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Our previous study concerning the pathogen-induced biphasic pattern of nitric oxide (NO) burst revealed that the decline phase and a low level of NO, due to S-nitrosoglutathione reductase (GSNOR) activity, might be decisive in the upregulation of stress-sensitive genes via histone H3/H4 methylation in potato leaves inoculated with avr P. infestans. The present study refers to the NO-related impact on genes regulating DNA (de)methylation, being in dialog with histone methylation. The excessive amounts of NO after the pathogen or GSNO treatment forced the transient upregulation of histone SUVH4 methylation and DNA hypermethylation. Then the diminished NO bioavailability reduced the SUVH4-mediated suppressive H3K9me2 mark on the R3a gene promoter and enhanced its transcription. However, we found that the R3a gene is likely to be controlled by the RdDM methylation pathway. The data revealed the time-dependent downregulation of the DCL3, AGO4, and miR482e genes, exerting upregulation of the targeted R3a gene correlated with ROS1 overexpression. Based on these results, we postulate that the biphasic waves of NO burst in response to the pathogen appear crucial in establishing potato resistance to late blight through the RdDM pathway controlling R gene expression.

We provide evidence that alterations in DNA methylation patterns contribute to the regulation of stress-responsive gene expression for an intergenerational resistance of β-aminobutyric acid (BABA)-primed potato to Phytophthora infestans. Plants exposed to BABA rapidly modified their methylation capacity toward genome-wide DNA hypermethylation. De novo induced DNA methylation (5-mC) correlated with the up-regulation of Chromomethylase 3 (CMT3), Domains rearranged methyltransferase 2 (DRM2), and Repressor of silencing 1 (ROS1) genes in potato. BABA transiently activated DNA hypermethylation in the promoter region of the R3a resistance gene triggering its downregulation in the absence of the oomycete pathogen. However, in the successive stages of priming, an excessive DNA methylation state changed into demethylation with the active involvement of potato DNA glycosylases. Interestingly, the 5-mC–mediated changes were transmitted into the next generation in the form of intergenerational stress memory. Descendants of the primed potato, which derived from tubers or seeds carrying the less methylated R3a promoter, showed a higher transcription of R3a that associated with an augmented intergenerational resistance to virulent P. infestans when compared to the inoculated progeny of unprimed plants. Furthermore, our study revealed that enhanced transcription of some SA-dependent genes (NPR1, StWRKY1, and PR1) was not directly linked with DNA methylation changes in the promoter region of these genes, but was a consequence of methylation-dependent alterations in the transcriptional network.