Ready for battle: histone modifications shape rice intergenerational memory to protect against nematode attack

Intergenerational acquired resistance (IAR) occurs when offspring inherit enhanced defenses or tolerance to stresses that have been encountered by the parent plants. This study confirms that infection of rice by the root-knot nematode Meloidogyne graminicola leads to IAR in the offspring. Genome-wide and targeted gene expression analyses demonstrated that offspring of nematode-infected plants are better prepared to fight against such attack through 'spring loading' of hormone-related plant defense genes. These genes are suppressed under basal conditions in IAR plants but show a more dramatic induction upon nematode attack. ChIP-sequencing of the offspring of IAR versus naive plants indicated that histone modifications are involved in the spring-loaded expression pattern. We detected, enrichment of H3K4me3 on defense-related genes and H3K27me3 on development-related genes in the roots of IAR plants. Detailed bioinformatic analyses indicated significant epigenetic changes to the abscisic acid, ethylene, and Mitogen Activated Protein Kinase (MAPK) signalling pathways in the offspring of nematode-infected plants. A rice line with reduced activity of MPK5 was found to be deficient in defense spring loading and lacked the IAR phenotype. Our results demonstrate that histone modifications act as carriers of stress memory for infection by root-knot nematodes in rice and identify MPK5 as one of the drivers for inherited resistance.