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

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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.

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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

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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.

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Authors and Affiliations

  1. Laboratory of Plant Molecular Physiology, Graduate School of Agricultural and Life Sciences, The University of Tokyo, Tokyo, 113-8657, Japan

    Takumi Yoshida, Naohiko Ohama, Jun Nakajima, Satoshi Kidokoro, Junya Mizoi, Daisuke Todaka, Yuriko Osakabe, Yoh Sakuma & Kazuko Yamaguchi-Shinozaki

  2. Biological Resources and Post-harvest Division, Japan International Research Center for Agricultural Sciences, Tsukuba, Ibaraki, 305-8686, Japan

    Satoshi Kidokoro, Junya Mizoi, Kazuo Nakashima, Kyonoshin Maruyama, Daisuke Todaka, Yoh Sakuma & Kazuko Yamaguchi-Shinozaki

  3. RIKEN Plant Science Center, Yokohama, Kanagawa, 230-0045, Japan

    Jong-Myong Kim, Motoaki Seki & Kazuo Shinozaki

  4. ZMBP-Allgemeine Genetik, Universitaet Tübingen, 72075, Tübingen, Germany

    Friedrich Schöffl

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  1. Takumi Yoshida
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  2. Naohiko Ohama
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  3. Jun Nakajima
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  14. Kazuo Shinozaki
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  15. Kazuko Yamaguchi-Shinozaki
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Corresponding author

Correspondence to Kazuko Yamaguchi-Shinozaki.

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Communicated by A. Schnittger.

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Yoshida, T., Ohama, N., Nakajima, J. et al. Arabidopsis HsfA1 transcription factors function as the main positive regulators in heat shock-responsive gene expression. Mol Genet Genomics 286, 321–332 (2011). https://doi.org/10.1007/s00438-011-0647-7

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