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Arabidopsis thaliana TBP-associated factor 5 is essential for plant growth and development

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Abstract

The TATA binding protein-associated factor 5 (TAF5) is a subunit of TFIID and SAGA complexes involved in RNA polymerase II transcription initiation and histone acetylation. Although members of the putative SAGA complex in Arabidopsis such as GCN5 and ADA2b have important roles in plant development and abiotic stress responses, the function of other components of the Arabidopsis putative SAGA complex, like TAF5, is unknown. We used reverse genetics to elucidate the biological role of TAF5 in Arabidopsis thaliana. The absence of homozygote taf5 mutants indicated that AtTAF5 is an essential gene for the plant viability. Genetic approaches also revealed that AtTAF5 plays a critical role in regulatory mechanisms involved in male gametogenesis and pollen tube growth. Moreover, Arabidopsis taf5 heterozygous mutants displayed terminal flower-like phenotype, suggesting that TAF5 could be involved in molecular mechanisms that regulate indeterminate inflorescence meristems. Therefore, this work suggests that Arabidopsis TAF5 is necessary and sufficient for a complete plant life cycle.

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References

  • Alonso JM, Stepanova AN, Leisse TJ, Kim CJ, Chen H et al (2003) Genome-wide insertional mutagenesis of Arabidopsis thaliana. Science 301:653–657

    Article  PubMed  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 

  • Apone LM, Virbasius CA, Reese JC, Green MR (1996) Yeast TAFII90 is required for cell-cycle progression through G2/M but not for general transcription activation. Genes Dev 10:2368–2380

    Article  PubMed  CAS  Google Scholar 

  • Baker SP, Grant PA (2007) The SAGA continues: expanding the cellular role of a transcriptional co-activator complex. Oncogene 37:5329–5340

    Article  Google Scholar 

  • Benhamed M, Bertrand C, Servet C, Zhou D-X (2006) Arabidopis 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 

  • Bertrand C, Bergounioux C, Domenichini S, Delarue M, Zhou D-X (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 

  • Bertrand C, Benhamed M, Li Y-F, Ayadi M, Lemonnier G, Renou J-P, Delarue M, Zhou D-X (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 

  • Bhattacharya S, Takada S, Jacobson RH (2007) Structural analysis and dimerization potential of the human TAF5 subunit of TFIID. Proc Natl Acad Sci USA 104:1189–1194

    Article  PubMed  CAS  Google Scholar 

  • Boavista LC, McCormick S (2007) Temperature as a determinant factor for increased and reproducible in vitro pollen germination in Arabidopsis thaliana. Plant J 52:570–582

    Article  Google Scholar 

  • Boavista LC, Shuai B, Yu H-J, Pagnussat GC, Sundaresan V, McCormick S (2009) A collection of Ds insertional mutants associated with defects in male gametophyte development and function in Arabidopsis thaliana. Genetics 181:1369–1385

    Article  Google Scholar 

  • Borges F, Gomes G, Gardner R, Moreno N, McCormick S, Feijo JA, Becker JD (2008) Comparative transcriptomics of Arabidopsis sperm cells. Plant Physiol 148:1168–1181

    Article  PubMed  CAS  Google Scholar 

  • Bradley D, Ratcliffe O, Vincent C, Carpenter R, Coen E (1997) Inflorescence commitment and architecture in Arabidopsis. Science 275:80–83

    Article  PubMed  CAS  Google Scholar 

  • Burley SK, Roeder RG (1996) Biochemistry and structural biology of transcription factor IID (TFIID). Annu Rev Biochem 65:769–799

    Google Scholar 

  • Chalkley GE, Verrijzer CP (1999) DNA binding site selection by RNA polymerase II TAFs: a TAF(II)250-TAF(II)150 complex recognizes the initiator. EMBO J 18:4835–4845

    Article  PubMed  CAS  Google Scholar 

  • Chen Z, Hafidh S, Poh SH, Twell D, Berger F (2009) Hyperproliferation caused by loss of Retinoblastoma prevents cell fate establishment during Arabidopsis male gametogenesis. Proc Natl Acad Sci USA 106:7257–7262

    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 (2006) Multi-tasking on chromatin with the SAGA coactivator complexes. Mutat Res 618:135–148

    Google Scholar 

  • Durso RJ, Fisher AK, Albright-Frey TJ, Reese JC (2001) Analysis of TAF90 mutants displaying allele-specific and broad defects in transcription. Mol Cell Biol 21:7331–7344

    Article  PubMed  CAS  Google Scholar 

  • Freiman RN (2009) Specific variants of general transcription factors regulate germ cell development in diverse organisms. Biochim Biophys Acta Gene Regul Mech 1789:161–166

    Article  CAS  Google Scholar 

  • Furumoto T, Tamada Y, Izumida A, Nakatani H, Hata S, Izui K (2005) Abundant expression in vascular tissue of plant TAF10, an orthologous gene for TATA box-binding protein-associated factor 10, in Flaveria trinervia and abnormal morphology of Arabidopsis thaliana transformants on its overexpression. Plant Cell Physiol 46:108–117

    Article  PubMed  CAS  Google Scholar 

  • Gao X, Ren F, Lu YT (2006) The Arabidopsis mutant stg1 identifies a function for TBP-associated factor 10 in plant osmotic stress adaptation. Plant Cell Physiol 47:1285–1294

    Article  PubMed  CAS  Google Scholar 

  • Gasch A, Hoffmann A, Horikoshi M, Roeder RG, Chua NH (1990) Arabidopsis thaliana contains two genes for TFIID. Nature 346:390–394

    Article  PubMed  CAS  Google Scholar 

  • Gouet P, Courcelle E, Stuart DI, Metoz F (1999) ESPript: multiple sequence alignments in PostScript. Bioinformatics 15:305–308

    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 

  • Green MR (2000) TBP-associated factors (TAFIIs) multiple, selective transcriptional mediators in common complexes. Trends Biochem Sci 25:59–63

    Article  PubMed  CAS  Google Scholar 

  • Gurley WB, O’Grady K, Czarnecka-Verner E, Lawit SJ (2006) General transcription factors and the core promoter: ancient roots. In: Grasser KD (ed) Regulation of transcription in plants. Annu Plant Rev 29:1–21, Blackwell, Oxford

  • Hahn S (1998) The role of TAFs in RNA polymerase II transcription. Cell 95:579–582

    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

    Article  CAS  Google Scholar 

  • Hiller Μ, Lin T-Y, Wood C, Fuller TM (2001) Developmental regulation of transcription by a tissue-specific TAF homolog. Genes Dev 15:1021–1030

    Article  PubMed  CAS  Google Scholar 

  • Hiller Μ, Chen ΧM, Pringle J, Suchorolski M, Sancak Y, Viswanathan S, Bolival B, Lin T-Y, Marino S, Fuller TM (2004) Testis-specific TAF homologs collaborate to control a tissue specific transcription program. Development 131:5297–5308

    Article  PubMed  CAS  Google Scholar 

  • Honys D, Twell D (2004) Transcriptome analysis of haploid male gametophyte development in Arabidopsis. Genome Biol 5:R85. doi:10.1186/gb-2004-5-11-r85

    Article  PubMed  Google Scholar 

  • Johnsson-Brousseau SA, McCormick S (2004) A compendium of methods useful for characterizing Arabidopsis pollen mutants and gametophytically-expressed genes. Plant J 39:761–775

    Article  Google Scholar 

  • Kim HJ, Oh S-A, Brownfield L, Ryu H, Hwang I, Twell D, Nam H-G (2008) Control of plant male germline proliferation by SCFFBL17 degradation of cell cycle inhibitors. Nature 455:1134–1137

    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 

  • Lago C, Clerici E, Mizzi L, Colombo L, Kater MM (2004) TBP-associated factors in Arabidopsis. Gene 342:231–241

    Article  PubMed  CAS  Google Scholar 

  • Lago C, Clerici E, Dreni L, Horlow C, Caporali E, Colombo L, Kater MM (2005) The Arabidopsis TFIID factor AtTAF6 controls pollen tube growth. Dev Biol 285:91–100

    Article  PubMed  CAS  Google Scholar 

  • Lawit JS, O’Grady K, Gurley BW, Czarnecka-Verner E (2007) Yeast two-hybrid map of Arabidopsis TFIID. Plant Mol Biol 64:73–87

    Article  PubMed  CAS  Google Scholar 

  • Lee TI, Young RA (1998) Regulation of gene expression by TBP-associated proteins. Genes Dev 12:1398–1408

    Article  PubMed  CAS  Google Scholar 

  • Leurent C, Sanders SL, Demeny MA, Garbett KA, Ruhlmann C, Weil PA, Tora L, Schultz P (2004) Mapping key functional sites within yeast TFIID. EMBO J 23:719–727

    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 

  • Mandel AM, Yanofsky MF (1995) A gene triggering flower formation in Arabidopsis. Nature 377:522–524

    Article  PubMed  CAS  Google Scholar 

  • McCormick S (1993) Male gametophyte development. Plant Cell 5:1265–1275

    Article  PubMed  Google Scholar 

  • McCormick S (2004) Control of male gametophyte development. Plant Cell 16(Suppl):S142–S153

    Article  PubMed  CAS  Google Scholar 

  • Pina C, Pinto F, Feijo JA, Becker JD (2005) Gene family analysis of the Arabidopsis pollen transcriptome reveals biological implications for cell growth, division control, and gene expression regulation. Plant Physiol 138:744–756

    Article  PubMed  CAS  Google Scholar 

  • Poon D, Bai Y, Campbell AM, Bjorklund S, Kim Y-J, Zhou S, Kornberg RD, Weil PA (1995) Identification and characterization of a TFIID-like multiprotein complex from Saccharomyces cerevisiae. Proc Natl Acad Sci USA 92:8224–8228

    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 

  • Qin Y, Leydon AR, Manziello A, Pandey R, Mount D, Denic S, Vasic B, Johnson MA, Palanivelu R (2009) Penetration of the stigma and style elicits a novel transcriptome in pollen tubes, pointing to genes critical for growth in a pistil. PloS Genet 5:8. doi:10.1371/journal.pgen.1000621

    Article  Google Scholar 

  • Robles LM, Wampole JS, Christians MJ, Larsen PB (2007) Arabidopsis enhanced ethylene response 4 encodes an EIN3-interacting TFIID transcription factor required for proper ethylene response, including ERF1 induction. J Exp Bot 58:2627–2639

    Article  PubMed  CAS  Google Scholar 

  • Roeder RG (1996) The role of general initiation factors in transcription by RNA polymerase II. Trends Biochem Sci 21:327–335

    PubMed  CAS  Google Scholar 

  • Servet C, Conde E, Silva N, Zhou D-X (2010) Histone acetyltransferase AtGCN5/HAG1 is a versatile regulator of developmental and inducible gene expression in Arabidopsis. Mol Plant 34:670–677

    Article  Google Scholar 

  • Sessions A, Burke E, Presting G et al (2002) A high-throughput Arabidopsis reverse genetics system. Plant Cell 14:2985–2994

    Article  PubMed  CAS  Google Scholar 

  • Shannon S, Meeks-Wagner DR (1991) A mutation in the Arabidopsis TFL1 gene affects inflorescence meristem development. Plant Cell 3:877–892

    Article  PubMed  CAS  Google Scholar 

  • Sieberer T, Hauser MT, 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 

  • Smith TF, Gaitatzes C, Saxena K, Neer EJ (1999) The WD40 repeat: a common architecture for diverse functions. Trends Biochem Sci 24:181–185

    Article  PubMed  CAS  Google Scholar 

  • Takada S, Goto K (2003) TERMINAL FLOWER2, an Arabidopsis homolog of HETEROCHROMATIN PROTEIN1, counteracts the activation of FLOWERING LOCUS T by CONSTANS in the vascular tissues of leaves to regulate flowering time. Plant Cell 15:2856–2865

    Article  PubMed  CAS  Google Scholar 

  • Tamada Y, Nakamori K, Nakatani H, Matsuda K, Hata S, Furumoto T, Izui K (2007) Temporary expression of the TAF10 gene and its requirement for normal development of Arabidopsis thaliana. Plant Cell Physiol 48:134–146

    Article  PubMed  CAS  Google Scholar 

  • Tao Y, Guermah M, Martinez E, Oelgeschlager T, Hasegawa S, Takada R, Yamamoto T, Horikoshi M, Roeder RG (1997) Specific interactions and potential functions of human TAFII100. J Biol Chem 272:6714–6721

    Article  PubMed  CAS  Google Scholar 

  • Tora L (2002) A unified nomenclature for TATA box binding protein (TBP)-associated factors (TAFs) involved in RNA polymerase II transcription. Genes Dev 16:673–675

    Article  PubMed  CAS  Google Scholar 

  • Verrijzer CP, Yokomori K, Chen JL, Tjian R (1994) Drosophila TAFII150: similarity to yeast gene TSM-1 and specific binding to core promoter DNA. Science 264:933–941

    Article  PubMed  CAS  Google Scholar 

  • Vlachonasios KE, Thomashow MF, Trizenberg 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 

  • Walker KA, Blackwell TK (2003) A broad but restricted requirement for TAF-5 (Human TAFII100) for embryonic transcription in Caenorhabditis elegans. J Biol Chem 278:6181–6186

    Article  PubMed  CAS  Google Scholar 

  • Wang Y, Zhang WZ, Song LF, Zou JJ, Su Z, Wu WH (2008) Transcriptome analyses show changes in gene expression to accompany pollen germination and tube growth in Arabidopsis. Plant Physiol 148:1201–1211

    Article  PubMed  CAS  Google Scholar 

  • Weigel D, Nilsson O (1995) A developmental switch sufficient for flower initiation in diverse plants. Nature 377:495–500

    Article  PubMed  CAS  Google Scholar 

  • Wright KJ, Marr MT II, Tjian R (2006) TAF4 nucleates a core subcomplex of TFIID and mediates activated transcription from a TATA-less promoter. Proc Natl Acad Sci USA 103:12347–12352

    Article  PubMed  CAS  Google Scholar 

  • Yadegari R, Drews GN (2004) Female gametophyte development. Plant Cell 16(Suppl):S133–S141

    Article  PubMed  CAS  Google Scholar 

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Acknowledgments

We thank Drs Amy Hark (Muhlenberg College) and Vasilis Gegas (John Innes Centre) for thoughtful discussions during the course of this work. We also thank Dr Maria Moustaka and Savvas Genitsaris (Aristotle University of Thessaloniki) for the assistance with fluorescence microscopy. This research was supported by Greek General Secretary of Research and Technology grant number 82337 and by funds from Aristotle University of Thessaloniki, School of Biology to KV.

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  1. Department of Botany, School of Biology, Faculty of Science, Aristotle University of Thessaloniki, 54124, Thessaloniki, Greece

    Niki Mougiou, Stylianos Poulios, Athanasios Kaldis & Konstantinos E. Vlachonasios

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  1. Niki Mougiou
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  2. Stylianos Poulios
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Correspondence to Konstantinos E. Vlachonasios.

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Mougiou, N., Poulios, S., Kaldis, A. et al. Arabidopsis thaliana TBP-associated factor 5 is essential for plant growth and development. Mol Breeding 30, 355–366 (2012). https://doi.org/10.1007/s11032-011-9626-2

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