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PMID: 17138697 Published · ppublish English Journal Article Research Support, Non-U.S. Gov't

CONSTANS and the CCAAT box binding complex share a functionally important domain and interact to regulate flowering of Arabidopsis.

The Plant cell ·Vol. 18 ·No. 11 ·2006-11-00 ·Pages 2971-84

Wenkel S, Turck F, Singer K, Gissot L, Le Gourrierec J, Samach A, Coupland G

Abstract

The CCT (for CONSTANS, CONSTANS-LIKE, TOC1) domain is found in 45 Arabidopsis thaliana proteins involved in processes such as photoperiodic flowering, light signaling, and regulation of circadian rhythms. We show that this domain exhibits similarities to yeast HEME ACTIVATOR PROTEIN2 (HAP2), which is a subunit of the HAP2/HAP3/HAP5 trimeric complex that binds to CCAAT boxes in eukaryotic promoters. Moreover, we demonstrate that CONSTANS (CO), which promotes Arabidopsis flowering, interacts with At HAP3 and At HAP5 in yeast, in vitro, and in planta. Mutations in CO that delay flowering affect residues highly conserved between CCT and the DNA binding domain of HAP2. Taken together, these data suggest that CO might replace At HAP2 in the HAP complex to form a trimeric CO/At HAP3/At HAP5 complex. Flowering was delayed by overexpression of At HAP2 or At HAP3 throughout the plant or in phloem companion cells, where CO is expressed. This phenotype was correlated with reduced abundance of FLOWERING LOCUS T (FT) mRNA and no change in CO mRNA levels. At HAP2 or At HAP3 overexpression may therefore impair formation of a CO/At HAP3/At HAP5 complex leading to reduced expression of FT. During plant evolution, the number of genes encoding HAP proteins was greatly amplified, and these proteins may have acquired novel functions, such as mediating the effect of CCT domain proteins on gene expression.

MeSH Terms
Amino Acid Sequence Arabidopsis/cytology,physiology Arabidopsis Proteins/chemistry,genetics,metabolism CCAAT-Binding Factor/metabolism Circadian Rhythm/physiology DNA-Binding Proteins/chemistry,metabolism Flowers/cytology,physiology Gene Expression Regulation, Plant Molecular Sequence Data Oligopeptides Peptides Protein Binding Protein Structure, Secondary Protein Structure, Tertiary RNA, Messenger/genetics,metabolism Recombinant Fusion Proteins/metabolism Saccharomyces cerevisiae Sequence Alignment Sequence Homology Transcription Factors/chemistry,genetics,metabolism
Chemicals
Arabidopsis Proteins CCAAT-Binding Factor CONSTANS protein, Arabidopsis DNA-Binding Proteins GI protein, Arabidopsis HAP2a protein, Arabidopsis HAP3a protein, Arabidopsis HAP5a protein, Arabidopsis Oligopeptides Peptides RNA, Messenger Recombinant Fusion Proteins Transcription Factors FLAG peptide
Authors & Affiliations
7 authors, click to expand affiliations / ORCID
Wenkel Stephan
Max Planck Institute for Plant Breeding Research, D-50829 Cologne, Germany.
Turck Franziska
Singer Kamy
Gissot Lionel
Le Gourrierec José
Samach Alon
Coupland George
References (71)
71 references, click to expand
  1. Assembly of protein tertiary structures from fragments with similar local sequences using simulated annealing and Bayesian scoring functions.
    J Mol Biol. 1997 Apr 25;268(1):209-25 PMID: 9149153
  2. The Saccharomyces cerevisiae Hap5p homolog from fission yeast reveals two conserved domains that are essential for assembly of heterotetrameric CCAAT-binding factor.
    Mol Cell Biol. 1997 Dec;17(12):7008-18 PMID: 9372932
  3. Arabidopsis LEAFY COTYLEDON1 is sufficient to induce embryo development in vegetative cells.
    Cell. 1998 Jun 26;93(7):1195-205 PMID: 9657152
  4. Multiple genes encoding the conserved CCAAT-box transcription factor complex are expressed in Arabidopsis.
    Plant Physiol. 1998 Jul;117(3):1015-22 PMID: 9662544
  5. Ab initio protein structure prediction of CASP III targets using ROSETTA.
    Proteins. 1999;Suppl 3:171-6 PMID: 10526365
  6. The developmental role of microRNA in plants.
    Curr Opin Plant Biol. 2005 Feb;8(1):38-44 PMID: 15653398
  7. Chromatin immunoprecipitation (ChIP) on chip experiments uncover a widespread distribution of NF-Y binding CCAAT sites outside of core promoters.
    J Biol Chem. 2005 Apr 8;280(14):13606-15 PMID: 15647281
  8. The molecular biology of the CCAAT-binding factor NF-Y.
    Gene. 1999 Oct 18;239(1):15-27 PMID: 10571030
  9. A pair of related genes with antagonistic roles in mediating flowering signals.
    Science. 1999 Dec 3;286(5446):1960-2 PMID: 10583960
  10. Activation tagging of the floral inducer FT.
    Science. 1999 Dec 3;286(5446):1962-5 PMID: 10583961
  11. Integration of spatial and temporal information during floral induction in Arabidopsis.
    Science. 2005 Aug 12;309(5737):1056-9 PMID: 16099980
  12. Arabidopsis SENESCENCE-ASSOCIATED GENE101 stabilizes and signals within an ENHANCED DISEASE SUSCEPTIBILITY1 complex in plant innate immunity.
    Plant Cell. 2005 Sep;17(9):2601-13 PMID: 16040633
  13. The flowering integrator FT regulates SEPALLATA3 and FRUITFULL accumulation in Arabidopsis leaves.
    Plant Cell. 2005 Oct;17(10):2661-75 PMID: 16155177
  14. Assembly of the Hap2p/Hap3p/Hap4p/Hap5p-DNA complex in Saccharomyces cerevisiae.
    Eukaryot Cell. 2005 Nov;4(11):1829-39 PMID: 16278450
  15. The assembly of the CAAT-box binding complex at a photosynthesis gene promoter is regulated by light, cytokinin, and the stage of the plastids.
    J Biol Chem. 1999 Dec 10;274(50):36009-14 PMID: 10585491
  16. Interactions of the developmental regulator ABI3 with proteins identified from developing Arabidopsis seeds.
    Plant J. 2000 Jan;21(2):143-55 PMID: 10743655
  17. Distinct roles of CONSTANS target genes in reproductive development of Arabidopsis.
    Science. 2000 Jun 2;288(5471):1613-6 PMID: 10834834
  18. Cloning of the Arabidopsis clock gene TOC1, an autoregulatory response regulator homolog.
    Science. 2000 Aug 4;289(5480):768-71 PMID: 10926537
  19. Hd1, a major photoperiod sensitivity quantitative trait locus in rice, is closely related to the Arabidopsis flowering time gene CONSTANS.
    Plant Cell. 2000 Dec;12(12):2473-2484 PMID: 11148291
  20. Regulation of the CCAAT-Binding NF-Y subunits in Arabidopsis thaliana.
    Gene. 2001 Feb 21;264(2):173-85 PMID: 11250072
  21. Isolation of a CONSTANS ortholog from Pharbitis nil and its role in flowering.
    Plant Physiol. 2001 Apr;125(4):1821-30 PMID: 11299362
  22. CONSTANS mediates between the circadian clock and the control of flowering in Arabidopsis.
    Nature. 2001 Apr 26;410(6832):1116-20 PMID: 11323677
  23. Rosetta in CASP4: progress in ab initio protein structure prediction.
    Proteins. 2001;Suppl 5:119-26 PMID: 11835488
  24. Functional importance of conserved domains in the flowering-time gene CONSTANS demonstrated by analysis of mutant alleles and transgenic plants.
    Plant J. 2001 Dec;28(6):619-31 PMID: 11851908
  25. Regulation of novel members of the Arabidopsis thaliana CCAAT-binding nuclear factor Y subunits.
    Gene. 2002 Jan 23;283(1-2):41-8 PMID: 11867211
  26. Ternary complex formation between MADS-box transcription factors and the histone fold protein NF-YB.
    J Biol Chem. 2002 Jul 19;277(29):26429-35 PMID: 11971906
  27. De novo prediction of three-dimensional structures for major protein families.
    J Mol Biol. 2002 Sep 6;322(1):65-78 PMID: 12215415
  28. Molecular basis of seasonal time measurement in Arabidopsis.
    Nature. 2002 Sep 19;419(6904):308-12 PMID: 12239570
  29. Hd3a, a rice ortholog of the Arabidopsis FT gene, promotes transition to flowering downstream of Hd1 under short-day conditions.
    Plant Cell Physiol. 2002 Oct;43(10):1096-105 PMID: 12407188
  30. LEAFY COTYLEDON1-LIKE defines a class of regulators essential for embryo development.
    Plant Cell. 2003 Jan;15(1):5-18 PMID: 12509518
  31. The NF-YB/NF-YC structure gives insight into DNA binding and transcription regulation by CCAAT factor NF-Y.
    J Biol Chem. 2003 Jan 10;278(2):1336-45 PMID: 12401788
  32. The Arabidopsis SeedGenes Project.
    Nucleic Acids Res. 2003 Jan 1;31(1):90-3 PMID: 12519955
  33. Arabidopsis LEAFY COTYLEDON1 represents a functionally specialized subunit of the CCAAT binding transcription factor.
    Proc Natl Acad Sci U S A. 2003 Feb 18;100(4):2152-6 PMID: 12578989
  34. The SPA1-like proteins SPA3 and SPA4 repress photomorphogenesis in the light.
    Plant J. 2003 Aug;35(3):373-85 PMID: 12887588
  35. An overview of the CCAAT-box binding factor in filamentous fungi: assembly, nuclear translocation, and transcriptional enhancement.
    Biosci Biotechnol Biochem. 2005 Apr;69(4):663-72 PMID: 15849404
  36. The Arabidopsis pseudo-response regulators, PRR5 and PRR7, coordinately play essential roles for circadian clock function.
    Plant Cell Physiol. 2005 Apr;46(4):609-19 PMID: 15695441
  37. The family of CONSTANS-like genes in Physcomitrella patens.
    Plant Biol (Stuttg). 2005 May;7(3):266-75 PMID: 15912446
  38. The xylem and phloem transcriptomes from secondary tissues of the Arabidopsis root-hypocotyl.
    Plant Physiol. 2005 Jun;138(2):803-18 PMID: 15923329
  39. Activation tagging of a gene for a protein with novel class of CCT-domain activates expression of a subset of sugar-inducible genes in Arabidopsis thaliana.
    Plant J. 2005 Jul;43(1):142-52 PMID: 15960623
  40. FKF1 F-box protein mediates cyclic degradation of a repressor of CONSTANS in Arabidopsis.
    Science. 2005 Jul 8;309(5732):293-7 PMID: 16002617
  41. Distinct roles of GIGANTEA in promoting flowering and regulating circadian rhythms in Arabidopsis.
    Plant Cell. 2005 Aug;17(8):2255-70 PMID: 16006578
  42. FD, a bZIP protein mediating signals from the floral pathway integrator FT at the shoot apex.
    Science. 2005 Aug 12;309(5737):1052-6 PMID: 16099979
  43. The pseudo-response regulator Ppd-H1 provides adaptation to photoperiod in barley.
    Science. 2005 Nov 11;310(5750):1031-4 PMID: 16284181
  44. Arabidopsis response regulators ARR3 and ARR4 play cytokinin-independent roles in the control of circadian period.
    Plant Cell. 2006 Jan;18(1):55-69 PMID: 16326927
  45. The transcription factor FLC confers a flowering response to vernalization by repressing meristem competence and systemic signaling in Arabidopsis.
    Genes Dev. 2006 Apr 1;20(7):898-912 PMID: 16600915
  46. The CCAAT binding factor can mediate interactions between CONSTANS-like proteins and DNA.
    Plant J. 2006 May;46(3):462-76 PMID: 16623906
  47. Genome-wide insertional mutagenesis of Arabidopsis thaliana.
    Science. 2003 Aug 1;301(5633):653-7 PMID: 12893945
  48. Arabidopsis PSEUDO-RESPONSE REGULATOR7 is a signaling intermediate in phytochrome-regulated seedling deetiolation and phasing of the circadian clock.
    Plant Cell. 2003 Nov;15(11):2654-65 PMID: 14563930
  49. FKF1 is essential for photoperiodic-specific light signalling in Arabidopsis.
    Nature. 2003 Nov 20;426(6964):302-6 PMID: 14628054
  50. Photoreceptor regulation of CONSTANS protein in photoperiodic flowering.
    Science. 2004 Feb 13;303(5660):1003-6 PMID: 14963328
  51. The wheat VRN2 gene is a flowering repressor down-regulated by vernalization.
    Science. 2004 Mar 12;303(5664):1640-4 PMID: 15016992
  52. CONSTANS acts in the phloem to regulate a systemic signal that induces photoperiodic flowering of Arabidopsis.
    Development. 2004 Aug;131(15):3615-26 PMID: 15229176
  53. Graft transmission of a floral stimulant derived from CONSTANS.
    Plant Physiol. 2004 Aug;135(4):2271-8 PMID: 15299137
  54. Photoperiod-regulated expression of the PpCOL1 gene encoding a homolog of CO/COL proteins in the moss Physcomitrella patens.
    Biochem Biophys Res Commun. 2004 Nov 26;324(4):1296-301 PMID: 15504355
  55. G to A substitution in the distal CCAAT box of the A gamma-globin gene in Greek hereditary persistence of fetal haemoglobin.
    Nature. 1985 Jan 24-30;313(6000):323-5 PMID: 2578619
  56. Human CCAAT-binding proteins have heterologous subunits.
    Cell. 1988 Apr 8;53(1):11-24 PMID: 3349524
  57. A yeast and a human CCAAT-binding protein have heterologous subunits that are functionally interchangeable.
    Cell. 1988 Apr 8;53(1):25-35 PMID: 3280141
  58. A CCAAT DNA binding factor consisting of two different components that are both required for DNA binding.
    J Biol Chem. 1988 Apr 25;263(12):5940-7 PMID: 3281949
  59. Identification and characterization of HAP4: a third component of the CCAAT-bound HAP2/HAP3 heteromer.
    Genes Dev. 1989 Aug;3(8):1166-78 PMID: 2676721
  60. Weight matrix descriptions of four eukaryotic RNA polymerase II promoter elements derived from 502 unrelated promoter sequences.
    J Mol Biol. 1990 Apr 20;212(4):563-78 PMID: 2329577
  61. The HAP2 subunit of yeast CCAAT transcriptional activator contains adjacent domains for subunit association and DNA recognition: model for the HAP2/3/4 complex.
    Genes Dev. 1990 Oct;4(10):1714-29 PMID: 2123465
  62. Biochemical analysis of the B subunit of the heteromeric CCAAT-binding factor. A DNA-binding domain and a subunit interaction domain are specified by two separate segments.
    J Biol Chem. 1992 Apr 25;267(12):8286-92 PMID: 1569083
  63. Mutations in yeast HAP2/HAP3 define a hybrid CCAAT box binding domain.
    EMBO J. 1993 Dec;12(12):4647-55 PMID: 8223474
  64. Subunit interaction in the CCAAT-binding heteromeric complex is mediated by a very short alpha-helix in HAP2.
    Proc Natl Acad Sci U S A. 1994 Apr 12;91(8):3009-13 PMID: 8159696
  65. Dominant negative analogs of NF-YA.
    J Biol Chem. 1994 Aug 12;269(32):20340-6 PMID: 8051128
  66. Studies on transcription activation by the multimeric CCAAT-binding factor CBF.
    J Biol Chem. 1995 Jan 6;270(1):468-75 PMID: 7814413
  67. Recombinant rat CBF-C, the third subunit of CBF/NFY, allows formation of a protein-DNA complex with CBF-A and CBF-B and with yeast HAP2 and HAP3.
    Proc Natl Acad Sci U S A. 1995 Feb 28;92(5):1624-8 PMID: 7878029
  68. The CONSTANS gene of Arabidopsis promotes flowering and encodes a protein showing similarities to zinc finger transcription factors.
    Cell. 1995 Mar 24;80(6):847-57 PMID: 7697715
  69. Three classes of mutations in the A subunit of the CCAAT-binding factor CBF delineate functional domains involved in the three-step assembly of the CBF-DNA complex.
    Mol Cell Biol. 1996 Jan;16(1):328-37 PMID: 8524312
  70. The transcriptional activity of the CCAAT-binding factor CBF is mediated by two distinct activation domains, one in the CBF-B subunit and the other in the CBF-C subunit.
    J Biol Chem. 1996 Jun 14;271(24):14485-91 PMID: 8662945
  71. Determination of functional domains in the C subunit of the CCAAT-binding factor (CBF) necessary for formation of a CBF-DNA complex: CBF-B interacts simultaneously with both the CBF-A and CBF-C subunits to form a heterotrimeric CBF molecule.
    Mol Cell Biol. 1996 Aug;16(8):4003-13 PMID: 8754798
Article Info
Journal
The Plant cell
Abbr.
Plant Cell
ISSN
1040-4651
Published
2006-11-00
Epub
2006-00-30
Pages
2971-84
Language
English
Region
England
NLM ID
9208688
PMCID
PMC1693937
Subset
IM
Databases
GENBANK
AAC63635, AAN15924
RefSeq
NP_001031887, NP_173616, NP_176013, NP_176726, NP_190428, NP_190902, NP_199575, NP_199858, NP_199859, NP_199860, NP_201152, NP_564180, NP_850305, NP_973796, NP_974030
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