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.

Cyclic dipeptides (CDPs) are one of the simplest compounds produced by living organisms. Plant-growth promoting rhizobacteria (PGPRs) also produce CDPs that can induce disease resistance. Bacillus vallismortis strain BS07 producing various CDPs has been evaluated as a potential biocontrol agent against multiple plant pathogens in chili pepper. However, plant signal pathway triggered by CDPs has not been fully elucidated yet. Here we introduce four CDPs, cyclo(Gly-L-Pro) previously identified from Aspergillus sp., and cyclo(L-Ala-L-Ile), cyclo(L-Ala-L-Leu), and cyclo(LLeu-L-Pro) identified from B. vallismortis BS07, which induce disease resistance in Arabidopsis against Pseudomonas syringae infection. The CDPs do not directly inhibit fungal and oomycete growth in vitro. These CDPs require PHYTOALEXIN DEFICIENT4, SALICYLIC ACID INDUCTION DEFICIENT2, and NONEXPRESSOR OF PATHOGENESIS-RELATED PROTEINS1 important for salicylic acid-dependent defense to induce resistance. On the other hand, regulators involved in jasmonate-dependent event, such as ETHYLENE RECEPTOR1, JASMONATE RESPONSE1, and JASMONATE INSENSITIVE1, are necessary to the CDP-induced resistance. Furthermore, treatment of these CDPs primes Arabidopsis plants to rapidly express PATHOGENESIS-RELATED PROTEIN4 at early infection phase. Taken together, we propose that these CDPs from PGPR strains accelerate activation of jasmonate-related signaling pathway during infection.

Immunity in plants arises from defense regulatory circuits that can be conceptualized as modules. Both the types (and isolates) of pathogen and the repertoire of plant receptors may cause different modules to be activated and affect the magnitude of activation. Two major defense enzymes of Arabidopsis are ALD1 and ICS1/SID2. ALD1 is an aminotransferase needed for producing the metabolites pipecolic acid, hydroxy-pipecolic acid, and possibly other defense signals. ICS1/SID2 produces isochorismate, an intermediate in the synthesis of salicylic acid (SA) and SA-derivatives. Metabolites resulting from the activation of these enzymes are found in petiole exudates and may serve as priming signals for systemic disease resistance in Arabidopsis. Mutants lacking ALD1 are known to have reduced SA accumulation. To further investigate the role of ALD1 in relation to the SA-related module, immunity phenotypes of double mutants that disrupt ALD1 and ICS1/SID2 or SA perception by NPR1 were compared with each single mutant after infection by different Pseudomonas strains. Exudates collected from these mutants after infection were also evaluated for their ability to confer disease resistance when applied to wild-type plants. During infection with virulent or attenuated strains, the loss of ALD1 does not increase the susceptibility of npr1 or sid2 mutants, suggesting the main role of ALD1 in this context is in amplifying the SA-related module. In contrast, after an infection that leads to strong pathogen recognition via the cytoplasmic immune receptor RPS2, ALD1 acts additively with both NPR1 and ICS1/SID2 to suppress pathogen growth. The additive effects are observed in early basal defense responses as well as SA-related events. Thus, there are specific conditions that dictate whether the modules independently contribute to immunity to provide additive protection during infection. In the exudate experiments, intact NPR1 and ICS1/SID2, but not ALD1 in the donor plants were needed for conferring immunity. Mixing exudates showed that loss of SID2 yields exudates that suppress active exudates from wild-type or ald1 plants. This indicates that ICS1/SID2 may not only lead to positive defense signals, but also prevent a suppressive signal(s).