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Histone dynamics and roles of histone acetyltransferases during cold-induced gene regulation in Arabidopsis

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Abstract

In Arabidopsis, CBF transcription factors bind to and activate certain cold-regulated (COR) gene promoters during cold acclimation. Consistent with the prevailing model that histone acetylation and nucleosomal depletion correspond with transcriptionally active genes, we now report that H3 acetylation increases and nucleosome occupancy decreases at COR gene promoters upon cold acclimation. Overexpression of CBF1 resulted in a constitutive increase in H3 acetylation and decrease in nucleosome occupancy, consistent with the constitutive activation of COR gene expression. Overexpression of a truncated form of CBF2 lacking its transcriptional activation domain resulted in a cold-stimulated increase in H3 acetylation, but no change in nucleosomal occupancy or COR gene expression, indicating that histone acetylation is congruent with but not sufficient for cold-activation of COR gene expression. Plants homozygous for T-DNA disruption alleles of GCN5 (encoding a histone acetyltransferase) or ADA2b (a GCN5-interacting protein) show diminished expression of COR genes during cold acclimation. Contrary to expectations, H3 acetylation at COR gene promoters was stimulated upon cold acclimation in ada2b and gcn5 plants as in wild type plants, but the decrease in nucleosome occupancy was diminished. Thus, GCN5 is not the HAT responsible for histone acetylation at COR gene promoters during cold acclimation. Several other HAT mutant plants were also tested; although some do affect COR gene expression, none affected histone acetylation. Therefore, H3 acetylation at the COR gene promoters is not solely dependent on any of the HATs tested.

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References

  • Altaf M, Auger A, Monnet-Saksouk J, Brodeur J, Piquet S, Cramet M, Bouchard N, Lacoste N, Utley RT, Gaudreau L, Cote J (2010) NuA4-dependent acetylation of nucleosomal histone H4 and H2A directly stimulates incorporation of H2A.Z by the SWR1 complex. J Biol Chem

  • Artus NN, Uemura M, Steponkus PL, Gilmour SJ, Lin C, Thomashow MF (1996) Constitutive expression of the cold-regulated Arabidopsis thaliana COR15a gene affects both chloroplast and protoplast freezing tolerance. Proc Natl Acad Sci USA 93:13404–13409

    Article  PubMed  CAS  Google Scholar 

  • Ascenzi R, Gantt JS (1999) Subnuclear distribution of the entire complement of linker histone variants in Arabidopsis thaliana. Chromosoma 108:345–355

    Article  PubMed  CAS  Google Scholar 

  • Auty R, Steen H, Myers LC, Persinger J, Bartholomew B, Gygi SP, Buratowski S (2004) Purification of active TFIID from Saccharomyces cerevisiae. Extensive promoter contacts and co-activator function. J Biol Chem 279:49973–49981

    Article  PubMed  CAS  Google Scholar 

  • Baker SP, Grant PA (2007) The SAGA continues: expanding the cellular role of a transcriptional co-activator complex. Oncogene 26:5329–5340

    Article  PubMed  CAS  Google Scholar 

  • Baker SS, Wilhelm KS, Thomashow MF (1994) The 5′-region of Arabidopsis thaliana cor15a has cis-acting elements that confer cold-, drought- and ABA-regulated gene expression. Plant Mol Biol 24:701–713

    Article  PubMed  CAS  Google Scholar 

  • Barbaric S, Reinke H, Horz W (2003) Multiple mechanistically distinct functions of SAGA at the PHO5 promoter. Mol Cell Biol 23:3468–3476

    Article  PubMed  CAS  Google Scholar 

  • Barlev NA, Emelyanov AV, Castagnino P, Zegerman P, Bannister AJ, Sepulveda MA, Robert F, Tora L, Kouzarides T, Birshtein BK, Berger SL (2003) A novel human Ada2 homologue functions with Gcn5 or Brg1 to coactivate transcription. Mol Cell Biol 23:6944–6957

    Article  PubMed  CAS  Google Scholar 

  • Benhamed M, Bertrand C, Servet C, Zhou DX (2006) Arabidopsis GCN5, HD1, and TAF1/HAF2 interact to regulate histone acetylation required for light-responsive gene expression. Plant Cell 18:2893–2903

    Article  PubMed  CAS  Google Scholar 

  • Berger SL (2002) Histone modifications in transcriptional regulation. Curr Opin Genet Dev 12:142–148

    Article  PubMed  CAS  Google Scholar 

  • Bertrand C, Benhamed M, Li YF, Ayadi M, Lemonnier G, Renou JP, Delarue M, Zhou DX (2005) Arabidopsis HAF2 gene encoding TATA-binding protein (TBP)-associated factor TAF1, is required to integrate light signals to regulate gene expression and growth. J Biol Chem 280:1465–1473

    Article  PubMed  CAS  Google Scholar 

  • Bond DM, Dennis ES, Pogson BJ, Finnegan EJ (2009) Histone acetylation, VERNALIZATION INSENSITIVE 3, FLOWERING LOCUS C, and the vernalization response. Mol Plant 2:724–737

    Article  PubMed  CAS  Google Scholar 

  • Bordoli L, Netsch M, Luthi U, Lutz W, Eckner R (2001) Plant orthologs of p300/CBP: conservation of a core domain in metazoan p300/CBP acetyltransferase-related proteins. Nucleic Acids Res 29:589–597

    Article  PubMed  CAS  Google Scholar 

  • Candau R, Zhou JX, Allis CD, Berger SL (1997) Histone acetyltransferase activity and interaction with ADA2 are critical for GCN5 function in vivo. EMBO J 16:555–565

    Article  PubMed  CAS  Google Scholar 

  • Canella D, Gilmour SJ, Kuhn LA, Thomashow MF (2009) DNA binding by the Arabidopsis CBF1 transcription factor requires the PKKP/RAGRxKFxETRHP signature sequence. Biochim Biophys Acta

  • Deng W, Liu C, Pei Y, Deng X, Niu L, Cao X (2007) Involvement of the histone acetyltransferase AtHAC1 in the regulation of flowering time via repression of FLOWERING LOCUS C in Arabidopsis. Plant Physiol 143:1660–1668

    Article  PubMed  CAS  Google Scholar 

  • Doherty CJ (2008) Transcriptional networks involved in response to low temperature stress in Arabidopsis thaliana. Thesis (Ph. D), Michgian State University, Dept. of Biochemistry and Molecular Biology

  • Earley KW, Shook MS, Brower-Toland B, Hicks L, Pikaard CS (2007) In vitro specificities of Arabidopsis co-activator histone acetyltransferases: implications for histone hyperacetylation in gene activation. Plant J 52:615–626

    Article  PubMed  CAS  Google Scholar 

  • Eberharter A, Sterner DE, Schieltz D, Hassan A, Yates JR III, Berger SL, Workman JL (1999) The ADA complex is a distinct histone acetyltransferase complex in Saccharomyces cerevisiae. Mol Cell Biol 19:6621–6631

    PubMed  CAS  Google Scholar 

  • Gamborg OL, Eveleigh DE (1968) Culture methods and detection of glucanases in suspension cultures of wheat and barley. Can J Biochem 46:417–421

    Article  PubMed  CAS  Google Scholar 

  • Gamborg OL, Miller RA, Ojima K (1968) Nutrient requirements of suspension cultures of soybean root cells. Exp Cell Res 50:151–158

    Article  PubMed  CAS  Google Scholar 

  • Gilmour SJ, Lin C, Thomashow MF (1996) Purification and properties of Arabidopsis thaliana COR (cold-regulated) gene polypeptides COR15am and COR6.6 expressed in Escherichia coli. Plant Physiol 111:293–299

    Article  PubMed  CAS  Google Scholar 

  • Gilmour SJ, Zarka DG, Stockinger EJ, Salazar MP, Houghton JM, Thomashow MF (1998) Low temperature regulation of the Arabidopsis CBF family of AP2 transcriptional activators as an early step in cold-induced COR gene expression. Plant J 16:433–442

    Article  PubMed  CAS  Google Scholar 

  • Gilmour SJ, Sebolt AM, Salazar MP, Everard JD, Thomashow MF (2000) Overexpression of the Arabidopsis CBF3 transcriptional activator mimics multiple biochemical changes associated with cold acclimation. Plant Physiol 124:1854–1865

    Article  PubMed  CAS  Google Scholar 

  • Gilmour SJ, Fowler SG, Thomashow MF (2004) Arabidopsis transcriptional activators CBF1, CBF2, and CBF3 have matching functional activities. Plant Mol Biol 54:767–781

    Article  PubMed  CAS  Google Scholar 

  • Govind CK, Zhang F, Qiu H, Hofmeyer K, Hinnebusch AG (2007) Gcn5 promotes acetylation, eviction, and methylation of nucleosomes in transcribed coding regions. Mol Cell 25:31–42

    Article  PubMed  CAS  Google Scholar 

  • Grant PA, Duggan L, Cote J, Roberts SM, Brownell JE, Candau R, Ohba R, Owen-Hughes T, Allis CD, Winston F, Berger SL, Workman JL (1997) Yeast Gcn5 functions in two multisubunit complexes to acetylate nucleosomal histones: characterization of an Ada complex and the SAGA (Spt/Ada) complex. Genes Dev 11:1640–1650

    Article  PubMed  CAS  Google Scholar 

  • Grau B, Popescu C, Torroja L, Ortuno-Sahagun D, Boros I, Ferrus A (2008) Transcriptional adaptor ADA3 of Drosophila melanogaster is required for histone modification, position effect variegation, and transcription. Mol Cell Biol 28:376–385

    Article  PubMed  CAS  Google Scholar 

  • Gu W, Roeder RG (1997) Activation of p53 sequence-specific DNA binding by acetylation of the p53 C-terminal domain. Cell 90:595–606

    Article  PubMed  CAS  Google Scholar 

  • Hajela RK, Horvath DP, Gilmour SJ, Thomashow MF (1990) Molecular cloning and expression of cor (cold-regulated) genes in Arabidopsis thaliana. Plant Physiol 93:1246–1252

    Article  PubMed  CAS  Google Scholar 

  • Han SK, Song JD, Noh YS, Noh B (2007) Role of plant CBP/p300-like genes in the regulation of flowering time. Plant J 49:103–114

    Article  PubMed  CAS  Google Scholar 

  • Hark AT, Vlachonasios KE, Pavangadkar KA, Rao S, Gordon H, Adamakis ID, Kaldis A, Thomashow MF, Triezenberg SJ (2009) Two Arabidopsis orthologs of the transcriptional coactivator ADA2 have distinct biological functions. Biochim Biophys Acta 1789:117–124

    PubMed  CAS  Google Scholar 

  • Herrera FJ, Triezenberg SJ (2004) VP16-dependent association of chromatin-modifying coactivators and underrepresentation of histones at immediate-early gene promoters during herpes simplex virus infection. J Virol 78:9689–9696

    Article  PubMed  CAS  Google Scholar 

  • Hong L, Schroth GP, Matthews HR, Yau P, Bradbury EM (1993) Studies of the DNA binding properties of histone H4 amino terminus. Thermal denaturation studies reveal that acetylation markedly reduces the binding constant of the H4 “tail” to DNA. J Biol Chem 268:305–314

    PubMed  CAS  Google Scholar 

  • Horiuchi J, Silverman N, Pina B, Marcus GA, Guarente L (1997) ADA1, a novel component of the ADA/GCN5 complex, has broader effects than GCN5, ADA2, or ADA3. Mol Cell Biol 17:3220–3228

    PubMed  CAS  Google Scholar 

  • Imhof A, Yang XJ, Ogryzko VV, Nakatani Y, Wolffe AP, Ge H (1997) Acetylation of general transcription factors by histone acetyltransferases. Curr Biol 7:689–692

    Article  PubMed  CAS  Google Scholar 

  • Jaglo-Ottosen KR, Gilmour SJ, Zarka DG, Schabenberger O, Thomashow MF (1998) Arabidopsis CBF1 overexpression induces COR genes and enhances freezing tolerance. Science 280:104–106

    Article  PubMed  CAS  Google Scholar 

  • Jenuwein T, Allis CD (2001) Translating the histone code. Science 293:1074–1080

    Article  PubMed  CAS  Google Scholar 

  • Kornberg RD, Lorch Y (1999) Chromatin-modifying and -remodeling complexes. Curr Opin Genet Dev 9:148–151

    Article  PubMed  CAS  Google Scholar 

  • Krebs JE, Kuo MH, Allis CD, Peterson CL (1999) Cell cycle-regulated histone acetylation required for expression of the yeast HO gene. Genes Dev 13:1412–1421

    Article  PubMed  CAS  Google Scholar 

  • Kuo MH, Allis CD (1998) Roles of histone acetyltransferases and deacetylases in gene regulation. Bioessays 20:615–626

    Article  PubMed  CAS  Google Scholar 

  • Lee TI, Young RA (2000) Transcription of eukaryotic protein-coding genes. Annu Rev Genet 34:77–137

    Article  PubMed  CAS  Google Scholar 

  • Lee DY, Hayes JJ, Pruss D, Wolffe AP (1993) A positive role for histone acetylation in transcription factor access to nucleosomal DNA. Cell 72:73–84

    Article  PubMed  CAS  Google Scholar 

  • Loidl P (1994) Histone acetylation: facts and questions. Chromosoma 103:441–449

    Article  PubMed  CAS  Google Scholar 

  • Mao Y, Pavangadkar KA, Thomashow MF, Triezenberg SJ (2006) Physical and functional interactions of Arabidopsis ADA2 transcriptional coactivator proteins with the acetyltransferase GCN5 and with the cold-induced transcription factor CBF1. Biochim Biophys Acta 1759:69–79

    PubMed  CAS  Google Scholar 

  • Martinez E, Kundu TK, Fu J, Roeder RG (1998) A human SPT3-TAFII31-GCN5-L acetylase complex distinct from transcription factor IID. J Biol Chem 273:23781–23785

    Article  PubMed  CAS  Google Scholar 

  • Meng G, Zhao Y, Nag A, Zeng M, Dimri G, Gao Q, Wazer DE, Kumar R, Band H, Band V (2004) Human ADA3 binds to estrogen receptor (ER) and functions as a coactivator for ER-mediated transactivation. J Biol Chem 279:54230–54240

    Article  PubMed  CAS  Google Scholar 

  • Nag A, Germaniuk-Kurowska A, Dimri M, Sassack MA, Gurumurthy CB, Gao Q, Dimri G, Band H, Band V (2007) An essential role of human Ada3 in p53 acetylation. J Biol Chem 282:8812–8820

    Article  PubMed  CAS  Google Scholar 

  • Nagy Z, Riss A, Romier C, le Guezennec X, Dongre AR, Orpinell M, Han J, Stunnenberg H, Tora L (2009) The human SPT20-containing SAGA complex plays a direct role in the regulation of endoplasmic reticulum stress-induced genes. Mol Cell Biol 29:1649–1660

    Article  PubMed  CAS  Google Scholar 

  • Novillo F, Medina J, Salinas J (2007) Arabidopsis CBF1 and CBF3 have a different function than CBF2 in cold acclimation and define different gene classes in the CBF regulon. Proc Natl Acad Sci USA 104:21002–21007

    Article  PubMed  Google Scholar 

  • Pandey R, Muller A, Napoli CA, Selinger DA, Pikaard CS, Richards EJ, Bender J, Mount DW, Jorgensen RA (2002) Analysis of histone acetyltransferase and histone deacetylase families of Arabidopsis thaliana suggests functional diversification of chromatin modification among multicellular eukaryotes. Nucleic Acids Res 30:5036–5055

    Article  PubMed  CAS  Google Scholar 

  • Pina B, Berger S, Marcus GA, Silverman N, Agapite J, Guarente L (1993) ADA3: a gene, identified by resistance to GAL4-VP16, with properties similar to and different from those of ADA2. Mol Cell Biol 13:5981–5989

    PubMed  CAS  Google Scholar 

  • Pray-Grant MG, Schieltz D, McMahon SJ, Wood JM, Kennedy EL, Cook RG, Workman JL, Yates JR III, Grant PA (2002) The novel SLIK histone acetyltransferase complex functions in the yeast retrograde response pathway. Mol Cell Biol 22:8774–8786

    Article  PubMed  CAS  Google Scholar 

  • Qi D, Larsson J, Mannervik M (2004) Drosophila Ada2b is required for viability and normal histone H3 acetylation. Mol Cell Biol 24:8080–8089

    Article  PubMed  CAS  Google Scholar 

  • Reinke H, Gregory PD, Horz W (2001) A transient histone hyperacetylation signal marks nucleosomes for remodeling at the PHO8 promoter in vivo. Mol Cell 7:529–538

    Article  PubMed  CAS  Google Scholar 

  • Roth SY, Denu JM, Allis CD (2001) Histone acetyltransferases. Annu Rev Biochem 70:81–120

    Article  PubMed  CAS  Google Scholar 

  • Sendra R, Tse C, Hansen JC (2000) The yeast histone acetyltransferase A2 complex, but not free Gcn5p, binds stably to nucleosomal arrays. J Biol Chem 275:24928–24934

    Article  PubMed  CAS  Google Scholar 

  • Shinwari ZK, Nakashima K, Miura S, Kasuga M, Seki M, Yamaguchi-Shinozaki K, Shinozaki K (1998) An Arabidopsis gene family encoding DRE/CRT binding proteins involved in low-temperature-responsive gene expression. Biochem Biophys Res Commun 250:161–170

    Article  PubMed  CAS  Google Scholar 

  • Sterner DE, Grant PA, Roberts SM, Duggan LJ, Belotserkovskaya R, Pacella LA, Winston F, Workman JL, Berger SL (1999) Functional organization of the yeast SAGA complex: distinct components involved in structural integrity, nucleosome acetylation, and TATA-binding protein interaction. Mol Cell Biol 19:86–98

    PubMed  CAS  Google Scholar 

  • Sterner DE, Belotserkovskaya R, Berger SL (2002a) SALSA, a variant of yeast SAGA, contains truncated Spt7, which correlates with activated transcription. Proc Natl Acad Sci USA 99:11622–11627

    Article  PubMed  CAS  Google Scholar 

  • Sterner DE, Wang X, Bloom MH, Simon GM, Berger SL (2002b) The SANT domain of Ada2 is required for normal acetylation of histones by the yeast SAGA complex. J Biol Chem 277:8178–8186

    Article  PubMed  CAS  Google Scholar 

  • Stockinger EJ, Gilmour SJ, Thomashow MF (1997) Arabidopsis thaliana CBF1 encodes an AP2 domain-containing transcriptional activator that binds to the C-repeat/DRE, a cis-acting DNA regulatory element that stimulates transcription in response to low temperature and water deficit. Proc Natl Acad Sci USA 94:1035–1040

    Article  PubMed  CAS  Google Scholar 

  • Stockinger EJ, Mao Y, Regier MK, Triezenberg SJ, Thomashow MF (2001) Transcriptional adaptor and histone acetyltransferase proteins in Arabidopsis and their interactions with CBF1, a transcriptional activator involved in cold-regulated gene expression. Nucleic Acids Res 29:1524–1533

    Article  PubMed  CAS  Google Scholar 

  • Syntichaki P, Topalidou I, Thireos G (2000) The Gcn5 bromodomain co-ordinates nucleosome remodelling. Nature 404:414–417

    Article  PubMed  CAS  Google Scholar 

  • Thomashow MF (2001) So what’s new in the field of plant cold acclimation? Lots!. Plant Physiol 125:89–93

    Article  PubMed  CAS  Google Scholar 

  • Timmers HT, Tora L (2005) SAGA unveiled. Trends Biochem Sci 30:7–10

    Article  PubMed  CAS  Google Scholar 

  • Triezenberg SJ (1995) Structure and function of transcriptional activation domains. Curr Opin Genet Dev 5:190–196

    Article  PubMed  CAS  Google Scholar 

  • Turner BM, O’Neill LP (1995) Histone acetylation in chromatin and chromosomes. Semin Cell Biol 6:229–236

    Article  PubMed  CAS  Google Scholar 

  • Vettese-Dadey M, Walter P, Chen H, Juan LJ, Workman JL (1994) Role of the histone amino termini in facilitated binding of a transcription factor, GAL4-AH, to nucleosome cores. Mol Cell Biol 14:970–981

    PubMed  CAS  Google Scholar 

  • Vlachonasios KE, Thomashow MF, Triezenberg SJ (2003) Disruption mutations of ADA2b and GCN5 transcriptional adaptor genes dramatically affect Arabidopsis growth, development, and gene expression. Plant Cell 15:626–638

    Article  PubMed  CAS  Google Scholar 

  • Wade PA, Pruss D, Wolffe AP (1997) Histone acetylation: chromatin in action. Trends Biochem Sci 22:128–132

    Article  PubMed  CAS  Google Scholar 

  • Wang Z, Triezenberg SJ, Thomashow MF, Stockinger EJ (2005) Multiple hydrophobic motifs in Arabidopsis CBF1 COOH-terminus provide functional redundancy in trans-activation. Plant Mol Biol 58:543–559

    Article  PubMed  CAS  Google Scholar 

  • Wassarman DA, Sauer F (2001) TAF(II)250: a transcription toolbox. J Cell Sci 114:2895–2902

    PubMed  CAS  Google Scholar 

  • Workman JL, Kingston RE (1998) Alteration of nucleosome structure as a mechanism of transcriptional regulation. Annu Rev Biochem 67:545–579

    Article  PubMed  CAS  Google Scholar 

  • Yamaguchi-Shinozaki K, Shinozaki K (1994) A novel cis-acting element in an Arabidopsis gene is involved in responsiveness to drought, low-temperature, or high-salt stress. Plant Cell 6:251–264

    Article  PubMed  CAS  Google Scholar 

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Acknowledgments

This research was supported by grants from the US National Science Foundation (MCB-0240309), the NSF Plant Genome Project (DBI 0110124 and DBI 0701709), the Department of Energy (DE-FG02-91ER20021) and the Michigan Agricultural Experiment Station and by the Van Andel Research Institute. We thank Drs. Kostas Vlachonasios and Amy Hark for thoughtful discussions during the course of this work, and Colleen Doherty and Sarah Gilmour for sharing plant lines and data prior to publication.

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Authors and Affiliations

  1. Graduate Program in Genetics, Michigan State University, East Lansing, MI, 48824, USA

    Kanchan Pavangadkar, Michael F. Thomashow & Steven J. Triezenberg

  2. Department of Microbiology and Molecular Genetics, Michigan State University, East Lansing, MI, 48824, USA

    Kanchan Pavangadkar & Michael F. Thomashow

  3. MSU-DOE Plant Research Laboratory, Michigan State University, East Lansing, MI, 48824, USA

    Michael F. Thomashow

  4. Department of Biochemistry and Molecular Genetics, Michigan State University, East Lansing, MI, 48824, USA

    Steven J. Triezenberg

  5. Van Andel Research Institute, 333 Bostwick NE, Grand Rapids, MI, 49503, USA

    Steven J. Triezenberg

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  1. Kanchan Pavangadkar
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  3. Steven J. Triezenberg
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Correspondence to Steven J. Triezenberg.

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Pavangadkar, K., Thomashow, M.F. & Triezenberg, S.J. Histone dynamics and roles of histone acetyltransferases during cold-induced gene regulation in Arabidopsis. Plant Mol Biol 74, 183–200 (2010). https://doi.org/10.1007/s11103-010-9665-9

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