Rice nucleosome patterns undergo remodeling coincident with stress-induced gene expression.

Qi Zhang, Dong-Ha Oh, Sandra Feuer DiTusa, Mangu V RamanaRao, Niranjan Baisakh, Maheshi Dassanayake, Aaron P Smith
Author Information
  1. Qi Zhang: Department of Biological Sciences, Louisiana State University, Baton Rouge, LA, 70803, USA.
  2. Dong-Ha Oh: Department of Biological Sciences, Louisiana State University, Baton Rouge, LA, 70803, USA.
  3. Sandra Feuer DiTusa: Department of Biological Sciences, Louisiana State University, Baton Rouge, LA, 70803, USA.
  4. Mangu V RamanaRao: School of Plant, Environmental, and Soil Sciences, Louisiana State University Agricultural Center, Baton Rouge, LA, 70803, USA.
  5. Niranjan Baisakh: School of Plant, Environmental, and Soil Sciences, Louisiana State University Agricultural Center, Baton Rouge, LA, 70803, USA.
  6. Maheshi Dassanayake: Department of Biological Sciences, Louisiana State University, Baton Rouge, LA, 70803, USA.
  7. Aaron P Smith: Department of Biological Sciences, Louisiana State University, Baton Rouge, LA, 70803, USA. apsmith@lsu.edu. ORCID

Abstract

BACKGROUND: Formation of nucleosomes along eukaryotic DNA has an impact on transcription. Major transcriptional changes occur in response to low external phosphate (Pi) in plants, but the involvement of chromatin-level mechanisms in Pi starvation responses have not been investigated.
RESULTS: We mapped nucleosomes along with transcriptional changes after 24-h of Pi starvation in rice (Oryza sativa) by deep sequencing of micrococcal nuclease digested chromatin and ribosome-depleted RNA. We demonstrated that nucleosome patterns at rice genes were affected by both cis- and trans-determinants, including GC content and transcription. Also, categorizing rice genes by nucleosome patterns across the transcription start site (TSS) revealed nucleosome patterns that correlated with distinct functional categories of genes. We further demonstrated that Pi starvation resulted in numerous dynamic nucleosomes, which were enhanced at genes differentially expressed in response to Pi starvation.
CONCLUSIONS: We demonstrate that rice nucleosome patterns are suggestive of gene functions, and reveal a link between chromatin remodeling and transcriptional changes in response to deficiency of a major macronutrient. Our findings help to enhance the understanding towards eukaryotic gene regulation at the chromatin level.

Keywords

References

  1. Nucleic Acids Res. 2012 May;40(10):e72 [PMID: 22323520]
  2. Dev Biol. 2010 Mar 15;339(2):258-66 [PMID: 19527704]
  3. Nat Genet. 2007 Oct;39(10):1235-44 [PMID: 17873876]
  4. Cell. 2004 Mar 5;116(5):699-709 [PMID: 15006352]
  5. Proc Natl Acad Sci U S A. 2014 Jun 17;111(24):E2462-71 [PMID: 24889621]
  6. J Biol Chem. 2007 Sep 21;282(38):27610-21 [PMID: 17631505]
  7. Plant Physiol. 2010 Jan;152(1):217-25 [PMID: 19897606]
  8. BMC Bioinformatics. 2009 Dec 22;10:442 [PMID: 20028554]
  9. Elife. 2015 Jul 21;4: [PMID: 26196146]
  10. Plant Physiol. 2009 Sep;151(1):262-74 [PMID: 19605549]
  11. Genome Res. 2012 Jan;22(1):151-62 [PMID: 22110044]
  12. Genome Res. 2012 Sep;22(9):1798-812 [PMID: 22955990]
  13. Mol Plant. 2010 Mar;3(2):288-99 [PMID: 20142416]
  14. Nucleic Acids Res. 2016 Jul 8;44(W1):W160-5 [PMID: 27079975]
  15. Genome Biol. 2009;10(3):R25 [PMID: 19261174]
  16. Front Microbiol. 2016 Jun 01;7:826 [PMID: 27313570]
  17. Nat Struct Mol Biol. 2013 Mar;20(3):267-73 [PMID: 23463311]
  18. Plant J. 2014 May;78(4):706-14 [PMID: 24606212]
  19. Nucleic Acids Res. 2016 Dec 1;44(21):10091-10105 [PMID: 27488188]
  20. Nature. 2011 Oct 05;478(7367):29-31 [PMID: 21979027]
  21. Genome Res. 2015 Aug;25(8):1182-95 [PMID: 26063739]
  22. Nat Protoc. 2012 Mar 01;7(3):562-78 [PMID: 22383036]
  23. Plant J. 2014 Nov;80(3):503-15 [PMID: 25155524]
  24. Proc Natl Acad Sci U S A. 2016 Oct 18;113(42):E6427-E6436 [PMID: 27698124]
  25. BMC Genomics. 2014 Apr 15;15:284 [PMID: 24735413]
  26. Genome Res. 2013 Feb;23(2):341-51 [PMID: 23193179]
  27. Plant Physiol. 2015 Aug;168(4):1406-16 [PMID: 26143253]
  28. EMBO J. 1986 Oct;5(10):2689-96 [PMID: 3536481]
  29. PLoS Genet. 2014 May 22;10(5):e1004378 [PMID: 24852592]
  30. Mol Cell Biol. 2012 May;32(9):1645-53 [PMID: 22354995]
  31. Mol Cell Biol. 2009 Jun;29(11):2960-81 [PMID: 19307305]
  32. J Proteomics. 2013 Dec 06;94:1-22 [PMID: 24012629]
  33. Cell. 2016 Jan 14;164(1-2):57-68 [PMID: 26771485]
  34. Plant Cell. 2013 Nov;25(11):4285-304 [PMID: 24249833]
  35. Plant Cell. 2014 Oct;26(10):3883-93 [PMID: 25361955]
  36. Annu Rev Plant Physiol Plant Mol Biol. 1999 Jun;50:665-693 [PMID: 15012223]
  37. Cell. 2013 Mar 14;152(6):1344-54 [PMID: 23498941]
  38. Rice (N Y). 2013 Feb 06;6(1):4 [PMID: 24280374]
  39. Curr Opin Plant Biol. 2013 May;16(2):205-12 [PMID: 23566853]
  40. Plant Physiol. 2013 Jun;162(2):1127-41 [PMID: 23572549]
  41. Nat Genet. 2016 Oct;48(10):1273-8 [PMID: 27571261]
  42. Nat Biotechnol. 2011 Jan;29(1):24-6 [PMID: 21221095]
  43. Plant Signal Behav. 2011 Jul;6(7):927-9 [PMID: 21617375]
  44. PLoS Biol. 2008 Mar 18;6(3):e65 [PMID: 18351804]
  45. FEBS Lett. 2012 Feb 17;586(4):289-95 [PMID: 22285489]
  46. Genome Biol. 2013 Apr 25;14(4):R36 [PMID: 23618408]
  47. Nature. 2010 Jul 15;466(7304):388-92 [PMID: 20512117]
  48. Nature. 2011 May 22;474(7352):516-20 [PMID: 21602827]
  49. Plant Physiol. 2003 Jul;132(3):1260-71 [PMID: 12857808]
  50. Plant Physiol. 2008 Apr;146(4):1673-86 [PMID: 18263782]
  51. Science. 2009 Feb 20;323(5917):1014-5 [PMID: 19229022]
  52. Nature. 1997 Sep 18;389(6648):251-60 [PMID: 9305837]
  53. Nature. 2008 May 15;453(7193):358-62 [PMID: 18408708]
  54. Nucleic Acids Res. 2015 Mar 31;43(6):e40 [PMID: 25564527]
  55. Nat Rev Genet. 2009 Mar;10(3):161-72 [PMID: 19204718]
  56. New Phytol. 2003 Mar;157(3):423-447 [PMID: 33873400]
  57. J Biol Chem. 2005 Apr 1;280(13):12065-8 [PMID: 15664979]
  58. Bioinformatics. 2010 Mar 15;26(6):841-2 [PMID: 20110278]
  59. Genome Res. 2008 Jul;18(7):1073-83 [PMID: 18550805]
  60. Proc Natl Acad Sci U S A. 2014 Oct 14;111(41):14953-8 [PMID: 25271318]
  61. Nucleic Acids Res. 2010 Jul;38(Web Server issue):W64-70 [PMID: 20435677]
  62. Genome. 2009 Mar;52(3):294-7 [PMID: 19234558]

Grants

  1. IOS-1127051/Directorate for Biological Sciences
  2. MCB-1616827/Directorate for Biological Sciences
  3. PJ011379/Rural Development Administration

MeSH Term

Chromatin Assembly and Disassembly
Gene Expression Regulation, Plant
Nucleosomes
Oryza
Sequence Analysis, RNA
Stress, Physiological
Transcription Factors

Chemicals

Nucleosomes
Transcription Factors