Two Arabidopsis Homologs of Human Lysine-Specific Demethylase Function in Epigenetic Regulation of Plant Defense Responses

Abstract

Epigenetic marks such as covalent histone modification and DNA methylation are crucial for mitotically and meiotically inherited cellular memory-based plant immunity. However, the roles of individual players in the epigenetic regulation of plant immunity are not fully understood. Here we reveal the functions of two Arabidopsis thaliana homologs of human lysine-specific demethylase1-like1, LDL1 and LDL2, in the maintenance of methyl groups at lysine 4 of histone H3 and in plant immunity to Pseudomonas syringae infection. The growth of virulent P. syringae strains was reduced in ldl1 and ldl2 single mutants compared to wild-type plants. Local and systemic disease resistance responses, which coincided with the rapid, robust transcription of defense-related genes, were more stably expressed in ldl1 ldl2 double mutants than in the single mutants. At the nucleosome level, mono-methylated histone H3K4 accumulated in ldl1 ldl2 plants genome-wide and in the mainly promoter regions of the defense-related genes examined in this study. Furthermore, in silico comparative analysis of RNA-sequencing and chromatin immunoprecipitation data suggested that several WRKY transcription factors, e.g., WRKY22/40/70, might be partly responsible for the enhanced immunity of ldl1 ldl2. These findings suggest that LDL1 and LDL2 control the transcriptional sensitivity of a group of defense-related genes to establish a primed defense response in Arabidopsis.

Priming seeds for the future: Plant immune memory and application in crop protection

“…Functional characterization of histone-modifying enzymes sheds novel light on the epigenetic regulation of plant defense priming and immune memory. AtLDL1 and AtLDL2 were identified as two Arabidopsis homologs of human lysine-specific demethylase1-like1 (LDL1; Noh et al, 2021). The ldl1 ldl2 double mutant displayed increased H3K4me1 accumulation at the promoter regions of defense-related genes, potentiated defenserelated transcription, and enhanced disease resistance against the secondary Pseudomonas infection (Noh et al, 2021).…”

Alternative splicing as a key player in the fine‐tuning of the immunity response in Arabidopsis

“…For example, in the case of Pst‐infected Arabidopsis plants, expression of genes encoding major defence factors, PR1 (PATHOGENESIS‐RELATED GENE 1), PR2, PR5, NPR1 (NONEXPRESSOR OF PATHOGENESIS‐RELATED GENES 1), and PAD4 (PHYTOALEXIN DEFICIENT 4), is induced by histone acetylation and DNA methylation mediated by the Elongator complex (DeFraia et al, 2013; Wang et al, 2013b). Likewise, several other histone deacetylases (e.g., HD2B and HDA6), methyltransferases (e.g., SDG8, SDG25, and OS97), demethylases (e.g., IBM1, JMJ27, LDL1, and LDL2), and ubiquitin ligases (e.g., HUB1 and HUB2) as well as DNA methylases and demethylases (e.g., ROS1 or RNA polymerase V subunits that mediate siRNA‐dependent transcriptional gene silencing) regulate the expression of immune‐responsive genes, including transcription factors, resistance genes, and abscisic acid, salicylic acid, and jasmonic acid hormone signalling genes, in response to pathogen attack (Deleris et al, 2016; Kim, 2021; Noh et al, 2021).…”

“…(DeFraia et al, 2013;Wang et al, 2013b). Likewise, several other histone deacetylases (e.g., HD2B and HDA6), methyltransferases (e.g., SDG8, SDG25, and OS97), demethylases (e.g., IBM1, JMJ27, LDL1, and LDL2), and ubiquitin ligases (e.g., HUB1 and HUB2) as well as DNA methylases and demethylases (e.g., ROS1 or RNA polymerase V subunits that mediate siRNA-dependent transcriptional gene silencing) regulate the expression of immune-responsive genes, including transcription factors, resistance genes, and abscisic acid, salicylic acid, and jasmonic acid hormone signalling genes, in response to pathogen attack (Deleris et al, 2016;Kim, 2021;Noh et al, 2021).…”

Chromosome-level Genomes Reveal the Genetic Basis of Descending Dysploidy and Sex Determination in Morus Plants

“…Mulberry production is severely threatened by diseases, which highlights the importance of breeding programs with a focus on disease resistance for crop improvement. Our selective sweep analyses revealed genomic regions and candidate genes associated with disease resistance, and some selected genes were involved in increasing plant defence responses (e.g., NHL10, LPXD2, CRK10/25, and JMJ25) (Figure 5D) [26][27][28][29][30][31]. Signals for positive selection in cultivars compared with WD were also detected for the gene G2OX8, which encodes the gibberellin 2-betahydroxylase enzyme, resulting in changes in hypocotyl length or plant height via the gibberellin signalling pathway (Figure 5E) [32,33].…”