Removal of repressive histone marks creates epigenetic memory of recurring heat inArabidopsis

Abstract

1 Acclimation to high temperature increases plants' tolerance of subsequent 2 lethal high temperatures 1-3 . Although epigenetic regulation of plant gene 3 expression is well studied, how plants maintain a memory of environmental 4 changes over time remains unclear. Here, we show that JUMONJI (JMJ) 5 proteins 4-8 , demethylases involved in histone H3 lysine 27 trimethylation 6 (H3K27me3), are necessary for Arabidopsis thaliana heat acclimation. 7 Acclimation induces sustained H3K27me3 demethylation at key HEAT SHOCK 8 PROTEIN (HSP) loci by JMJs, poising the HSP genes for subsequent 9 activation. Upon sensing heat after a 3-day interval, JMJs directly reactivate 10 HSP genes. Finally, jmj mutants fail to maintain heat memory under fluctuating 11field temperature conditions. Our findings of an epigenetic memory mechanism 12 involving histone demethylases may have implications for environmental 13 adaptation of field plants. 14 15 3 Main 1 The ability to adapt to environmental changes is essential for plants, as sessile 2 organisms, to survive 1 . Plants memorize heat experience over several days and 3 develop future responsiveness 2 . Exposure to moderate temperature enables 4 plants to acquire thermotolerance for subsequent lethal high temperature 3 . In 5 Arabidopsis thaliana, HEAT SHOCK TRANSCRIPTION FACTOR A2 (HSFA2) 6 is necessary for the maintenance of acquired thermotolerance 9, 10 . HEAT 7 SHOCK PROTEIN (HSP) genes encode molecular chaperones that protect 8 cellular proteins from denaturation. Upon sensing of high temperature, the 9 transient binding of HSFA2 at HSPs governs the sustained increase of histone 10 marks such as histone H3 lysine 4 trimethylation (H3K4me3) and the 11 expression of the HSP genes 11-13 . Then, the expression of heat-memory genes 12 declines gradually while H3K4me3 levels remain high. In that situation, proper 13 maintenance of repressive histone marks should also play important roles in the 14 downregulation of HSP genes 13 . Despite the importance of histone modification 15 enzymes, little is known about the underlying mechanism of those enzymes in 16 flexible and reversible HSP gene expression. 17 JUMONJI (JMJ) proteins 4-8 , demethylases involved in histone H3 18 lysine 27 trimethylation (H3K27me3), are evolutionarily conserved and regulate 19diverse biological processes. In this study, we investigate the role these 20 H3K27me3 demethylases on acquired thermotolerance in response to recurring 21 heat. We demonstrate that JMJ proteins keep repressive histone marks at low 22 levels on chaperone-encoding small HSPs 11-13 that function as memory genes. 23Using inducible JMJs and mutants of small HSPs, we demonstrate the 24 underlying cause of heat memory is the lower H3K27me3 on small HSPs. This 25 histone modification-based transcriptional memory is well-aligned with a 26 mathematical stochastic model that we developed, which predicts expression 27 levels of sHSPs. Moreover, we recapitulate fluctuating temperature conditions 28 and suggest that JMJ-mediated sustained H3K27me3 dem...

Histone Demethylases Coordinate the Antagonistic Interaction Between Abscisic Acid and Brassinosteroid Signaling in Arabidopsis

“…To test if JMJ30 and JMJ32 upregulate BZR1 in response to ABA through histone demethylation, we first measured the H3K27me3 levels in the BZR1 locus. In a published genome-wide ChIP-seq dataset, the gene body of the BZR1 was covered with H3K27me3 repressive marks in the absence of hormones, in both wild type and jmj30 jmj32 ref6 elf6 mutants ( Figure 3D ; Yamaguchi et al, 2020 ). H3 levels were also similar in these samples ( Figure 3D ).…”

“…Thus, JMJ30 and JMJ32 control the ABA and BR signal transduction pathways by regulating distinct downstream targets to balance growth and stress responses through H3K27me3 removal ( Figure 7 ). Overall, H3K27 demethylases tend to have redundant roles during plant development and stress responses ( Lu et al, 2011 ; Gan et al, 2014 ; Zheng et al, 2019 ; Yamaguchi et al, 2020 ). Unlike JMJ30 and JMJ32, ELF6, and REF6 could also control H3K9me3 in a direct way by unknown mechanisms ( Yu et al, 2008 ).…”

JMJ Histone Demethylases Balance H3K27me3 and H3K4me3 Levels at the HSP21 Locus during Heat Acclimation in Arabidopsis

“…All Arabidopsis thaliana lines used in this study were in the Columbia (Col-0) background. The jmj30-2 jmj32-1 elf6-1 ref6-3 quadruple mutant was described previously [19]. Prior to growth, genotypes were confirmed by PCR using Emerald Amp polymerase (Takara, Japan) (Figure S1).…”

“…Five Arabidopsis Jumonji C domain-containing proteins (JMJs), JMJ30, JMJ32, early flowering (ELF), relative of elf (REF6), and JMJ13, are reported to have H3K27 demethylase activity [12][13][14][15][16][17][18]. We recently reported that JMJ30, JMJ32, REF6, and ELF6 are redundantly required for heat acclimation [19]. After exposure to moderate temperature, JMJs affect the expression of several HSP genes, including HSP21 [20], and remove H3K27me3 at the HSP22 and HSP17.6C loci [21].…”

Histone Demethylases as Counterbalance to H3K27me3 Silencing in Plants

“…In addition to the circadian cycle, Arabidopsis JMJ30 also influences several developmental processes. For example, JMJ30 promotes callus formation from leaf explants ( Lee et al., 2018 ), contributes to abscisic acid-dependent growth arrest ( Wu et al., 2019 ), and has been recently found important for plant heat acclimation ( Yamaguchi et al., 2020 ). This chromatin factor is especially relevant in regulating flowering time.…”