Home LiteratureArticle Details
PMID: 27203113 Published · ppublish English Journal Article Research Support, Non-U.S. Gov't Research Support, U.S. Gov't, Non-P.H.S.

Cistrome and Epicistrome Features Shape the Regulatory DNA Landscape.

Cell ·Vol. 165 ·No. 5 ·2016-05-19 ·Pages 1280-1292

O'Malley RC, Huang SC, Song L, Lewsey MG, Bartlett A, Nery JR, Galli M, Gallavotti A, Ecker JR

Abstract

The cistrome is the complete set of transcription factor (TF) binding sites (cis-elements) in an organism, while an epicistrome incorporates tissue-specific DNA chemical modifications and TF-specific chemical sensitivities into these binding profiles. Robust methods to construct comprehensive cistrome and epicistrome maps are critical for elucidating complex transcriptional networks that underlie growth, behavior, and disease. Here, we describe DNA affinity purification sequencing (DAP-seq), a high-throughput TF binding site discovery method that interrogates genomic DNA with in-vitro-expressed TFs. Using DAP-seq, we defined the Arabidopsis cistrome by resolving motifs and peaks for 529 TFs. Because genomic DNA used in DAP-seq retains 5-methylcytosines, we determined that >75% (248/327) of Arabidopsis TFs surveyed were methylation sensitive, a property that strongly impacts the epicistrome landscape. DAP-seq datasets also yielded insight into the biology and binding site architecture of numerous TFs, demonstrating the value of DAP-seq for cost-effective cistromic and epicistromic annotation in any organism.

MeSH Terms
Amino Acid Motifs Arabidopsis/genetics DNA, Plant/genetics,metabolism Epigenesis, Genetic Genome, Plant Indoleacetic Acids/metabolism Plant Proteins/genetics Response Elements Sequence Analysis, DNA/methods Transcription Factors/metabolism
Chemicals
DNA, Plant Indoleacetic Acids Plant Proteins Transcription Factors
Authors & Affiliations
9 authors, click to expand affiliations / ORCID
O'Malley Ronan C
Genomic Analysis Laboratory, The Salk Institute for Biological Studies, 10010 N. Torrey Pines Rd., La Jolla, CA 92037, USA; Plant Biology Laboratory, The Salk Institute for Biological Studies, 10010 N. Torrey Pines Rd., La Jolla, CA 92037, USA.
Huang Shao-Shan Carol
Genomic Analysis Laboratory, The Salk Institute for Biological Studies, 10010 N. Torrey Pines Rd., La Jolla, CA 92037, USA; Plant Biology Laboratory, The Salk Institute for Biological Studies, 10010 N. Torrey Pines Rd., La Jolla, CA 92037, USA.
Song Liang
Plant Biology Laboratory, The Salk Institute for Biological Studies, 10010 N. Torrey Pines Rd., La Jolla, CA 92037, USA.
Lewsey Mathew G
Plant Biology Laboratory, The Salk Institute for Biological Studies, 10010 N. Torrey Pines Rd., La Jolla, CA 92037, USA.
Bartlett Anna
Genomic Analysis Laboratory, The Salk Institute for Biological Studies, 10010 N. Torrey Pines Rd., La Jolla, CA 92037, USA.
Nery Joseph R
Genomic Analysis Laboratory, The Salk Institute for Biological Studies, 10010 N. Torrey Pines Rd., La Jolla, CA 92037, USA.
Galli Mary
Genomic Analysis Laboratory, The Salk Institute for Biological Studies, 10010 N. Torrey Pines Rd., La Jolla, CA 92037, USA; Waksman Institute, Rutgers University, Piscataway, NJ 08854-8020, USA.
Gallavotti Andrea
Waksman Institute, Rutgers University, Piscataway, NJ 08854-8020, USA.
Ecker Joseph R
Genomic Analysis Laboratory, The Salk Institute for Biological Studies, 10010 N. Torrey Pines Rd., La Jolla, CA 92037, USA; Plant Biology Laboratory, The Salk Institute for Biological Studies, 10010 N. Torrey Pines Rd., La Jolla, CA 92037, USA; Howard Hughes Medical Institute, The Salk Institute for Biological Studies, 10010 N. Torrey Pines Rd., La Jolla, CA 92037, USA. Electronic address: ecker@salk.edu.
References (55)
55 references, click to expand
  1. An atlas of over 90,000 conserved noncoding sequences provides insight into crucifer regulatory regions.
    Nat Genet. 2013 Aug;45(8):891-8 PMID: 23817568
  2. HSF1 drives a transcriptional program distinct from heat shock to support highly malignant human cancers.
    Cell. 2012 Aug 3;150(3):549-62 PMID: 22863008
  3. DIP-chip: rapid and accurate determination of DNA-binding specificity.
    Genome Res. 2005 Mar;15(3):421-7 PMID: 15710749
  4. Mutations of the Drosophila zinc finger-encoding gene vielfältig impair mitotic cell divisions and cause improper chromosome segregation.
    Mol Biol Cell. 2006 May;17(5):2356-65 PMID: 16525017
  5. Temporal transcriptional response to ethylene gas drives growth hormone cross-regulation in Arabidopsis.
    Elife. 2013 Jun 11;2:e00675 PMID: 23795294
  6. Multiplexed massively parallel SELEX for characterization of human transcription factor binding specificities.
    Genome Res. 2010 Jun;20(6):861-73 PMID: 20378718
  7. Accurate prediction of inducible transcription factor binding intensities in vivo.
    PLoS Genet. 2012;8(3):e1002610 PMID: 22479205
  8. ChIP-Seq: technical considerations for obtaining high-quality data.
    Nat Immunol. 2011 Sep 20;12(10):918-22 PMID: 21934668
  9. deepTools: a flexible platform for exploring deep-sequencing data.
    Nucleic Acids Res. 2014 Jul;42(Web Server issue):W187-91 PMID: 24799436
  10. Determinants of nucleosome positioning.
    Nat Struct Mol Biol. 2013 Mar;20(3):267-73 PMID: 23463311
  11. Disentangling the many layers of eukaryotic transcriptional regulation.
    Annu Rev Genet. 2012;46:43-68 PMID: 22934649
  12. MEME-ChIP: motif analysis of large DNA datasets.
    Bioinformatics. 2011 Jun 15;27(12):1696-7 PMID: 21486936
  13. The accessible chromatin landscape of the human genome.
    Nature. 2012 Sep 6;489(7414):75-82 PMID: 22955617
  14. What are super-enhancers?
    Nat Genet. 2015 Jan;47(1):8-12 PMID: 25547603
  15. Establishing, maintaining and modifying DNA methylation patterns in plants and animals.
    Nat Rev Genet. 2010 Mar;11(3):204-20 PMID: 20142834
  16. Structural basis for oligomerization of auxin transcriptional regulators.
    Nat Commun. 2014 Apr 07;5:3617 PMID: 24710426
  17. Genome-wide high-resolution mapping and functional analysis of DNA methylation in arabidopsis.
    Cell. 2006 Sep 22;126(6):1189-201 PMID: 16949657
  18. Cell cycle control across the eukaryotic kingdom.
    Trends Cell Biol. 2013 Jul;23(7):345-56 PMID: 23566594
  19. The Arabidopsis nucleosome remodeler DDM1 allows DNA methyltransferases to access H1-containing heterochromatin.
    Cell. 2013 Mar 28;153(1):193-205 PMID: 23540698
  20. Shotgun bisulphite sequencing of the Arabidopsis genome reveals DNA methylation patterning.
    Nature. 2008 Mar 13;452(7184):215-9 PMID: 18278030
  21. Role of the Arabidopsis thaliana NAC transcription factors ANAC019 and ANAC055 in regulating jasmonic acid-signaled defense responses.
    Cell Res. 2008 Jul;18(7):756-67 PMID: 18427573
  22. Arabidopsis JACKDAW and MAGPIE zinc finger proteins delimit asymmetric cell division and stabilize tissue boundaries by restricting SHORT-ROOT action.
    Genes Dev. 2007 Sep 1;21(17):2196-204 PMID: 17785527
  23. An encyclopedia of mouse DNA elements (Mouse ENCODE).
    Genome Biol. 2012 Aug 13;13(8):418 PMID: 22889292
  24. Quantitative modeling of transcription factor binding specificities using DNA shape.
    Proc Natl Acad Sci U S A. 2015 Apr 14;112(15):4654-9 PMID: 25775564
  25. Highly integrated single-base resolution maps of the epigenome in Arabidopsis.
    Cell. 2008 May 2;133(3):523-36 PMID: 18423832
  26. Evolution of the ARF gene family in land plants: old domains, new tricks.
    Mol Biol Evol. 2013 Jan;30(1):45-56 PMID: 22977118
  27. The plant Polycomb repressive complex 1 (PRC1) existed in the ancestor of seed plants and has a complex duplication history.
    BMC Evol Biol. 2015 Mar 13;15:44 PMID: 25881027
  28. ARF1, a transcription factor that binds to auxin response elements.
    Science. 1997 Jun 20;276(5320):1865-8 PMID: 9188533
  29. A modular analysis of the auxin signalling network.
    PLoS One. 2015 Mar 25;10(3):e0122231 PMID: 25807071
  30. In pursuit of design principles of regulatory sequences.
    Nat Rev Genet. 2014 Jul;15(7):453-68 PMID: 24913666
  31. Model-based analysis of ChIP-Seq (MACS).
    Genome Biol. 2008;9(9):R137 PMID: 18798982
  32. Auxin signaling modules regulate maize inflorescence architecture.
    Proc Natl Acad Sci U S A. 2015 Oct 27;112(43):13372-7 PMID: 26464512
  33. A genome-scale resource for the functional characterization of Arabidopsis transcription factors.
    Cell Rep. 2014 Jul 24;8(2):622-32 PMID: 25043187
  34. Single-cell chromatin accessibility reveals principles of regulatory variation.
    Nature. 2015 Jul 23;523(7561):486-90 PMID: 26083756
  35. Determination and inference of eukaryotic transcription factor sequence specificity.
    Cell. 2014 Sep 11;158(6):1431-43 PMID: 25215497
  36. Defining clusters from a hierarchical cluster tree: the Dynamic Tree Cut package for R.
    Bioinformatics. 2008 Mar 1;24(5):719-20 PMID: 18024473
  37. Convergence of Light and ABA signaling on the ABI5 promoter.
    PLoS Genet. 2014 Feb 27;10(2):e1004197 PMID: 24586210
  38. Universal protein-binding microarrays for the comprehensive characterization of the DNA-binding specificities of transcription factors.
    Nat Protoc. 2009;4(3):393-411 PMID: 19265799
  39. Mapping and dynamics of regulatory DNA and transcription factor networks in A. thaliana.
    Cell Rep. 2014 Sep 25;8(6):2015-30 PMID: 25220462
  40. NAC transcription factors: structurally distinct, functionally diverse.
    Trends Plant Sci. 2005 Feb;10(2):79-87 PMID: 15708345
  41. Systematic discovery and characterization of regulatory motifs in ENCODE TF binding experiments.
    Nucleic Acids Res. 2014 Mar;42(5):2976-87 PMID: 24335146
  42. DNA-binding specificities of plant transcription factors and their potential to define target genes.
    Proc Natl Acad Sci U S A. 2014 Feb 11;111(6):2367-72 PMID: 24477691
  43. Competition between DNA methylation and transcription factors determines binding of NRF1.
    Nature. 2015 Dec 24;528(7583):575-9 PMID: 26675734
  44. Arabidopsis AtHB7 and AtHB12 evolved divergently to fine tune processes associated with growth and responses to water stress.
    BMC Plant Biol. 2014 May 31;14:150 PMID: 24884528
  45. g:Profiler--a web server for functional interpretation of gene lists (2011 update).
    Nucleic Acids Res. 2011 Jul;39(Web Server issue):W307-15 PMID: 21646343
  46. The role of bZIP transcription factors in green plant evolution: adaptive features emerging from four founder genes.
    PLoS One. 2008 Aug 13;3(8):e2944 PMID: 18698409
  47. Non-targeted transcription factors motifs are a systemic component of ChIP-seq datasets.
    Genome Biol. 2014 Jul 29;15(7):412 PMID: 25070602
  48. Genome-wide identification of regulatory DNA elements and protein-binding footprints using signatures of open chromatin in Arabidopsis.
    Plant Cell. 2012 Jul;24(7):2719-31 PMID: 22773751
  49. CG methylated microarrays identify a novel methylated sequence bound by the CEBPB|ATF4 heterodimer that is active in vivo.
    Genome Res. 2013 Jun;23(6):988-97 PMID: 23590861
  50. Structural basis for DNA binding specificity by the auxin-dependent ARF transcription factors.
    Cell. 2014 Jan 30;156(3):577-89 PMID: 24485461
  51. MONOPTEROS controls embryonic root initiation by regulating a mobile transcription factor.
    Nature. 2010 Apr 8;464(7290):913-6 PMID: 20220754
  52. Patterns of population epigenomic diversity.
    Nature. 2013 Mar 14;495(7440):193-8 PMID: 23467092
  53. The Arabidopsis abscisic acid response gene ABI5 encodes a basic leucine zipper transcription factor.
    Plant Cell. 2000 Apr;12(4):599-609 PMID: 10760247
  54. DNA-affinity-purified chip (DAP-chip) method to determine gene targets for bacterial two component regulatory systems.
    J Vis Exp. 2014 Jul 21;(89):null PMID: 25079303
  55. High resolution genome wide binding event finding and motif discovery reveals transcription factor spatial binding constraints.
    PLoS Comput Biol. 2012;8(8):e1002638 PMID: 22912568
Article Info
Journal
Cell
Abbr.
Cell
ISSN
1097-4172
DOI
10.1016/j.cell.2016.04.038
Email
ecker@salk.edu
Published
2016-05-19
Pages
1280-1292
Language
English
Region
United States
NLM ID
0413066
PMCID
PMC4907330
Subset
IM
Grants
Howard Hughes Medical Institute · United States
NCI NIH HHS · P30 CA014195 · United States
HHMI · United States
Corrections
ErratumIn
PMID: 27610578
External Links
PubMed source DOI: 10.1016/j.cell.2016.04.038 PMC Full Text View journal details
Analysis Services
Analysis Services

Contact

No. 2 Wenbo Road, Zhangqiu District, Jinan, Shandong

Qilu Normal University · Genelibs Bioinformatics Lab

750 Shunhua Rd, Jinan

2F, Bldg F, University Science Park

Tel: 0531-88819269

WeChat Official Account

Follow our WeChat subscription account for real-time updates and the latest in medical and biological research.


Business Email

E-mail: product@genelibs.com

Copyright © 2026.Genelibs Jinan Honghui Biotechnology Co., Ltd. 鲁ICP备20007159号-2