Stress induced gene expression drives transient DNA methylation changes at adjacent repetitive elements.

David Secco, Chuang Wang, Huixia Shou, Matthew D Schultz, Serge Chiarenza, Laurent Nussaume, Joseph R Ecker, James Whelan, Ryan Lister
Author Information
  1. David Secco: ARC Centre of Excellence in Plant Energy Biology, The University of Western Australia, Perth, Australia.
  2. Chuang Wang: State Key laboratory of Plant Physiology and Biochemistry, College of Life Science, Zhejiang University, Hangzhou, China.
  3. Huixia Shou: State Key laboratory of Plant Physiology and Biochemistry, College of Life Science, Zhejiang University, Hangzhou, China.
  4. Matthew D Schultz: Genomic Analysis Laboratory, Salk Institute for Biological Studies, La Jolla, United States.
  5. Serge Chiarenza: UMR 6191 CEA, Centre National de la Recherche Scientifique, Laboratoire de Biologie du Développement des Plantes, Université d'Aix-Marseille, Saint-Paul-lez-Durance, France.
  6. Laurent Nussaume: UMR 6191 CEA, Centre National de la Recherche Scientifique, Laboratoire de Biologie du Développement des Plantes, Université d'Aix-Marseille, Saint-Paul-lez-Durance, France.
  7. Joseph R Ecker: Genomic Analysis Laboratory, Salk Institute for Biological Studies, La Jolla, United States.
  8. James Whelan: Joint Research Laboratory in Genomics and Nutriomics, Zhejiang University, Hangzhou, China.
  9. Ryan Lister: ARC Centre of Excellence in Plant Energy Biology, The University of Western Australia, Perth, Australia.

Abstract

Cytosine DNA methylation (mC) is a genome modification that can regulate the expression of coding and non-coding genetic elements. However, little is known about the involvement of mC in response to environmental cues. Using whole genome bisulfite sequencing to assess the spatio-temporal dynamics of mC in rice grown under phosphate starvation and recovery conditions, we identified widespread phosphate starvation-induced changes in mC, preferentially localized in transposable elements (TEs) close to highly induced genes. These changes in mC occurred after changes in nearby gene transcription, were mostly DCL3a-independent, and could partially be propagated through mitosis, however no evidence of meiotic transmission was observed. Similar analyses performed in Arabidopsis revealed a very limited effect of phosphate starvation on mC, suggesting a species-specific mechanism. Overall, this suggests that TEs in proximity to environmentally induced genes are silenced via hypermethylation, and establishes the temporal hierarchy of transcriptional and epigenomic changes in response to stress.

Keywords

References

  1. Plant Cell Rep. 2008 Jun;27(6):1065-73 [PMID: 18309491]
  2. Nat Rev Genet. 2010 Mar;11(3):204-20 [PMID: 20142834]
  3. Nat Biotechnol. 2013 Jan;31(1):46-53 [PMID: 23222703]
  4. Proc Natl Acad Sci U S A. 2014 Mar 11;111(10):3877-82 [PMID: 24554078]
  5. BMC Plant Biol. 2011 Jan 12;11:10 [PMID: 21226959]
  6. Plant Cell Environ. 2006 Jan;29(1):115-25 [PMID: 17086758]
  7. Arabidopsis Book. 2002;1:e0024 [PMID: 22303200]
  8. Plant Cell Rep. 2013 Aug;32(8):1151-9 [PMID: 23719757]
  9. Nat Biotechnol. 2013 Feb;31(2):154-9 [PMID: 23354102]
  10. PLoS Genet. 2015 Jan 08;11(1):e1004920 [PMID: 25569172]
  11. Biometrics. 2013 Mar;69(1):1-7 [PMID: 23379645]
  12. Nature. 2011 Sep 20;480(7376):245-9 [PMID: 22057020]
  13. Nature. 2014 Apr 17;508(7496):411-5 [PMID: 24670663]
  14. Plant Cell Physiol. 2012 May;53(5):801-8 [PMID: 22457398]
  15. PLoS One. 2010 Mar 03;5(3):e9514 [PMID: 20209086]
  16. PLoS One. 2013;8(2):e55772 [PMID: 23418457]
  17. Proc Natl Acad Sci U S A. 2005 Aug 16;102(33):11934-9 [PMID: 16085708]
  18. Mol Biol Evol. 2012 Oct;29(10):3193-203 [PMID: 22593226]
  19. Mol Plant. 2010 Mar;3(2):288-99 [PMID: 20142416]
  20. EMBO Rep. 2014 Apr;15(4):446-52 [PMID: 24562611]
  21. Plant Cell. 2014 Jan;26(1):454-64 [PMID: 24474629]
  22. Nat Rev Genet. 2014 Jun;15(6):394-408 [PMID: 24805120]
  23. J Exp Bot. 2014 Jun;65(10):2801-12 [PMID: 24744427]
  24. PLoS Genet. 2012;8(12):e1003127 [PMID: 23271981]
  25. Nat Protoc. 2012 Mar 01;7(3):562-78 [PMID: 22383036]
  26. Plant Physiol. 2013 May;162(1):116-31 [PMID: 23542151]
  27. Science. 2013 Aug 9;341(6146):1237905 [PMID: 23828890]
  28. Cell. 2008 May 2;133(3):523-36 [PMID: 18423832]
  29. Genome Res. 2009 Aug;19(8):1419-28 [PMID: 19478138]
  30. Curr Opin Plant Biol. 2009 Apr;12(2):133-9 [PMID: 19179104]
  31. Annu Rev Plant Biol. 2011;62:185-206 [PMID: 21370979]
  32. Cell. 2012 Sep 28;151(1):167-80 [PMID: 23021223]
  33. Proc Natl Acad Sci U S A. 2014 Jun 10;111(23):8547-52 [PMID: 24912148]
  34. Genome Biol. 2012 Oct 11;13(10):249 [PMID: 23058244]
  35. Cell. 2013 Mar 28;153(1):193-205 [PMID: 23540698]
  36. Plant Cell. 2013 Oct;25(10):4061-74 [PMID: 24122828]
  37. Curr Opin Plant Biol. 2013 May;16(2):164-9 [PMID: 23562565]
  38. Nature. 2014 Nov 27;515(7528):587-90 [PMID: 25219852]
  39. Proc Natl Acad Sci U S A. 2010 May 11;107(19):8689-94 [PMID: 20395551]
  40. PLoS One. 2012;7(11):e49331 [PMID: 23145152]
  41. Nat Genet. 2007 Aug;39(8):1033-7 [PMID: 17643101]
  42. Plant J. 2011 Mar;65(5):820-8 [PMID: 21251104]
  43. Plant Signal Behav. 2013 Aug;8(8): [PMID: 23759554]
  44. Oncogene. 2001 Oct 25;20(48):7120-7 [PMID: 11704838]
  45. Plant J. 2009 Jan;57(2):322-31 [PMID: 18808455]
  46. BMC Genomics. 2012 Jul 02;13:300 [PMID: 22747568]
  47. Mol Genet Genomics. 2007 May;277(5):589-600 [PMID: 17273870]
  48. Proc Natl Acad Sci U S A. 2015 Jan 20;112(3):917-22 [PMID: 25561534]
  49. Plant Cell. 2011 Apr;23(4):1523-35 [PMID: 21521698]
  50. Plant Physiol. 2010 Jan;152(1):217-25 [PMID: 19897606]
  51. Trends Plant Sci. 2013 Jul;18(7):367-76 [PMID: 23618952]
  52. BMC Genet. 2014;15 Suppl 1:S9 [PMID: 25080211]
  53. Nature. 2008 Mar 13;452(7184):215-9 [PMID: 18278030]
  54. Trends Plant Sci. 2011 Aug;16(8):442-50 [PMID: 21684794]
  55. Plant Cell. 2013 Nov;25(11):4285-304 [PMID: 24249833]
  56. Proc Natl Acad Sci U S A. 2012 Aug 7;109(32):E2183-91 [PMID: 22733782]
  57. Plant J. 2007 Jan;49(1):38-45 [PMID: 17144899]
  58. J Exp Bot. 2011 Mar;62(6):1951-60 [PMID: 21193578]
  59. PLoS One. 2012;7(6):e40203 [PMID: 22761959]
  60. Nucleic Acids Res. 2011 Sep 1;39(16):6919-31 [PMID: 21586580]
  61. Science. 2010 May 14;328(5980):916-9 [PMID: 20395474]
  62. Plant Cell. 2013 Jul;25(7):2400-15 [PMID: 23881411]
  63. J Genet Genomics. 2011 Sep 20;38(9):419-24 [PMID: 21930101]
  64. Proc Natl Acad Sci U S A. 1996 Aug 6;93(16):8449-54 [PMID: 8710891]
  65. Mol Cell. 2010 May 14;38(3):465-75 [PMID: 20381393]
  66. Plant J. 2012 Feb;69(3):462-74 [PMID: 21973320]
  67. Plant J. 2009 Mar;57(5):895-904 [PMID: 19000161]
  68. Science. 2011 Oct 21;334(6054):369-73 [PMID: 21921155]
  69. Plant Physiol. 2007 Dec;145(4):1460-70 [PMID: 17932308]
  70. Proc Natl Acad Sci U S A. 2014 Oct 14;111(41):14947-52 [PMID: 25271326]
  71. Genes Dev. 2002 Jan 1;16(1):6-21 [PMID: 11782440]
  72. New Phytol. 2012 Mar;193(4):842-51 [PMID: 22403821]
  73. Proc Natl Acad Sci U S A. 2014 Oct 14;111(41):14953-8 [PMID: 25271318]
  74. Biochim Biophys Acta. 2011 Aug;1809(8):459-68 [PMID: 21515434]
  75. Plant Mol Biol. 2004 Jul;55(5):727-41 [PMID: 15604713]
  76. PLoS Genet. 2011 Mar;7(3):e1002021 [PMID: 21455488]

MeSH Term

5-Methylcytosine
Arabidopsis
DNA Methylation
DNA, Plant
Gene Expression Regulation
Genome, Plant
Oryza
Phosphates
Regulatory Elements, Transcriptional
Sequence Analysis, DNA
Stress, Physiological

Chemicals

DNA, Plant
Phosphates
5-Methylcytosine