Ascorbate oxidation activates systemic defence against root-knot nematode Meloidogyne graminicola in rice

Abstract

Abstract Ascorbic acid (AA) is the major antioxidant buffer produced in the shoot tissue of plants. Previous studies on root-knot nematode (RKN; Meloidogyne graminicola)-infected rice (Oryza sativa) plants showed differential expression of AA-recycling genes, although their functional role was unknown. Our results confirmed increased dehydroascorbate (DHA) levels in nematode-induced root galls, while AA mutants were significantly more susceptible to nematode infection. External applications of ascorbate oxidase (AO), DHA, or reduced AA, revealed systemic effects of ascorbate oxidation on rice defence versus RKN, associated with a primed accumulation of H2O2 upon nematode infection. To confirm and further investigate these systemic effects, a transcriptome analysis was done on roots of foliar AO-treated plants, revealing activation of the ethylene (ET) response and jasmonic acid (JA) biosynthesis pathways in roots, which was confirmed by hormone measurements. Activation of these pathways by methyl-JA, or ethephon treatment can complement the susceptibility phenotype of the rice Vitamin C (vtc1) mutant. Experiments on the jasmonate signalling (jar1) mutant or using chemical JA/ET inhibitors confirm that the effects of ascorbate oxidation are dependent on both the JA and ET pathways. Collectively, our data reveal a novel pathway in which ascorbate oxidation induces systemic defence against RKNs.