMID: 24924192]
  21. Nature. 2014 Jul 31;511(7511):606-10 [PMID: 25079557]
  22. Nat Rev Genet. 2013 Mar;14(3):204-20 [PMID: 23400093]
  23. BMC Genomics. 2012 Sep 15;13:480 [PMID: 22978521]
  24. Nat Protoc. 2013 Sep;8(9):1765-86 [PMID: 23975260]
  25. Cell. 2015 Jun 4;161(6):1453-67 [PMID: 26046444]
  26. Mol Biol Evol. 2012 Aug;29(8):1907-16 [PMID: 22328716]
  27. Proc Natl Acad Sci U S A. 2009 Jul 7;106(27):11206-11 [PMID: 19556545]
  28. Trends Genet. 2015 Jun;31(6):329-35 [PMID: 25743487]
  29. Nat Struct Mol Biol. 2013 Mar;20(3):332-8 [PMID: 23353788]
  30. BMC Bioinformatics. 2015 Dec 02;16:401 [PMID: 26627443]
  31. PLoS Biol. 2010 Nov 02;8(11):e1000506 [PMID: 21072239]
  32. Proc Natl Acad Sci U S A. 2015 Jun 2;112(22):6796-9 [PMID: 25368180]
  33. Annu Rev Cell Dev Biol. 2014;30:561-80 [PMID: 25000994]
  34. Mol Cell Biol. 2002 Jan;22(2):480-91 [PMID: 11756544]
  35. Development. 2015 Nov 15;142(22):3833-44 [PMID: 26417043]
  36. Cell. 2015 Jun 4;161(6):1437-52 [PMID: 26046443]
  37. Nat Protoc. 2012 Mar 08;7(4):617-36 [PMID: 22402632]
  38. Nature. 2012 Oct 4;490(7418):49-54 [PMID: 22992520]
  39. PLoS One. 2013 Jun 10;8(6):e65598 [PMID: 23762400]
  40. Mol Cell Biol. 2004 Oct;24(20):8862-71 [PMID: 15456861]
  41. Nat Rev Genet. 2012 May 29;13(7):484-92 [PMID: 22641018]
  42. Proc Natl Acad Sci U S A. 2015 Apr 28;112(17):E2116 [PMID: 25848065]
  43. Front Physiol. 2014 Jun 17;5:224 [PMID: 24987376]
  44. Nat Commun. 2015 Mar 11;6:6513 [PMID: 25758336]
  45. Dev Cell. 2016 Jan 25;36(2):152-63 [PMID: 26812015]
  46. Front Physiol. 2014 Apr 07;5:129 [PMID: 24778620]
  47. Mar Biotechnol (NY). 2013 Dec;15(6):739-53 [PMID: 23877618]
  48. Nature. 2006 Jul 20;442(7100):307-11 [PMID: 16732293]
  49. Nature. 2015 Jan 15;517(7534):321-6 [PMID: 25592537]
  50. Science. 2010 May 14;328(5980):916-9 [PMID: 20395474]
  51. Mol Biol Evol. 2016 Apr;33(4):1019-28 [PMID: 26715626]
  52. Development. 2006 Sep;133(17):3411-8 [PMID: 16887828]
  53. BMC Genomics. 2010 Aug 27;11:483 [PMID: 20799955]

MeSH Term

Animals
DNA Methylation
Gene Expression Regulation, Developmental
Genome
Ostreidae

Word Cloud

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