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PMID: 25281686 Published · ppublish English Journal Article Research Support, Non-U.S. Gov't

Chromatin-dependent repression of the Arabidopsis floral integrator genes involves plant specific PHD-containing proteins.

The Plant cell ·Vol. 26 ·No. 10 ·2014-10-00 ·Pages 3922-38

López-González L, Mouriz A, Narro-Diego L, Bustos R, Martínez-Zapater JM, Jarillo JA, Piñeiro M

Abstract

The interplay among histone modifications modulates the expression of master regulatory genes in development. Chromatin effector proteins bind histone modifications and translate the epigenetic status into gene expression patterns that control development. Here, we show that two Arabidopsis thaliana paralogs encoding plant-specific proteins with a plant homeodomain (PHD) motif, SHORT LIFE (SHL) and EARLY BOLTING IN SHORT DAYS (EBS), function in the chromatin-mediated repression of floral initiation and play independent roles in the control of genes regulating flowering. Previous results showed that repression of the floral integrator FLOWERING LOCUS T (FT) requires EBS. We establish that SHL is necessary to negatively regulate the expression of SUPPRESSOR OF OVEREXPRESSION OF CO1 (SOC1), another floral integrator. SHL and EBS recognize di- and trimethylated histone H3 at lysine 4 and bind regulatory regions of SOC1 and FT, respectively. These PHD proteins maintain an inactive chromatin conformation in SOC1 and FT by preventing high levels of H3 acetylation, bind HISTONE DEACETYLASE6, and play a central role in regulating flowering time. SHL and EBS are widely conserved in plants but are absent in other eukaryotes, suggesting that the regulatory module mediated by these proteins could represent a distinct mechanism for gene expression control in plants.

MeSH Terms
Acetylation Amino Acid Sequence Arabidopsis/genetics,growth & development,metabolism Arabidopsis Proteins/genetics,metabolism Chromatin/genetics,metabolism Flowers/genetics,growth & development,metabolism Gene Expression Regulation, Developmental/radiation effects Gene Expression Regulation, Plant/radiation effects Histone Deacetylases/genetics,metabolism Histones/metabolism Homeodomain Proteins/genetics,metabolism Lysine/metabolism MADS Domain Proteins/genetics,metabolism Methylation Molecular Sequence Data Mutation Nuclear Proteins/genetics,metabolism Photoperiod Protein Binding Reverse Transcriptase Polymerase Chain Reaction Sequence Homology, Amino Acid Time Factors
Chemicals
AGL20 protein, Arabidopsis Arabidopsis Proteins Chromatin EBS protein, Arabidopsis FT protein, Arabidopsis Histones Homeodomain Proteins MADS Domain Proteins Nuclear Proteins SHL protein, Arabidopsis HDA6 protein, Arabidopsis Histone Deacetylases Lysine
Authors & Affiliations
7 authors, click to expand affiliations / ORCID
López-González Leticia
Centro de Biotecnología y Genómica de Plantas, Instituto Nacional de Investigaciones Agrarias-Universidad Politécnica de Madrid, 28223 Madrid, Spain.
Mouriz Alfonso
Centro de Biotecnología y Genómica de Plantas, Instituto Nacional de Investigaciones Agrarias-Universidad Politécnica de Madrid, 28223 Madrid, Spain.
Narro-Diego Laura
Centro de Biotecnología y Genómica de Plantas, Instituto Nacional de Investigaciones Agrarias-Universidad Politécnica de Madrid, 28223 Madrid, Spain.
Bustos Regla
Centro de Biotecnología y Genómica de Plantas, Instituto Nacional de Investigaciones Agrarias-Universidad Politécnica de Madrid, 28223 Madrid, Spain.
Martínez-Zapater José Miguel
Instituto de Ciencias de la Vid y del Vino, Consejo Superior de Investigaciones Científicas, Universidad de La Rioja, Gobierno de La Rioja, 26006 Logroño, Spain.
Jarillo Jose A
Centro de Biotecnología y Genómica de Plantas, Instituto Nacional de Investigaciones Agrarias-Universidad Politécnica de Madrid, 28223 Madrid, Spain.
Piñeiro Manuel
Centro de Biotecnología y Genómica de Plantas, Instituto Nacional de Investigaciones Agrarias-Universidad Politécnica de Madrid, 28223 Madrid, Spain [email protected].
References (59)
59 references, click to expand
  1. early bolting in short days: an Arabidopsis mutation that causes early flowering and partially suppresses the floral phenotype of leafy.
    Plant Cell. 2001 May;13(5):1011-24 PMID: 11340178
  2. Decoding of methylated histone H3 tail by the Pygo-BCL9 Wnt signaling complex.
    Mol Cell. 2008 May 23;30(4):507-18 PMID: 18498752
  3. Floral dip: a simplified method for Agrobacterium-mediated transformation of Arabidopsis thaliana.
    Plant J. 1998 Dec;16(6):735-43 PMID: 10069079
  4. Mutations in the Arabidopsis SWC6 gene, encoding a component of the SWR1 chromatin remodelling complex, accelerate flowering time and alter leaf and flower development.
    J Exp Bot. 2008;59(3):653-66 PMID: 18296430
  5. Chromatin regulation of flowering.
    Trends Plant Sci. 2012 Sep;17(9):556-62 PMID: 22658650
  6. Integrative epigenomic mapping defines four main chromatin states in Arabidopsis.
    EMBO J. 2011 May 18;30(10):1928-38 PMID: 21487388
  7. Structural basis of silencing: Sir3 BAH domain in complex with a nucleosome at 3.0 Å resolution.
    Science. 2011 Nov 18;334(6058):977-82 PMID: 22096199
  8. Regulation of flowering time by Arabidopsis MSI1.
    Development. 2006 May;133(9):1693-702 PMID: 16554362
  9. ARABIDOPSIS TRITHORAX-RELATED7 is required for methylation of lysine 4 of histone H3 and for transcriptional activation of FLOWERING LOCUS C.
    Plant Cell. 2009 Oct;21(10):3257-69 PMID: 19855050
  10. Arabidopsis ORC1 is a PHD-containing H3K4me3 effector that regulates transcription.
    Proc Natl Acad Sci U S A. 2009 Feb 10;106(6):2065-70 PMID: 19171893
  11. ARABIDOPSIS TRITHORAX1 dynamically regulates FLOWERING LOCUS C activation via histone 3 lysine 4 trimethylation.
    Plant Cell. 2008 Mar;20(3):580-8 PMID: 18375656
  12. cis-Regulatory elements and chromatin state coordinately control temporal and spatial expression of FLOWERING LOCUS T in Arabidopsis.
    Plant Cell. 2010 May;22(5):1425-40 PMID: 20472817
  13. Distinct roles of CONSTANS target genes in reproductive development of Arabidopsis.
    Science. 2000 Jun 2;288(5471):1613-6 PMID: 10834834
  14. The Arabidopsis PHD-finger protein SHL is required for proper development and fertility.
    Mol Gen Genet. 2000 Nov;264(4):363-70 PMID: 11129039
  15. EARLY BOLTING IN SHORT DAYS is related to chromatin remodeling factors and regulates flowering in Arabidopsis by repressing FT.
    Plant Cell. 2003 Jul;15(7):1552-62 PMID: 12837946
  16. Arabidopsis AL PHD-PRC1 complexes promote seed germination through H3K4me3-to-H3K27me3 chromatin state switch in repression of seed developmental genes.
    PLoS Genet. 2014 Jan;10(1):e1004091 PMID: 24465219
  17. The genetic basis of flowering responses to seasonal cues.
    Nat Rev Genet. 2012 Sep;13(9):627-39 PMID: 22898651
  18. HISTONE DEACETYLASE6 interacts with FLOWERING LOCUS D and regulates flowering in Arabidopsis.
    Plant Physiol. 2011 May;156(1):173-84 PMID: 21398257
  19. The PHD finger: a versatile epigenome reader.
    Trends Biochem Sci. 2011 Jul;36(7):364-72 PMID: 21514168
  20. Histone acetylation: truth of consequences?
    Biochem Cell Biol. 2009 Feb;87(1):139-50 PMID: 19234530
  21. Repression of FLOWERING LOCUS T chromatin by functionally redundant histone H3 lysine 4 demethylases in Arabidopsis.
    PLoS One. 2009 Nov 25;4(11):e8033 PMID: 19946624
  22. Silencing by plant Polycomb-group genes requires dispersed trimethylation of histone H3 at lysine 27.
    EMBO J. 2006 Oct 4;25(19):4638-49 PMID: 16957776
  23. Histone modifications in transcriptional activation during plant development.
    Biochim Biophys Acta. 2011 Oct;1809(10):567-76 PMID: 21777708
  24. Photoperiodic regulation of flowering time through periodic histone deacetylation of the florigen gene FT.
    PLoS Biol. 2013 Sep;11(9):e1001649 PMID: 24019760
  25. Allosteric regulation of transport activity by heterotrimerization of Arabidopsis ammonium transporter complexes in vivo.
    Plant Cell. 2013 Mar;25(3):974-84 PMID: 23463773
  26. Regulation of the floral repressor gene FLC: the complexity of transcription in a chromatin context.
    Curr Opin Plant Biol. 2011 Feb;14(1):38-44 PMID: 20884277
  27. From decision to commitment: the molecular memory of flowering.
    Mol Plant. 2009 Jul;2(4):628-642 PMID: 19825644
  28. The balance between CONSTANS and TEMPRANILLO activities determines FT expression to trigger flowering.
    Curr Biol. 2008 Sep 9;18(17):1338-43 PMID: 18718758
  29. Structural basis for lower lysine methylation state-specific readout by MBT repeats of L3MBTL1 and an engineered PHD finger.
    Mol Cell. 2007 Nov 30;28(4):677-91 PMID: 18042461
  30. Rapid and reversible light-mediated chromatin modifications of Arabidopsis phytochrome A locus.
    Plant Cell. 2011 Feb;23(2):459-70 PMID: 21317377
  31. Arabidopsis TFL2/LHP1 specifically associates with genes marked by trimethylation of histone H3 lysine 27.
    PLoS Genet. 2007 Jun;3(6):e86 PMID: 17542647
  32. ING2 PHD domain links histone H3 lysine 4 methylation to active gene repression.
    Nature. 2006 Jul 6;442(7098):96-9 PMID: 16728974
  33. Flowering time regulation: photoperiod- and temperature-sensing in leaves.
    Trends Plant Sci. 2013 Oct;18(10):575-83 PMID: 23790253
  34. It takes a PHD to read the histone code.
    Cell. 2006 Jul 14;126(1):22-4 PMID: 16839870
  35. A genetic and physiological analysis of late flowering mutants in Arabidopsis thaliana.
    Mol Gen Genet. 1991 Sep;229(1):57-66 PMID: 1896021
  36. UpSET recruits HDAC complexes and restricts chromatin accessibility and acetylation at promoter regions.
    Cell. 2012 Dec 7;151(6):1214-28 PMID: 23177352
  37. SWISS-MODEL: An automated protein homology-modeling server.
    Nucleic Acids Res. 2003 Jul 1;31(13):3381-5 PMID: 12824332
  38. Induction and analysis of gibberellin sensitive mutants in Arabidopsis thaliana (L.) heynh.
    Theor Appl Genet. 1980 Nov;58(6):257-63 PMID: 24301503
  39. Signals and combinatorial functions of histone modifications.
    Annu Rev Biochem. 2011;80:473-99 PMID: 21529160
  40. Remembering the prolonged cold of winter.
    Curr Biol. 2013 Sep 9;23(17):R807-11 PMID: 24028964
  41. A plant-specific histone H3 lysine 4 demethylase represses the floral transition in Arabidopsis.
    Plant J. 2010 May 1;62(4):663-73 PMID: 20202164
  42. Changes in gene expression in response to altered SHL transcript levels.
    Plant Mol Biol. 2003 Dec;53(6):805-20 PMID: 15082927
  43. Regulation of flowering time: all roads lead to Rome.
    Cell Mol Life Sci. 2011 Jun;68(12):2013-37 PMID: 21611891
  44. The Arabidopsis LHP1 protein colocalizes with histone H3 Lys27 trimethylation.
    Nat Struct Mol Biol. 2007 Sep;14(9):869-71 PMID: 17676062
  45. PAF1-complex-mediated histone methylation of FLOWERING LOCUS C chromatin is required for the vernalization-responsive, winter-annual habit in Arabidopsis.
    Genes Dev. 2004 Nov 15;18(22):2774-84 PMID: 15520273
  46. A functional link between rhythmic changes in chromatin structure and the Arabidopsis biological clock.
    Plant Cell. 2007 Jul;19(7):2111-23 PMID: 17616736
  47. The TERMINAL FLOWER2 (TFL2) gene controls the reproductive transition and meristem identity in Arabidopsis thaliana.
    Genetics. 1998 Jun;149(2):597-605 PMID: 9611176
  48. An epigenetic integrator: new insights into genome regulation, environmental stress responses and developmental controls by histone deacetylase 6.
    Plant Cell Physiol. 2012 May;53(5):794-800 PMID: 22253092
  49. EARLY IN SHORT DAYS 7 (ESD7) encodes the catalytic subunit of DNA polymerase epsilon and is required for flowering repression through a mechanism involving epigenetic gene silencing.
    Plant J. 2010 Feb;61(4):623-36 PMID: 19947980
  50. SnapShot: Control of flowering in Arabidopsis.
    Cell. 2010 Apr 30;141(3):550, 550.e1-2 PMID: 20434991
  51. Gene regulation: a finger on the mark.
    Nature. 2006 Jul 6;442(7098):31-2 PMID: 16823438
  52. Mutational analysis of the Sir3 BAH domain reveals multiple points of interaction with nucleosomes.
    Mol Cell Biol. 2009 May;29(10):2532-45 PMID: 19273586
  53. Timing is everything in plant development. The central role of floral repressors.
    Plant Sci. 2011 Oct;181(4):364-78 PMID: 21889042
  54. Arabidopsis ING and Alfin1-like protein families localize to the nucleus and bind to H3K4me3/2 via plant homeodomain fingers.
    Plant J. 2009 May;58(3):511-24 PMID: 19154204
  55. Vernalization: winter and the timing of flowering in plants.
    Annu Rev Cell Dev Biol. 2009;25:277-99 PMID: 19575660
  56. Repression of FLOWERING LOCUS C and FLOWERING LOCUS T by the Arabidopsis Polycomb repressive complex 2 components.
    PLoS One. 2008;3(10):e3404 PMID: 18852898
  57. JMJ14 is an H3K4 demethylase regulating flowering time in Arabidopsis.
    Cell Res. 2010 Mar;20(3):387-90 PMID: 20177424
  58. Chromatin remodeling in plant development.
    Int J Dev Biol. 2009;53(8-10):1581-96 PMID: 19247973
  59. A PHD finger of NURF couples histone H3 lysine 4 trimethylation with chromatin remodelling.
    Nature. 2006 Jul 6;442(7098):86-90 PMID: 16728976
Article Info
Journal
The Plant cell
Abbr.
Plant Cell
ISSN
1532-298X
DOI
10.1105/tpc.114.130781
Email
[email protected]
Published
2014-10-00
Epub
2014-00-03
Pages
3922-38
Language
English
Region
England
NLM ID
9208688
PMCID
PMC4247585
Subset
IM
External Links
PubMed source DOI: 10.1105/tpc.114.130781 PMC Full Text View journal details
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