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Molecular Genetics and Genomics

, Volume 286, Issue 5–6, pp 321–332 | Cite as

Arabidopsis HsfA1 transcription factors function as the main positive regulators in heat shock-responsive gene expression

  • Takumi Yoshida
  • Naohiko Ohama
  • Jun Nakajima
  • Satoshi Kidokoro
  • Junya Mizoi
  • Kazuo Nakashima
  • Kyonoshin Maruyama
  • Jong-Myong Kim
  • Motoaki Seki
  • Daisuke Todaka
  • Yuriko Osakabe
  • Yoh Sakuma
  • Friedrich Schöffl
  • Kazuo Shinozaki
  • Kazuko Yamaguchi-Shinozaki
Original Paper

Abstract

Arabidopsis DREB2A is a key transcription factor of heat- and drought-responsive gene expression, and DREB2A expression is induced by these stresses. We analyzed the DREB2A promoter and found a heat shock element that functions as a cis-acting element in the heat shock (HS)-responsive expression of DREB2A. Among the 21 Arabidopsis heat shock factors, we chose 4 HsfA1-type proteins as candidate transcriptional activators (HsfA1a, HsfA1b, HsfA1d, and HsfA1e) based on transactivation activity and expression patterns. We generated multiple mutants and found that the HS-responsive expression of DREB2A disappeared in hsfa1a/b/d triple and hsfa1a/b/d/e quadruple mutants. Moreover, HS-responsive gene expression, including that of molecular chaperones and transcription factors, was globally and drastically impaired in the hsfa1a/b/d triple mutant, which exhibited greatly reduced tolerance to HS stress. HsfA1 protein accumulation in the nucleus was negatively regulated by their interactions with HSP90, and other factors potentially strongly activate the HsfA1 proteins under HS stress. The hsfa1a/b/d/e quadruple mutant showed severe growth retardation, and many genes were downregulated in this mutant even under non-stress conditions. Our study indicates that HsfA1a, HsfA1b, and HsfA1d function as main positive regulators in HS-responsive gene expression and four HsfA1-type proteins are important in gene expression for normal plant growth.

Keywords

Heat shock transcription factors DREB2A Heat stress tolerance HSP90 Plant growth 

Abbreviations

BiFC

Bimolecular fluorescence complementation

CFP

Cyan fluorescent protein

ChIP

Chromatin immunoprecipitation

DRE

Dehydration-responsive element

DREB2A

Dehydration-responsive element binding protein 2A

GDA

Geldanamycin

GFP

Green fluorescent protein

GM

Germination medium

GUS

β-Glucuronidase

HS

Heat shock

HSE

Heat shock element

HSF

Heat shock factor

HSP

Heat shock protein

LUC

Luciferase

NES

Nuclear export signal

qRT-PCR

Quantitative real-time PCR

ROS

Reactive oxygen species

WT

Wild type

YFP

Yellow fluorescent protein

Notes

Acknowledgments

This work was supported by Grant-in-Aid for JSPS Fellows (21.5337 to T.Y.), the Grants-in-Aid for Scientific Research on Innovative Areas 22119004, SATREPS of Japan Science and Technology Agency, the Program for Promotion of Basic and Applied Researches for Innovations in Bio-oriented Industry (BRAIN), and grants from the Ministry of Agriculture, Forestry and Fisheries, Japan.

Supplementary material

438_2011_647_MOESM1_ESM.xls (1.2 mb)
Supplementary material 1 (XLS 1225 kb)
438_2011_647_MOESM2_ESM.pdf (6.9 mb)
Supplementary material 1 (PDF 7077 kb)

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Copyright information

© Springer-Verlag 2011

Authors and Affiliations

  • Takumi Yoshida
    • 1
  • Naohiko Ohama
    • 1
  • Jun Nakajima
    • 1
  • Satoshi Kidokoro
    • 1
    • 2
  • Junya Mizoi
    • 1
    • 2
  • Kazuo Nakashima
    • 2
  • Kyonoshin Maruyama
    • 2
  • Jong-Myong Kim
    • 3
  • Motoaki Seki
    • 3
  • Daisuke Todaka
    • 1
    • 2
  • Yuriko Osakabe
    • 1
  • Yoh Sakuma
    • 1
    • 2
  • Friedrich Schöffl
    • 4
  • Kazuo Shinozaki
    • 3
  • Kazuko Yamaguchi-Shinozaki
    • 1
    • 2
  1. 1.Laboratory of Plant Molecular Physiology, Graduate School of Agricultural and Life SciencesThe University of TokyoTokyoJapan
  2. 2.Biological Resources and Post-harvest DivisionJapan International Research Center for Agricultural SciencesTsukubaJapan
  3. 3.RIKEN Plant Science CenterYokohamaJapan
  4. 4.ZMBP-Allgemeine Genetik, Universitaet TübingenTübingenGermany

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