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

Abstract

Exposure to moderately high temperature enables plants to acquire thermotolerance to high temperatures that might otherwise be lethal. In Arabidopsis thaliana, histone H3 lysine 27 trimethylation (H3K27me3) at the heat shock protein 17.6C (HSP17.6C) and HSP22 loci is removed by Jumonji C domain-containing protein (JMJ) histone demethylases, thus allowing the plant to ‘remember’ the heat experience. Other heat memory genes, such as HSP21, are downregulated in acclimatized jmj quadruple mutants compared to the wild type, but how those genes are regulated remains uncharacterized. Here, we show that histone H3 lysine 4 trimethylation (H3K4me3) at HSP21 was maintained at high levels for at least three days in response to heat. This heat-dependent H3K4me3 accumulation was compromised in the acclimatized jmj quadruple mutant as compared to the acclimatized wild type. JMJ30 directly bound to the HSP21 locus in response to heat and coordinated H3K27me3 and H3K4me3 levels under standard and fluctuating conditions. Our results suggest that JMJs mediate the balance between H3K27me3 and H3K4me3 at the HSP21 locus through proper maintenance of H3K27me3 removal during heat acclimation.

A Review on the Role of Endophytes and Plant Growth Promoting Rhizobacteria in Mitigating Heat Stress in Plants

“…JUMONJI (JMJ proteins are responsible for chromatin organization. These are histone demethylase proteins found in nature [ 111 , 112 , 113 ]. Demethylases are enzymes that eliminate methyl groups from molecules and promote structural support to chromosomes.…”

Epigenetic stress memory: A new approach to study cold and heat stress responses in plants

“…Like the regulation of cold acclimation by reduced H3K27me3, heat tolerance is also regulated by reduced H3K27me3 at HSP17.6C and HSP22 genes mediated by JMJC histone demethylases, thus increasing heat stress memory in Arabidopsis . In addition, the removal of H3K27me3 by JMJC ( Figure 2 ) is to maintain the accumulation of H3K4me3 at HSP21 gene during heat response, suggesting that the balance between H3K27me3 and H3K4me3 levels is required for stress memory ( Yamaguchi and Ito, 2021 ). Reduced H3K9me2 attenuates heat responses and is an important component in the regulation of Fertilization-Independent Endosperm1 ( OsFIE1 ), a member of PRC2, in Arabidopsis seed development under moderate heat stress ( Folsom et al., 2014 ).…”

“…Genes such as HSP17.6C , HSP21 and HSP22 , members of the small HSPs (sHSPs), are key factors of heat stress memory and associated with histone methylation (H3K4me3 and H3K27me3). JMJ genes balance H3K4me3 and H3K27me3 at HSP21 during heat acclimation and activate HSP genes when sensing heat stress, whereas jmj mutants do not maintain heat memory ( Yamaguchi and Ito, 2021 ; Yamaguchi et al., 2021 ). In Arabidopsis , the enzyme Filamentation Temperature-Sensitive H6 (FtsH6) degrades or resets HSP21 abundance during heat stress recovery.…”

Molecular Bases of Heat Stress Responses in Vegetable Crops With Focusing on Heat Shock Factors and Heat Shock Proteins

“…A recent discovery showed that genes encoding stem cell regulators such as CLAVATA1 ( CLV1 ), CLV3 , and HSP17.6A , and the primary carbohydrate metabolism gene FRUCTOSE-BISPHOSPHATE ALDOLASE 6 ( FBA6 ) are involved in the HS transcriptional memory in the shoot apical meristem ( Olas et al, 2021 ). JUMONJI-C DOMAIN CONTAINING PROTEINs ( JMJs ) that code for H3K27me3 demethylases are regulators of heat acclimation through controlling the methylation status of HSP loci ( Pan et al, 2007 ; Xiao et al, 2016 ; Yamaguchi et al, 2021 ; Yamaguchi and Ito, 2021 ).…”