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Arabidopsis thaliana transcriptional co-activators ADA2b and SGF29a are implicated in salt stress responses

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The transcriptional co-activator ADA2b is a component of GCN5-containing complexes in eukaryotes. In Arabidopsis, ada2b mutants result in pleiotropic developmental defects and altered responses to low-temperature stress. SGF29 has recently been identified as another component of GCN5-containing complexes. In the Arabidopsis genome there are two orthologs of yeast SGF29, designated as SGF29a and SGF29b. We hypothesized that, in Arabidopsis, one or both SGF29 proteins may work in concert with ADA2b to regulate genes in response to abiotic stress, and we set out to explore the role of SGF29a and ADA2b in salt stress responses. In root growth and seed germination assays, sgf29a-1 mutants were more resistant to salt stress than their wild-type counterparts, whereas ada2b-1 mutant was hypersensitive. The sgf29a;ada2b double mutant displayed similar phenotypes to ada2b-1 mutant with reduced salt sensitivity. The expression of several abiotic stress-responsive genes was reduced in ada2b-1 mutants after 3 h of salt stress in comparison with sgf29a-1 and wild-type plants. In the sgf29a-1;ada2b-1 double mutant, the salt-induced gene expression was affected similarly to ada2b-1. These results suggest that under salt stress the function of SGF29a was masked by ADA2b and perhaps SGF29a could play an auxiliary role to ADA2b action. In chromatin immunoprecipitation assays, reduced levels of histone H3 and H4 acetylation in the promoter and coding region of COR6.6, RAB18, and RD29b genes were observed in ada2b-1 mutants relative to wild-type plants. In conclusion, ADA2b positively regulates salt-induced gene expression by maintaining the locus-specific acetylation of histones H4 and H3.

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References

  • Abramoff MD, Magelhaes PJ, Ram SJ (2004) Image Processing with ImageJ. Biophoton Inter 11:36–42

    Google Scholar 

  • Anzola JM, Sieberer T, Ortbauer M, Butt H, Korbei B, Weinhofer I, Müllner AE, Luschnig C (2010) Putative Arabidopsis transcriptional adaptor protein (PROPORZ1) is required to modulate histone acetylation in response to auxin. Proc Natl Acad Sci USA 107:10308–10313

    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 

  • 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 

  • Benhamed M, Martin-Magniette ML, Taconnat L, Bitton F, Servet C, De Clercq R, De Meyer B, Buysschaert C, Rombauts S, Villarroel R, Aubourg S, Beynon J, Bhalerao RP, Coupland G, Gruissem W, Menke FLH, Weisshaar B, Renou JP, Zhou DX, Hilson P (2008) Genome-scale Arabidopsis promoter array identifies targets of the histone acetyltransferase GCN5. Plant J 56:493–504

    Article  PubMed  CAS  Google Scholar 

  • Bertrand C, Bergounioux C, Domenichini S, Delarue M, Zhou DX (2003) Arabidopsis histone acetyltransferase AtGCN5 regulates the floral meristem activity through the WUSCHEL/AGAMOUS pathway. J Biol Chem 278:28246–28251

    Article  PubMed  CAS  Google Scholar 

  • Brownell JE, Zhou J, Ranalli T, Kobayashi R, Edmondson DG, Roth SY, Allis CD (1996) Tetrahymena histone acetyltransferase A: a homolog to yeast Gcn5p linking histone acetylation to gene activation. Cell 84:843–851

    Article  PubMed  CAS  Google Scholar 

  • Carré C, Szymczak D, Pidoux J, Antoniewski C (2005) The histone H3 acetylase dGcn5 is a key player in Drosophila melanogaster metamorphosis. Mol Cell Biol 25:8228–8238

    Article  PubMed  Google Scholar 

  • Chen LT, Luo M, Wang YY, Wu K (2010) Involvement of Arabidopsis histone deacetylase HDA6 in ABA and salt stress response. J Exp Bot 61:3345–3353

    Article  PubMed  CAS  Google Scholar 

  • Chinnusamy V, Zhu JK (2009) Epigenetic regulation of stress responses in plants. Curr Opin Plant Biol 12:133–139

    Article  PubMed  CAS  Google Scholar 

  • Ciurciu A, Komonyi O, Pankotai T, Boros IM (2006) The Drosophila histone acetyltransferase Gcn5 and transcriptional adaptor Ada2a are involved in nucleosomal histone H4 acetylation. Mol Cell Biol 26:9413–9423

    Article  PubMed  CAS  Google Scholar 

  • Ciurciu A, Tombacz I, Popescu C, Boros I (2009) GAL4 induces transcriptionally active puff in the absence of dSAGA- and ATAC-specific chromatin acetylation in the Drosophila melanogaster polytene chromosome. Chromosoma 118:513–526

    Article  PubMed  CAS  Google Scholar 

  • Cohen R, Schocken J, Kaldis A, Vlachonasios KE, Hark AT, McCain ER (2009) The histone acetyltransferase GCN5 affects the inflorescence meristem and stamen development in Arabidopsis. Planta 230:1207–1221

    Article  PubMed  CAS  Google Scholar 

  • Daniel JA, Grant PA (2007) Multi-tasking on chromatin with the SAGA coactivator complexes. Mutat Res 618:135–148

    Article  PubMed  CAS  Google Scholar 

  • Fowler S, Thomashow MF (2002) Arabidopsis transcriptome profiling indicates that multiple regulatory pathways are activated during cold acclimation in addition to the CBF cold response pathway. Plant Cell 14:1675–1690

    Article  PubMed  CAS  Google Scholar 

  • Gendrel AV, Lippman Z, Yordan C, Colot V, Martienssen RA (2002) Dependence of heterochromatic histone H3 methylation patterns on the Arabidopsis gene DDM1. Science 297:1871–1873

    Article  PubMed  CAS  Google Scholar 

  • Gilmour SJ, Artus NN, Thomashow MF (1992) cDNA sequence analysis and expression of two cold-regulated genes of Arabidopsis thaliana. Plant Mol Biol 18:13–21

    Article  PubMed  CAS  Google Scholar 

  • Grant PA, Duggan L, Côté 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 

  • Grant PA, Schieltz D, Pray-Grant MG, Steger DJ, Reese JC, Yates JR III, Workman JL (1998) A subset of TAF(II)s are integral components of the SAGA complex required for nucleosome acetylation and transcriptional stimulation. Cell 94:45–53

    Article  PubMed  CAS  Google Scholar 

  • Guelman S, Suganuma T, Florens L, Swanson SK, Kiesecker CL, Kusch T, Anderson S, Yates JR III, Washburn MP, Abmayr SM, Workman JL (2006) Host cell factor and an uncharacterized SANT domain protein are stable components of ATAC, a novel dAda2A/dGcn5-containing histone acetyltransferase complex in Drosophila. Mol Cell Biol 26:871–882

    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 Gene Reg Mech 1789:117–124

    CAS  Google Scholar 

  • Hasewaga PM, Bressan RA, Zhu J-K, Bohnert HJ (2000) Plant cellular and molecular responses to high salinity. Ann Rev Plant Physiol Plant Mol Biol 51:463–499

    Article  Google Scholar 

  • Huang Y, Fang J, Bedford MT, Zhang Y, Xu RM (2006) Recognition of histone H3 lysine-4 methylation by the double tudor domain of JMJD2A. Science 312:748–751

    Article  PubMed  CAS  Google Scholar 

  • Hugouviex V, Kwak JM, Schroeder JI (2001) An mRNA capping protein, ABH1, modulates early abscisic acid signal transduction. Cell 106:477–487

    Article  Google Scholar 

  • Kim JM, To TK, Ishida J, Morosawa T, Kawashima M, Matsui A, Toyoda T, Kimura H, Shinozaki K, Seki M (2008) Alterations of lysine modifications on the histone H3N-tail under drought stress conditions in Arabidopsis thaliana. Plant Cell Physiol 49:1580–1588

    Article  PubMed  CAS  Google Scholar 

  • Kim JM, To TK, Nishioka T, Seki M (2010) Chromatin regulation functions in plant abiotic stress responses. Plant Cell Environ 33:604–611

    Article  PubMed  Google Scholar 

  • Ko JH, Yang SH, Han KH (2006) Upregulation of an Arabidopsis RING-H2 gene, XERICO, confers drought tolerance through increased abscisic acid biosynthesis. Plant J 47:343–355

    Article  PubMed  CAS  Google Scholar 

  • Kornet N, Scheres B (2009) Members of the GCN5 histone acetyltransferase complex regulate PLETHORA-mediated root stem cell niche maintenance and transit amplifying cell proliferation in Arabidopsis. Plant Cell 21:1070–1079

    Article  PubMed  CAS  Google Scholar 

  • Kouzarides T (2007) Chromatin modifications and their function. Cell 128:693–705

    Article  PubMed  CAS  Google Scholar 

  • Kurabe N, Katagiri K, Komiya Y, Ito R, Sugiyama A, Kawasaki Y, Tashiro F (2007) Deregulated expression of a novel component of TFTC/STAGA histone acetyltransferase complexes, rat SGF29, in hepatocellular carcinoma: possible implication for the oncogenic potential of c-Myc. Oncogene 26:5626–5634

    Article  PubMed  CAS  Google Scholar 

  • Kusch T, Guelman S, Abmayr SM, Workman JL (2003) Two Drosophila Ada2 homologues function in different multiprotein complexes. Mol Cell Biol 23:3305–3319

    Article  PubMed  CAS  Google Scholar 

  • Lee J, Thompson JR, Botuyan MV, Mer G (2008) Distinct binding modes specify the recognition of methylated histones H3K4 and H4K20 by JMJD2A-tudor. Nat Struct Mol Biol 15:109–111

    Article  PubMed  CAS  Google Scholar 

  • Long JA, Ohno C, Smith ZR, Meyerowitz EM (2006) TOPLESS regulates apical embryonic fate in Arabidopsis. Science 312:1520–1523

    Article  PubMed  CAS  Google Scholar 

  • Macgregor DR, Deak KI, Ingram PA, Malamy JE (2008) Root system architecture in Arabidopsis grown in culture is regulated by sucrose uptake in the aerial tissues. Plant Cell 20:2643–2660

    Article  PubMed  CAS  Google Scholar 

  • Mantyla E, Lang V, Palva ET (1995) Role of Abscisic acid in drought-induced freezing tolerance, cold acclimation, and accumulation of LT178 and RAB18 proteins in Arabidopsis thaliana. Plant Physiol 107:141–148

    PubMed  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 Gene Str Exp 1759:69–79

    CAS  Google Scholar 

  • Munns R, Tester M (2008) Mechanisms of salinity tolerance. Annu Rev Plant Biol 59:651–681

    Article  PubMed  CAS  Google Scholar 

  • Muratoglu S, Georgieva S, Papai G, Scheer E, Enunlu I, Komonyi O, Cserpan I, Lebedeva L, Nabirochkina E, Udvardy A, Tora L, Boros I (2003) Two different Drosophila ADA2 homologues are present in distinct GCN5 histone acetyltransferase-containing complexes. Mol Cell Biol 23:306–321

    Article  PubMed  CAS  Google Scholar 

  • Nagy Z, Tora L (2007) Distinct GCN5/PCAF-containing complexes function as co-activators and are involved in transcription factor and global histone acetylation. Oncogene 26:5341–5357

    Article  PubMed  CAS  Google Scholar 

  • Nagy Z, Riss A, Fujiyama S, Krebs A, Orpinell M, Jansen P, Cohen A, Stunnenberg HG, Kato S, Tora L (2010) The metazoan ATAC and SAGA coactivator HAT complexes regulate different sets of inducible target genes. Cell Mol Life Sci 67:611–628

    Article  PubMed  CAS  Google Scholar 

  • Pankotai T, Komonyi O, Bodai L, Újfaludi Z, Muratoglu S, Ciurciu A, Tora L, Szabad J, Boros I (2005) The homologous Drosophila transcriptional adaptors ADA2a and ADA2b are both required for normal development but have different functions. Mol Cell Biol 25:8215–8227

    Article  PubMed  CAS  Google Scholar 

  • Pavangadkar K, Thomashow MF, Triezenberg SJ (2010) Histone dynamics and roles of histone acetyltransferases during cold-induced gene regulation in Arabidopsis. Plant Mol Biol 74:183–200

    Article  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 

  • Prigge MJ, Wagner DR (2001) The Arabidopsis SERRATE gene encodes a zinc-finger protein required for normal shoot development. Plant Cell 5:1263–1280

    Article  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 

  • Rodriguez-Navarro S (2009) Insights into SAGA function during gene expression. EMBO Rep 10:843–850

    Article  PubMed  CAS  Google Scholar 

  • Samson F, Brunaud V, Balzergue S, Dubreucq B, Lepiniec L, Pelletier G, Caboche M, Lecharny A (2002) FLAGdb/FST: a database of mapped flanking insertion sites (FSTs) of Arabidopsis thaliana T-DNA transformants. Nucleic Acids Res 30:94–97

    Article  PubMed  CAS  Google Scholar 

  • Sanders SL, Jennings J, Canutescu A, Link AJ, Weil PA (2002) Proteomics of the eukaryotic transcription machinery: identification of proteins associated with components of yeast TFIID by multidimensional mass spectrometry. Mol Cell Biol 22:4723–4738

    Article  PubMed  CAS  Google Scholar 

  • Seki M, Narusaka M, Ishida J, Nanjo T, Fujita M, Oono Y, Kamiya A, Nakajima M, Enju A, Sakurai T, Satou M, Akiyama K, Taji T, Yamaguchi-ShinoZaki K, Carninci P, Kawai J, Hayashizaki Y, Shinozaki K (2002) Monitoring the expression profile of ca. 7000 Arabidopsis genes under drought, cold and high salinity stresses using a full-length cDNA microarray. Plant J 31:279–292

    Article  PubMed  CAS  Google Scholar 

  • Servet C, Benhamed M, Latrasse D, Kim W, Delarue M, Zhou DX (2008) Characterization of a phosphatase 2C protein as an interacting partner of the histone acetyltransferase GCN5 in Arabidopsis. Biochim Biophys Acta Gene Reg Mech 1779:376–382

    CAS  Google Scholar 

  • Servet C, Silva NCE, Zhou DX (2010) Histone acetyltransferase AtGCN5/HAG1 is a versatile regulator of developmental and inducible gene expression in Arabidopsis. Mol Plant 3:670–677

    Article  PubMed  CAS  Google Scholar 

  • Sieberer T, Hauser M, Seifert GJ, Luschnig C (2003) PROPORZ1, a putative Arabidopsis transcriptional adaptor protein, mediates auxin and cytokinin signals in the control of cell proliferation. Curr Biol 13:837–842

    Article  PubMed  CAS  Google Scholar 

  • Sokol A, Kwiatkowska A, Jerzmanowski A, Prymakowska-Bosak M (2007) Up-regulation of stress-inducible genes in tobacco and Arabidopsis cells in response to abiotic stresses and ABA treatment correlates with dynamic changes in histone H3 and H4 modifications. Planta 227:245–254

    Article  PubMed  CAS  Google Scholar 

  • Sridha S, Wu K (2006) Identification of AtHD2C as a novel regulator of abscisic acid responses in Arabidopsis. Plant J 46:124–133

    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 

  • Suganuma T, Gutierrez JL, Li B, Florens L, Swanson SK, Washburn MP, Abmayr SM, Workman JL (2008) ATAC is a double histone acetyltransferase complex that stimulates nucleosome sliding. Nat Struct Mol Biol 15:364–372

    Article  PubMed  CAS  Google Scholar 

  • Thomashow MF (1999) PLANT COLD ACCLIMATION: freezing tolerance genes and regulatory mechanisms. Annu Rev Plant Physiol Plant Mol Biol 50:571–599

    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 

  • Uno Y, Furihata T, Abe H, Yoshida R, Shinozaki K, Yamaguchi-Shinozaki K (2000) Arabidopsis basic leucine zipper transcription factors involved in an abscisic acid-dependent signal transduction pathway under drought and high-salinity conditions. Proc Natl Acad Sci USA 97:11632–11637

    Article  PubMed  CAS  Google Scholar 

  • Vermeulen M, Ebert CH, Matarese F, Marks H, Denissov S, Buttler F, Lee KK, Olsen JV, Hyman AA, Stunnenberg HG, Mann M (2010) Quantitative intection proteomics and genome-wide profiling of epigenetic histone marks and their readers. Cell 142:967–980

    Article  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 

  • Waterborg JH, Harrington RE, Winicov I (1989) Differential histone acetylation in alfalfa (Medicago sativa) due to growth in NaCl: responses in salt stressed and salt tolerant callus cultures. Plant Physiol 90:237–245

    Article  PubMed  CAS  Google Scholar 

  • Xiong L, Zhu JK (2002) Salt tolerance: September 30, 2002. The arabidopsis book. American Society of Plant Biologists, Rockville. 10.1199/tab.0048

  • Xiong L, Gong Z, Rock CD, Subramanian S, Guo Y, Xu W, Galbraith D, Zhu JK (2001a) Modulation of abscisic acid signal transduction and biosynthesis by an Sm-like protein in Arabidopsis. Dev Cell 1:771–781

    Article  PubMed  CAS  Google Scholar 

  • Xiong L, Ishitani M, Lee H, Zhu JK (2001b) The Arabidopsis LOS5/ABA3 locus encodes a molybdenum cofactor sulfurase and modulates cold stress- and osmotic stress-responsive gene expression. Plant Cell 13:2063–2083

    Article  PubMed  CAS  Google Scholar 

  • Xiong L, Lee BH, Ishitani M, Lee H, Zhang C, Zhu JK (2001c) FIERY1 encoding an inositol polyphosphate 1-phosphatase is a negative regulator of abscisic acid and stress signaling in Arabidopsis. Genes Dev 15:1971–1984

    Article  PubMed  CAS  Google Scholar 

  • Xiong L, Schumaker KS, Zhu JK (2002) Cell signaling during cold, drought, and salt stress. Plant Cell 14:S165–S183

    Article  PubMed  CAS  Google Scholar 

  • Xu W, Edmondson DG, Evrard YA, Wakamiya M, Behringer RR, Roth SY (2000) Loss of Gcn5l2 leads to increased apoptosis and mesodermal defects during mouse development. Nat Genet 26:229–232

    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 

  • Yamauchi T, Yamauchi J, Kuwata T, Tamura T, Yamashita T, Bae N, Westphal H, Ozato K, Nakatani Y (2000) Distinct but overlapping roles of histone acetylase PCAF and of the closely related PCAF-B/GCN5 in mouse embryogenesis. Proc Natl Acad Sci USA 97:11303–11306

    Article  PubMed  CAS  Google Scholar 

  • Zentella R, Zhang Z, Park M, Thomas SG, Endo A, Murase K, Fleet CM, Jikumaru Y, Nambara E, Kamiya Y, Sun TP (2007) Global analysis of DELLA direct targets in early gibberellin signaling in Arabidopsis. Plant Cell 19:3037–3057

    Article  PubMed  CAS  Google Scholar 

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Acknowledgments

The authors would like to thank Amy Hark, Muhlenberg College for providing ada2a-2 seeds. We also thank Drs. Amy Hark, Steven Triezenberg (Van Andel Research Institute), Vasilis Gegas (John Innes Centre) and Sotiris Kampranis (Tufts University) for helpful comments on the manuscript. We acknowledge Drs. Moussa Behmamed, Marianne Delarue and Dao-Xiu Zhu, University Paris Sud 11, France for training AK to ChIP assays. OT was supported by an Erasmus-LLP student exchange program between Aristotle University of Thessaloniki and Canakkalle Onsekiz Mart University. This work was supported by Greek General Secretary of Research and Technology grand number 82337 and by funds from Aristotle University of Thessaloniki, School of Biology to KV.

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Correspondence to Konstantinos E. Vlachonasios.

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Kaldis, A., Tsementzi, D., Tanriverdi, O. et al. Arabidopsis thaliana transcriptional co-activators ADA2b and SGF29a are implicated in salt stress responses. Planta 233, 749–762 (2011). https://doi.org/10.1007/s00425-010-1337-0

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