Advertisement

Plant Molecular Biology

, Volume 96, Issue 4–5, pp 367–374 | Cite as

The Arabidopsis histone chaperone FACT is required for stress-induced expression of anthocyanin biosynthetic genes

  • Alexander Pfab
  • Matthias Breindl
  • Klaus D. Grasser
Article

Abstract

Key message

The histone chaperone FACT is involved in the expression of genes encoding anthocyanin biosynthetic enzymes also upon induction by moderate high-light and therefore contributes to the stress-induced plant pigmentation.

Abstract

The histone chaperone FACT consists of the SSRP1 and SPT16 proteins and associates with transcribing RNAPII (RNAPII) along the transcribed region of genes. FACT can promote transcriptional elongation by destabilising nucleosomes in the path of RNA polymerase II, thereby facilitating efficient transcription of chromatin templates. Transcript profiling of Arabidopsis plants depleted in SSRP1 or SPT16 demonstrates that only a small subset of genes is differentially expressed relative to wild type. The majority of these genes is either up- or down-regulated in both the ssrp1 and spt16 plants. Among the down-regulated genes, those encoding enzymes of the biosynthetic pathway of the plant secondary metabolites termed anthocyanins (but not regulators of the pathway) are overrepresented. Upon exposure to moderate high-light stress several of these genes are up-regulated to a lesser extent in ssrp1/spt16 compared to wild type plants, and accordingly the mutant plants accumulate lower amounts of anthocyanin pigments. Moreover, the expression of SSRP1 and SPT16 is induced under these conditions. Therefore, our findings indicate that FACT is a novel factor required for the accumulation of anthocyanins in response to light-induction.

Keywords

SSRP1 SPT16 Chromatin Histones Gene transcription 

Notes

Acknowledgements

We thank Thomas Stempfl for help with the microarray analyses and Gerd Jürgens for the Arabidopsis line harbouring the AtRPS5A::GUS construct. This work was supported by the German Research Foundation (DFG) through Grant Gr1159/14-1 and the EC Research Training Network CHIP-ET, FP7-PEOPLE-2013-ITN607880 to K.D.G.

Author contributions

KDG conceived and supervised the study; AP and KDG designed experiments; AP and MB performed experiments; all authors analysed data; KDG wrote the manuscript; all authors reviewed and edited the manuscript.

Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflict of interests.

Supplementary material

11103_2018_701_MOESM1_ESM.pdf (1.1 mb)
Supplementary material 1 (PDF 1097 KB)

References

  1. Albert NW, Lewis DH, Zhang H, Irving LJ, Jameson PE, Davies KM (2009) Light-induced vegetative anthocyanin pigmentation in Petunia. J Exp Bot 60:2191–2202CrossRefPubMedPubMedCentralGoogle Scholar
  2. Antosch M, Mortensen SA, Grasser KD (2012) Plant proteins containing high mobility group box DNA-binding domains modulate different nuclear processes. Plant Physiol 159:875–883CrossRefPubMedPubMedCentralGoogle Scholar
  3. Antosch M, Schubert V, Holzinger P, Houben A, Grasser KD (2015) Mitotic lifecycle of chromosomal 3xHMG-box proteins and the role of their N-terminal domain in the association with rDNA loci and proteolysis. New Phytol 208:1067–1077CrossRefPubMedGoogle Scholar
  4. Antosz W, Pfab A, Ehrnsberger HF, Holzinger P, Köllen K, Mortensen SA, Bruckmann A, Schubert T, Längst G, Griesenbeck J, Schubert V, Grasser M, Grasser KD (2017) Composition of the Arabidopsis RNA polymerase II transcript elongation complex reveals the interplay between elongation and mRNA processing factors. Plant Cell 29:854–870CrossRefPubMedPubMedCentralGoogle Scholar
  5. Babicki S, Arndt D, Marcu A, Liang Y, Grant JR, Maciejewski A, Wishart DS (2017) Heatmapper: web-enabled heat mapping for all. Nucleic Acid Res 44:W147-W153Google Scholar
  6. Belotserkovskaya R, Oh S, Bondarenko VA, Orphanides G, Studitsky VM, Reinberg D (2003) FACT facilitates transcription-dependent nucleosome alteration. Science 301:1090–1093CrossRefPubMedGoogle Scholar
  7. Bolstad BM, Irizarry RA, Astrand M, Speed TP (2003) A comparison of normalization methods for high density oligonucleotide array data based on variance and bias. Bioinformatics 22:185–193CrossRefGoogle Scholar
  8. Brkljacic J, Grotewold E (2017) Combinatorial control of plant gene expression. Biochim Biophys Acta 1860:31–40CrossRefPubMedGoogle Scholar
  9. Cheung V, Chua G, Batada NN, Landry CR, Michnick SW, Hughes TR, Winston F (2008) Chromatin- and transcription-related factors repress transcription from within coding regions throughout the Saccharomyces cerevisiae genome. PLoS Biol 6:e277CrossRefPubMedPubMedCentralGoogle Scholar
  10. Duroux M, Houben A, Ruzicka K, Friml J, Grasser KD (2004) The chromatin remodelling complex FACT associates with actively transcribed regions of the Arabidopsis genome. Plant J 40:660–671CrossRefPubMedGoogle Scholar
  11. Dürr J, Lolas IB, Sørensen BB, Schubert V, Houben A, Melzer M, Deutzmann R, Grasser M, Grasser KD (2014) The transcript elongation factor SPT4/SPT5 is involved in auxin-related gene expression in Arabidopsis. Nucleic Acid Res 42:4332–4347CrossRefPubMedPubMedCentralGoogle Scholar
  12. Formosa T (2012) The role of FACT in making and breaking nucleosomes. Biochim Biophys Acta 1819:247–255CrossRefPubMedGoogle Scholar
  13. Grasser M, Kane CM, Merkle T, Melzer M, Emmersen J, Grasser KD (2009) Transcript elongation factor TFIIS is involved in Arabidopsis seed dormancy. J Mol Biol 386:598–611CrossRefPubMedGoogle Scholar
  14. Hellemans J, Mortier G, De Paepe A, Speleman F, Vandesompele J (2007) qBase relative quantification framework and software for management and automated analysis of real-time quantitative PCR data. Genome Biol 8:R19CrossRefPubMedPubMedCentralGoogle Scholar
  15. Jefferson RA (1987) Assaying chimeric genes in plants: the GUS gene fusion system. Plant Mol Biol Rep 5:387–405CrossRefGoogle Scholar
  16. Jonkers I, Lis JT (2015) Getting up to speed with transcription elongation by RNA polymerase II. Nat Rev Mol Cell Biol 16:167–177CrossRefPubMedPubMedCentralGoogle Scholar
  17. Kudo T, Sasaki Y, Terashima S, Matsuda-Imai N, Takano T, Saito M, Kanno M, Ozaki S, Suwabe K, Suzuki G, Watanabe M, Matsuoka M, Takayama S, Yano K (2016) Identification of reference genes for quantitative expression analysis using large-scale RNA-seq data of Arabidopsis thaliana and model crop plants. Genes Genet Syst 91:111–125CrossRefPubMedGoogle Scholar
  18. Li G, Zeng SX, Landais I, Lu H (2007) Human SSRP1 has Spt16-dependent and -independent roles in gene transcription. J Biol Chem 282:6936–6945CrossRefPubMedGoogle Scholar
  19. Li S, Wang W, Gao J, Yin K, Wang R, Wang C, Petersen M, Mundy J, Qiu JL (2016) MYB75 phosphorylation by MPK4 Is required for light-induced anthocyanin accumulation in Arabidopsis. Plant Cell 28:2866–2883CrossRefPubMedPubMedCentralGoogle Scholar
  20. Lolas IB, Himanen K, Grønlund JT, Lynggaard C, Houben A, Melzer M, Van Lijsebettens M, Grasser KD (2010) The transcript elongation factor FACT affects Arabidopsis vegetative and reproductive development and genetically interacts with HUB1/2. Plant J 61:686–697CrossRefPubMedGoogle Scholar
  21. Lotkowska ME, Tohge T, Fernie AR, Xue GP, Balazadeh S, Mueller-Roeber B (2015) The Arabidopsis transcription factor MYB112 promotes anthocyanin formation during salinity and under high light stress. Plant Physiol 169:1862–1880PubMedPubMedCentralGoogle Scholar
  22. Mason PB, Struhl K (2003) The FACT complex travels with elongating RNA polymerase II and is important for the fidelity of transcriptional initiation in vivo. Mol Cell Biol 23:8323–8333CrossRefPubMedPubMedCentralGoogle Scholar
  23. Mayer A, Lidschreiber M, Siebert M, Leike K, Söding J, Cramer P (2010) Uniform transitions of the general RNA polymerase II transcription complex. Nat Struct Mol Biol 17:1272–1278CrossRefPubMedGoogle Scholar
  24. Nelissen H, DeGroeve S, Fleury D, Neyt P, Bruno L, Bitonti MB, Vandenbussche F, Van Der Straeten D, Yamaguchi T, Tsukaya H, Witters E, de Jaeger G, Houben A, Van Lijsebettens M (2010) Plant Elongator regulates auxin-related genes during RNA polymerase II-mediated transcription elongation. Proc Natl Acad Sci USA 107:1678–1683CrossRefPubMedPubMedCentralGoogle Scholar
  25. Orphanides G, Wu W-H, Lane WS, Hampsey M, Reinberg D (1999) The chromatin-specific transcription elongation factor FACT comprises human SPT16 and SSRP1 proteins. Nature 400:284–288CrossRefPubMedGoogle Scholar
  26. Perales M, Más P (2007) A functional link between rhythmic changes in chromatin structure and the Arabidopsis biological clock. Plant Cell 19:2111–2123CrossRefPubMedPubMedCentralGoogle Scholar
  27. Pérez-García P, Ma Y, Yanovsky MJ, Mas P (2015) Time-dependent sequestration of RVE8 by LNK proteins shapes the diurnal oscillation of anthocyanin biosynthesis. Proc Natl Acad Sci USA 112:5249–5253CrossRefPubMedPubMedCentralGoogle Scholar
  28. Reinberg D, Sims RJ (2006) de FACTo nucleosome dynamics. J Biol Chem 281:23297–23301CrossRefPubMedGoogle Scholar
  29. Reiter F, Wienerroither S, Stark A (2017) Combinatorial function of transcription factors and cofactors. Curr Opin Genet Dev 43:73–81CrossRefPubMedGoogle Scholar
  30. Saito K, Yonekura-Sakakibara K, Nakabayashi R, Higashi Y, Yamazaki M, Tohge T, Fernie AR (2013) The flavonoid biosynthetic pathway in Arabidopsis: structural and genetic diversity. Plant Physiol Biochem 72:21–34CrossRefPubMedGoogle Scholar
  31. Sims RJ, Belotserkovskaya R, Reinberg D (2004) Elongation by RNA polymerase II: the short and the long of it. Genes Dev 18:2437–2468CrossRefPubMedGoogle Scholar
  32. Tian T, Liu Y, Yan H, You Q, Yi X, Du Z, Xu W, Su Z (2017) agriGO v2.0: a GO analysis toolkit for the agricultural community, 2017 update. Nucleic Acid Res 45:W122-W129PubMedPubMedCentralGoogle Scholar
  33. Valieva ME, Armeev GA, Kudryashova KS, Gerasimova NS, Shaytan AK, Kulaeva OI, McCullough LL, Formosa T, Georgiev PG, Kirpichnikov MP, Studitsky VM, Feofanov AV (2016) Large-scale ATP-independent nucleosome unfolding by a histone chaperone. Nat Struct Mol Biol 23:1111–1116CrossRefPubMedPubMedCentralGoogle Scholar
  34. Van Lijsebettens M, Grasser KD (2014) Transcript elongation factors: shaping transcriptomes after transcript initiation. Trends Plant Sci 19:717–726CrossRefPubMedGoogle Scholar
  35. Vanderauwera S, Zimmermann P, Rombauts S, Vandenabeele S, Langebartels C, Gruissem W, Inzé D, Van Breusegem F (2005) Genome-wide analysis of hydrogen peroxide-regulated gene expression in Arabidopsis reveals a high light-induced transcriptional cluster involved in anthocyanin biosynthesis. Plant Physiol 139:806–821CrossRefPubMedPubMedCentralGoogle Scholar
  36. Wang HY, Klatte M, Jacoby M, Bäumlein H, Weisshaar B, Bauer P (2007) Iron deficiency-mediated stress regulation of four subgroup Ib BHLH genes in Arabidopsis thaliana. Planta 226:897–908CrossRefPubMedGoogle Scholar
  37. Wang N, Cui Y, Liu Y, Fan H, Du J, Huang Z, Yuan Y, Wu H, Ling HQ (2013) Requirement and functional redundancy of Ib subgroup bHLH proteins for iron deficiency responses and uptake in Arabidopsis thaliana. Mol Plant 6:503–513CrossRefPubMedGoogle Scholar
  38. Weijers D, Geldner N, Offringa R, Jürgens G (2001) Early paternal gene activity in Arabidopsis. Nature 414:709–710CrossRefPubMedGoogle Scholar
  39. Xin H, Takahata S, Blanksma M, McCullough L, Stillman DJ, Formosa T (2009) yFACT induces global accessibility of nucleosomal DNA without H2A-H2B displacement. Mol Cell 35:365–376CrossRefPubMedPubMedCentralGoogle Scholar
  40. Yin R, Messner B, Faus-Kessler T, Hoffmann T, Schwab W, Hajirezaei MR, von Saint Paul V, Heller W, Schäffner AR (2012) Feedback inhibition of the general phenylpropanoid and flavonol biosynthetic pathways upon a compromised flavonol-3-O-glycosylation. J Exp Bot 63:2465–2478CrossRefPubMedPubMedCentralGoogle Scholar
  41. Zhou W, Zhu Y, Dong A, Shen W-H (2015) Histone H2A/H2B chaperones: from molecules to chromatin-based functions in plant growth and development. Plant J 83:78–95CrossRefPubMedGoogle Scholar

Copyright information

© Springer Science+Business Media B.V., part of Springer Nature 2018

Authors and Affiliations

  1. 1.Cell Biology & Plant Biochemistry, Biochemistry CentreUniversity of RegensburgRegensburgGermany

Personalised recommendations