H3K27me3 demethylases alter HSP22 and HSP17.6C expression in response to recurring heat in Arabidopsis

Nobutoshi Yamaguchi, Satoshi Matsubara, Kaori Yoshimizu, Motohide Seki, Kouta Hamada, Mari Kamitani, Yuko Kurita, Yasuyuki Nomura, Kota Nagashima, Soichi Inagaki, Takamasa Suzuki, Eng-Seng Gan, Taiko To, Tetsuji Kakutani, Atsushi J. Nagano, Akiko Satake, Toshiro Ito

Acclimation to high temperature increases plants’ tolerance of subsequent lethal high temperatures. Although epigenetic regulation of plant gene expression is well studied, how plants maintain a memory of environmental changes over time remains unclear. Here, we show that JUMONJI (JMJ) proteins, demethylases involved in histone H3 lysine 27 trimethylation (H3K27me3), are necessary for Arabidopsis thaliana heat acclimation. Acclimation induces sustained H3K27me3 demethylation at HEAT SHOCK PROTEIN22 (HSP22) and HSP17.6C loci by JMJs, poising the HSP genes for subsequent activation. Upon sensing heat after a 3-day interval, JMJs directly reactivate these HSP genes. Finally, jmj mutants fail to maintain heat memory under fluctuating field temperature conditions. Our findings of an epigenetic memory mechanism involving histone demethylases may have implications for environmental adaptation of field plants.