Genome‐wide DNA hypomethylation shapes nematode pattern‐triggered immunity in plants

Abstract

Summary A role for DNA hypomethylation has recently been suggested in the interaction between bacteria and plants; it is unclear whether this phenomenon reflects a conserved response. Treatment of plants of monocot rice and dicot tomato with nematode‐associated molecular patterns from different nematode species or bacterial pathogen‐associated molecular pattern flg22 revealed global DNA hypomethylation. A similar hypomethylation response was observed during early gall induction by Meloidogyne graminicola in rice. Evidence for the causal impact of hypomethylation on immunity was revealed by a significantly reduced plant susceptibility upon treatment with DNA methylation inhibitor 5‐azacytidine. Whole‐genome bisulphite sequencing of young galls revealed massive hypomethylation in the CHH context, while not for CG or CHG nucleotide contexts. Further, CHH hypomethylated regions were predominantly associated with gene promoter regions, which was not correlated with activated gene expression at the same time point but, rather, was correlated with a delayed transcriptional gene activation. Finally, the relevance of CHH hypomethylation in plant defence was confirmed in rice mutants of the RNA‐directed DNA methylation pathway and DECREASED DNA METHYLATION 1. We demonstrated that DNA hypomethylation is associated with reduced susceptibility in rice towards root‐parasitic nematodes and is likely to be part of the basal pattern‐triggered immunity response in plants.

Epigenetic and Metabolic Changes in Root-Knot Nematode-Plant Interactions

“…Epigenetic changes were shown to regulate the expression of genes involved in plant resistance response [ 20 ]. DNA methylation, besides many other biological processes, is involved in mechanisms underlying plant response to pathogen and nematode attacks [ 20 , 23 ]. Methylation on promoter regions negatively correlates with gene expression levels [ 31 ], whereas DNA hypo-methylation has been associated with plant defense against nematodes [ 23 ].…”

“…DNA methylation, besides many other biological processes, is involved in mechanisms underlying plant response to pathogen and nematode attacks [ 20 , 23 ]. Methylation on promoter regions negatively correlates with gene expression levels [ 31 ], whereas DNA hypo-methylation has been associated with plant defense against nematodes [ 23 ]. Hypo-methylation of resistance genes enhances their expression to rapidly respond to environmental factors [ 20 ].…”

“…These data show that total DNA hypo-methylation is associated with enhanced defense gene expression in immune response, triggered by R-genes (ETI) against RKNs. Comparably, DNA hypo-methylation has already been reported to be part of a conserved PTI response to nematodes in monocot and dicot plants [ 23 ]. In contrast, gene silencing, induced by nematodes in host plants, might result from the hyper-methylation of total DNA observed in the present study in successfully infected susceptible plants.…”

“…De novo methylation is catalyzed by domains rearranged methyl-transferases (DRM), whilst maintenance is performed by three classes of enzymes: the most predominant CG methylation by methyl-transferase 1 (Met1) , CHG methylation by chromo-methyl-transferases (CMT2 and CMT3), and CHH methylation by DRM2 or CMT2. The RNA-directed DNA methylation (RdDM) pathway promotes the sequence targeting by DRMs, through the synthesis of small-RNA (smRNA) [ 20 ].The activation of different types of epigenetic mechanisms upon nematode infection has extensively been reported [ 23 ]. Gene silencing, produced in successful development of nematodes on susceptible plants through the manipulation of phyto-hormone pathways, has been ascribed to the activation of smRNA and miRNA pathways [ 16 , 24 ].…”

Epigenetic and Metabolic Mechanisms in Plant Resistance to Root-Knot Nematodes

“…The activation of different types of epigenetic mechanisms upon nematode infection has extensively been reported [23]. Gene silencing, produced in successful development of nematodes on susceptible plants through the manipulation of phyto-hormone pathways, has been ascribed to the activation of smRNAs and miRNAs pathways [16,24].…”