Transcriptome and Metabolome Profiling Reveal the Resistance Mechanisms of Rice against Brown Planthopper

Brown planthopper (Nilaparvata lugens Stål, BPH) is one of the most destructive insects affecting rice production. To better understand the physiological mechanisms of how rice responds to BPH feeding, we analyzed BPH-induced transcriptomic and metabolic changes in leaf sheaths of both BPH-susceptible and -resistant rice varieties. Our results demonstrated that the resistant rice reduced the settling, feeding and growth of BPH. Metabolic analyses indicated that BPH infestation caused more drastic overall metabolic changes in the susceptible variety than the resistant rice. Differently accumulated metabolites (DAMs) belonging to flavonoids were downregulated in the susceptible rice but upregulated in resistant variety. Transcriptomic analyses revealed more differentially expressed genes (DEGs) in susceptible rice than resistant rice, and DEGs related to stimulus were significantly upregulated in resistant rice but downregulated in susceptible rice. Combined analyses of transcriptome and metabolome showed that many DEGs and DAMs were enriched in phenylpropane biosynthesis, flavonoid biosynthesis, and plant hormone signal transduction. We conducted correlation analyses of DEGs and DAMs in these pathways and found a high correlation between DEGs and DAMs. Then, we found that the contents of endogenous indole 3-acetic acid (IAA) in resistant rice was lower than that of susceptible rice after BPH feeding, while the salicylic acid (SA) content was the opposite. For functional analysis, an exogenous application of IAA decreased rice resistance to BPH, but the exogenous application of SA increased resistance. In addition, biochemical assessment and quantitative PCR analysis showed that the lignin content of resistant accession was constitutively higher than in susceptible accession. By adding epigallocatechin, the substrate of anthocyanidin reductase (ANR), to the artificial diet decreased the performance of BPH. We first combined a transcriptome-metabolome-wide association study (TMWAS) on rice resistance to BPH in this study. We demonstrated that rice promoted resistance to BPH by inducing epigallocatechin and decreasing IAA. These findings provided useful transcriptomic and metabolic information for understanding the rice-BPH interactions.