JMJ27, an Arabidopsis H3K9 histone demethylase, modulates defense against Pseudomonas syringae and flowering time

Abstract

Histone methylation is known to dynamically regulate diverse developmental and physiological processes. Histone methyl marks are written by methyltransferases and erased by demethylases, and result in modification of chromatin structure to repress or activate transcription. However, little is known about how histone methylation may regulate defense mechanisms and flowering time in plants. Here we report characterization of JmjC DOMAIN-CONTAINING PROTEIN 27 (JMJ27), an Arabidopsis JHDM2 (JmjC domain-containing histone demethylase 2) family protein, which modulates defense against pathogens and flowering time. JMJ27 is a nuclear protein containing a zinc-finger motif and a catalytic JmjC domain with conserved Fe(II) and α-ketoglutarate binding sites, and displays H3K9me1/2 demethylase activity both in vitro and in vivo. JMJ27 is induced in response to virulent Pseudomonas syringae pathogens and is required for resistance against these pathogens. JMJ27 is a negative modulator of WRKY25 (a repressor of defense) and a positive modulator of several pathogenesis-related (PR) proteins. Additionally, loss of JMJ27 function leads to early flowering. JMJ27 negatively modulates the major flowering regulator CONSTANS (CO) and positively modulates FLOWERING LOCUS C (FLC). Taken together, our results indicate that JMJ27 functions as a histone demethylase to modulate both physiological (defense) and developmental (flowering time) processes in Arabidopsis.

Plant Immunity: From Signaling to Epigenetic Control of Defense

“…However, similar roles in the regulation of immunity may occur in related proteins. For instance, some proteins belonging to the Jumonji-C demethylase family contribute to immunity by repressing the expression of negative regulators of defense: Arabidopsis JMJ27 represses WRKY25 and WRKY33 by removing H3K9me1/2, while rice JMJ704 is necessary for the repression of OsWRKY66, NRR, and Os-11N3 via H3K4me2/3 demethylation [83,84]. Among the methyltransferases that have been reported to have a role in immunity are ATX1, SDG25, and SDG8, mutants of which are defective in basal defense, necrotroph resistance, and SAR, respectively [85][86][87][88].…”

Arabidopsis thaliana WRKY25 Transcription Factor Mediates Oxidative Stress Tolerance and Regulates Senescence in a Redox-Dependent Manner

“…JMJ27, a jumonji-family demethylases, removes repressive H3K9me2 and H3K9me1 marks and thereby activates transcription. ChIP analysis revealed that the chromatin at the WRKY25 promoter was hyper-methylated in jmj27 mutants indicating that JMJ27 regulates WRKY25 expression at least in part by directly controlling methylation levels of H3K9 histones (Dutta et al, 2017). WRKY53 expression is also regulated by epigenetic changes in histone methylation (Ay et al, 2009).…”

JMJ14 encoded H3K4 demethylase modulates immune responses by regulating defence gene expression and pipecolic acid levels

“…Histone modifications potentially provides a reversible and dynamic way to regulate many biological processes including plant immunity (Ramirez‐Prado et al , ). In Arabidopsis, histone deacetylase HDA6 (Wang et al , ), HDA19 (Zhou et al , ; Choi et al , ), methyltransferases ATX1 (Alvarez‐Venegas et al , ), ATXR7 (Xia et al , ), SDG8 (Berr et al , ) and SDG25 (Lee et al , ), demethylases FLD (Singh et al , ) and JMJ27 (Dutta et al , ), and H2B monoubiquitinase HUB1 (Dhawan et al , ; Zou et al , ), have been previously shown to affect plant resistance. In this study, we have discovered that JMJ14 is a positive regulator of plant immunity.…”