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DNA hypomethylation confers enhanced immunity against parasitic nematodes in plants

ABSTRACT: Background: Epigenetic processes play an important role in the plant response to adverse environmental conditions. A role for DNA hypomethylation has recently been suggested in the pathogenic interaction between bacteria and plants, yet it remains unclear whether this phenomenon reflects a conserved and general plant immunity response. We therefore investigated the role of DNA methylation in the plant defence against damaging parasitic nematodes. Methods and results: Treatment of roots of rice (monocot plant) and tomato (dicot plant) by a nematode-associated molecular pattern (NAMP) from different parasitic nematodes revealed global DNA hypomethylation using ELISA based quantification, suggesting conservation among plants. Focusing on root-knot induced gall tissue in rice, the causal impact of hypomethylation on immunity was revealed by a significantly reduced plant susceptibility upon 5-Azacitidine treatment. Whole genome bisulfite sequencing revealed that hypomethylation was massively present in the CHH context, while absent for CpG or CHG nucleotide contexts. 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 showed a delayed effect on transcriptional gene activation. Finally, the relevance of CHH hypomethylation in plant defence was confirmed in rice mutants of the RNA-directed DNA methylation pathway (RdDM) and DDM1, which are known to be steering DNA methylation in CHH context. Conclusions: We demonstrated that DNA hypomethylation confers enhanced defence in rice towards root-parasitic nematodes and is likely to be part of the basal NAMP-triggered immunity response in plants.

ORGANISM(S): Oryza sativa

PROVIDER: GSE130064 | GEO | 2020/07/07

REPOSITORIES: GEO

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Project description:Biotrophic plant pathogens have evolved sophisticated strategies to manipulate their host. They derive all of their nutrients from living plant tissues, by making intimate contact with their host while avoiding a resistance response. Rice is one of the most important crop plants worldwide and an excellent model system for studying monocotyledonous plants. Estimates of annual yield losses due to plant-parasitic nematodes on this crop range from 10 to 25% worldwide. One of the agronomically most important nematodes attacking rice is the rice root knot nematode Meloidogyne graminicola. Attack of plant roots by sedentary plant parasitic nematodes, like the root knot nematodes (RKN; Meloidogyne spp.) involves the development of specialized feeding cells in the vascular tissue. The second stage juvenile of the RKN punctures selected vascular cells with its stylet, injects pharyngeal secretions, and this ultimately leads to the reorganisation of these cells into typical feeding structures called giant cells (GCs), from which the nematode feeds for the remainder of its sedentary life cycle (Gheysen & Mitchum, 2011). Morphological and physiological reprogramming of the initial feeding cell leads to nucleus enlargement, proliferation of mitochondria and plastids, metabolic activation, cell cycle alterations and cell wall changes (Gheysen and Mitchum, 2011). The hyperplasia and hypertrophy of the surrounding cells leads to the formation of a root gall, which is typically formed at the root tips in the case of the rice RKN M. graminicola. In comparison with other RKN, M. graminicola has a very fast life cycle, with swelling of the root tips observed as early as 1 day after infection (dai). At 3 dai, terminal hook-like galls are clearly visible (Bridge et al., 2005). After 3 moults the nematodes are mature, around 10 dai. The M. graminicola females lay their eggs inside the galls, while most other RKN deposit egg masses at the gall surface, and hatched juveniles can reinfect the same or adjacent roots. In well-drained soil at 22-29ºC the life cycle of M. graminicola is completed in 19 days.

Project description:Biotrophic plant pathogens have evolved sophisticated strategies to manipulate their host. They derive all of their nutrients from living plant tissues, by making intimate contact with their host while avoiding a resistance response. Rice is one of the most important crop plants worldwide and an excellent model system for studying monocotyledonous plants. Estimates of annual yield losses due to plant-parasitic nematodes on this crop range from 10 to 25% worldwide. One of the agronomically most important nematodes attacking rice is the rice root knot nematode Meloidogyne graminicola. Attack of plant roots by sedentary plant parasitic nematodes, like the root knot nematodes (RKN; Meloidogyne spp.) involves the development of specialized feeding cells in the vascular tissue. The second stage juvenile of the RKN punctures selected vascular cells with its stylet, injects pharyngeal secretions, and this ultimately leads to the reorganisation of these cells into typical feeding structures called giant cells (GCs), from which the nematode feeds for the remainder of its sedentary life cycle (Gheysen & Mitchum, 2011). Morphological and physiological reprogramming of the initial feeding cell leads to nucleus enlargement, proliferation of mitochondria and plastids, metabolic activation, cell cycle alterations and cell wall changes (Gheysen and Mitchum, 2011). The hyperplasia and hypertrophy of the surrounding cells leads to the formation of a root gall, which is typically formed at the root tips in the case of the rice RKN M. graminicola. In comparison with other RKN, M. graminicola has a very fast life cycle, with swelling of the root tips observed as early as 1 day after infection (dai). At 3 dai, terminal hook-like galls are clearly visible (Bridge et al., 2005). After 3 moults the nematodes are mature, around 10 dai. The M. graminicola females lay their eggs inside the galls, while most other RKN deposit egg masses at the gall surface, and hatched juveniles can reinfect the same or adjacent roots. In well-drained soil at 22-29 degrees C the life cycle of M. graminicola is completed in 19 days. 2 biological replicates of nematode infected giant cells and control vascular cells were sampled at two time points: 7 and 14 dai

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DNA hypomethylation confers enhanced immunity against parasitic nematodes in plants

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