Metabolic and transcriptomic changes induced in host during hypersensitive response mediated resistance in rice against the Asian rice gall midge

BACKGROUND: An incompatible interaction between rice (Oryza sativa) and the Asian rice gall midge (AGM, Orseolia oryzae Wood-Mason), that is usually manifested through a hypersensitive response (HR), represents an intricate relationship between the resistant host and its avirulent pest. We investigated changes in the transcriptome and metabolome of the host (indica rice variety: RP2068-18-3-5, RP), showing HR when attacked by an avirulent gall midge biotype (GMB1), to deduce molecular and biochemical bases of such a complex interaction. Till now, such an integrated analysis of host transcriptome and metabolome has not been reported for any rice-insect interaction. RESULTS: Transcript and metabolic profiling data revealed more than 7000 differentially expressed genes and 80 differentially accumulated metabolites, respectively, in the resistant host. Microarray data revealed deregulation of carbon (C) and nitrogen (N) metabolism causing a C/N shift; up-regulation of tetrapyrrole synthesis and down-regulation of chlorophyll synthesis and photosynthesis. Integrated results revealed that genes involved in lipid peroxidation (LPO) were up-regulated and a marker metabolite for LPO (azelaic acid) accumulated during HR. This coincided with a greater accumulation of GABA (neurotransmitter and an insect antifeedant) at the feeding site. Validation of microarray results by semi-quantitative RT-PCR revealed temporal variation in gene expression profiles. CONCLUSIONS: The study revealed extensive reprogramming of the transcriptome and metabolome of RP upon GMB1 infestation leading to an HR that was induced by the generation and release of reactive oxygen species i.e. singlet oxygen and resulted in LPO-mediated cell death. RP thus used HR as a means to limit nutrient supply to the feeding maggots and simultaneously accumulated GABA, strategies that could have led to maggot mortality. The integrated results of transcript and metabolic profiling, for the first time, provided insights into an HR+ type of resistance in rice against gall midge. ELECTRONIC SUPPLEMENTARY MATERIAL: The online version of this article (doi:10.1186/s12284-016-0077-6) contains supplementary material, which is available to authorized users.