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.

中文翻译：

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转录组和代谢组分析揭示水稻对褐飞虱的抗性机制。

褐飞虱（Nilaparvata lugens Stål，BPH）是影响水稻生产最具破坏性的昆虫之一。为了更好地了解水稻对褐飞虱取食反应的生理机制，我们分析了褐飞虱诱导的褐飞虱敏感和抗性水稻品种叶鞘的转录组和代谢变化。我们的结果表明，抗性水稻减少了褐飞虱的沉降、取食和生长。代谢分析表明，褐飞虱侵染导致易感品种比抗性水稻更剧烈的整体代谢变化。属于类黄酮的不同积累代谢物（DAM）在感病水稻中下调，但在抗性品种中上调。转录组分析显示，感病水稻中的差异表达基因（DEG）多于抗病水稻，并且与刺激相关的DEG在抗病水稻中显着上调，但在感病水稻中下调。转录组和代谢组的联合分析表明，许多DEG和DAM在苯丙烷生物合成、类黄酮生物合成和植物激素信号转导方面富集。我们对这些途径中的DEG和DAM进行了相关性分析，发现DEG和DAM之间存在高度相关性。然后我们发现，饲喂褐飞虱后，抗性水稻中内源吲哚3-乙酸（IAA）含量低于感病水稻，而水杨酸（SA）含量则相反。对于功能分析，外源施用 IAA 降低了水稻对 BPH 的抗性，但外源施用 SA 增加了抗性。此外，生化评估和定量PCR分析表明，抗性种质的木质素含量基本高于感病种质。通过在人工饲料中添加表没食子儿茶素（花青素还原酶 (ANR) 的底物）可降低 BPH 的表现。在这项研究中，我们首先结合了转录组-代谢组范围关联研究（TMWAS）来研究水稻对褐飞虱的抗性。我们证明水稻通过诱导表没食子儿茶素和减少 IAA 来促进对 BPH 的抗性。这些发现为理解水稻-褐飞虱相互作用提供了有用的转录组和代谢信息。