Global regulation of plant immunity by histone lysine methyl transferases

Abstract

Posttranslational modification of histones modulates gene expression affecting diverse biological functions. We showed that the Arabidopsis thaliana histone methyl transferases SET DOMAIN GROUP8 (SDG8) and SDG25 regulate pep1-, flg22-, and effector-triggered immunity as well as systemic acquired resistance. Genome-wide basal and induced transcriptome changes regulated by SDG8 and/or SDG25 showed that two genes of the SDG-dependent transcriptome, CAROTENOID ISOMERASE2 (CCR2) and ECERIFERUM3 (CER3), were also required for plant immunity, establishing mechanisms in defense functions for SDG8 and SDG25. CCR2 catalyzes the biosynthesis of carotenoids, whereas CER3 is involved in the biosynthesis of cuticular wax. SDG8 and SDG25 affected distinct and overlapping global and locus-specific histone H3 lysine 4 (H3K4) and histone H3 lysine 36 (H3K36) methylations. Loss of immunity in sdg mutants was attributed to altered global and CCR2-and CER3-specific histone lysine methylation (HLM). Loss of immunity in sdg, ccr2, and cer3 mutants was also associated with diminished accumulation of lipids and loss of cuticle integrity. In addition, sdg8 and sdg25 mutants were impaired in H2B ubiquitination (H2Bubn) at CCR2, CER3, and H2Bubn regulated R gene, SNC1, revealing crosstalk between the two types of histone modifications. In summary, SDG8 and SDG25 contribute to plant immunity directly through HLM or indirectly through H2Bubn and by regulating expression of plant immunity genes, accumulation of lipids, biosynthesis of carotenoids, and maintenance of cuticle integrity.

Arabidopsis SDG8 Potentiates the Sustainable Transcriptional Induction of the Pathogenesis-Related Genes PR1 and PR2 During Plant Defense Response

“…We also detected in sdg8-1 an increased susceptibility and bacterial growth at 3 dpi when the virulent strain Pst DC3000 was used (Figures 1A,B). Previously, similar observations were made when the allelic mutant lines sdg8-2 (Palma et al, 2010;Lee et al, 2016) and sdg8-4 (De-La-Peña et al, 2012) were infected with Pst. In addition, we noted that sdg8-1 supported higher growth of the virulent than the avirulent Pst strain (Figure 1B), suggesting that ETI still operate in the mutant, but less efficiently than in WT plants.…”

“…Four HKMTs, exclusively from the TrxG group were so far reported to directly or indirectly contribute to the regulation of plant immunity, with their corresponding mutant being more susceptible to some pathogens (Alvarez-Venegas et al, 2007;Berr et al, 2010;Palma et al, 2010;De-La-Peña et al, 2012;Xia et al, 2013;Lee et al, 2016). Among them, the H3K36 di-and tri-methyltransferase SET DOMAIN GROUP 8 (SDG8) was involved in many biological processes, including the regulation of flowering time, organ growth, ovule and anther development, seed development, carotenoid biosynthesis, brassinosteroid-regulated gene expression, light-and/or carbonresponsive gene expression and RNA processing in response to temperature or nitrate signaling (Soppe et al, 1999;Zhao et al, 2005;Dong et al, 2008;Xu et al, 2008;Cazzonelli et al, 2009b;Grini et al, 2009;Tang et al, 2012;Li et al, 2019).…”

“…In addition, the H3K36 methylation deficient sdg8 mutant was also found more susceptible to hemibiotrophic pathogens and the SDG8 methyltransferase activity was suggested to be required for ETI through the establishment and/or maintenance of a transcription-permissive chromatin state at two R-genes (i.e., RPM1 and LAZ5, a RPS4like R-protein encoding gene; Palma et al, 2010). More recently, SDG8 together with SDG25 were proposed to contribute to immunity at least partly through the regulation of CAROTENOID ISOMERASE2 (CCR2) and ECERIFERUM3 (CER3/WAX2), two genes encoding enzymes involved in carotenoids and cuticular wax biosynthesis, respectively (Lee et al, 2016).…”

Interactive and noninteractive roles of histone H2B monoubiquitination and H3K36 methylation in the regulation of active gene transcription and control of plant growth and development

“…Among others, both H3K4me3 and H3K36me3 are associated with active transcription of flowering time genes (He, 2009;Berr et al, 2011). Loss-of-function of SET DOMAIN GROUP 8 (SDG8), which encodes a major H3K36methyltransferase in Arabidopsis, leads to early flowering (Kim et al, 2005b;Zhao et al, 2005;Xu et al, 2008) and reduced resistance to pathogens (Berr et al, 2010a;Palma et al, 2010;Lee et al, 2016), two phenotypes similar to the ones described in hub1/hub2 mutants.…”

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.…”