Lilies (genus: Lilium) play a significant role in the global cut-flower industry, but they are highly susceptible to Fusarium wilt caused by Fusarium oxysporum. However, Lilium regale, a wild lily species, exhibits remarkable resistance to F. oxysporum. To investigate the quantitative resistance of L. regale to Fusarium wilt, a comprehensive multi-omics analysis was conducted. Upon inoculation with F. oxysporum, L. regale roots showed a significant accumulation of phenylpropane metabolites, including lignin precursors, flavonoids, and hydroxycinnamic acids. These findings were consistent with the up-regulated expression of phenylpropanoid biosynthesis-related genes encoding various enzymes, as revealed by transcriptomics and proteomics analyses. Furthermore, metabolomics and proteomics data demonstrated differential activation of monoterpenoid and isoquinoline alkaloid biosynthesis. Colorimetry and high-performance liquid chromatography analyses revealed significantly higher levels of total flavonoids, lignin, ferulic acid, phlorizin, and quercetin contents in L. regale scales compared to susceptible lily ‘Siberia’ scales during F. oxysporum infection. These phenylpropanes exhibited inhibitory effects on F. oxysporum growth and suppressed the expression of pathogenicity-related genes. Transcriptional regulatory network analysis suggested that ethylene-responsive transcription factors (ERFs) may positively regulate phenylpropanoid biosynthesis. Therefore, LrERF4 was cloned and transiently overexpressed in the Fusarium wilt-susceptible Oriental hybrid lily, ‘Siberia’. The overexpression of LrERF4 resulted in increased levels of total flavonoids, lignin, ferulic acid, phlorizin, and quercetin, while the silencing of LrERF4 in L. regale through RNAi had opposite effect. In conclusion, phenylpropanoid metabolism plays a crucial role in the defense response of L. regale against Fusarium wilt, with LrERF4 acting as a positive regulator of phenylpropane biosynthesis.

中文翻译：

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综合多组学研究揭示了苯丙素代谢在百合对镰刀菌枯萎病的防御反应中的重要性


百合（属：百合）在全球切花产业中发挥着重要作用，但它们极易受到尖孢镰刀菌引起的枯萎病的影响。然而，野生百合品种 Lilium regale 对尖孢镰刀菌表现出显着的抗性。为了研究 L. regale 对枯萎病的定量抗性，进行了全面的多组学分析。接种尖孢镰刀菌后，富贵草根表现出苯丙烷代谢物的显着积累，包括木质素前体、类黄酮和羟基肉桂酸。这些发现与转录组学和蛋白质组学分析所揭示的编码各种酶的苯丙素生物合成相关基因的表达上调一致。此外，代谢组学和蛋白质组学数据证明了单萜和异喹啉生物碱生物合成的差异激活。比色法和高效液相色谱分析显示，在尖孢镰刀菌感染期间，与易感百合“西伯利亚”鳞片相比，百合鳞片中的总黄酮、木质素、阿魏酸、根皮苷和槲皮素含量显着更高。这些苯丙烷对尖孢镰刀菌的生长具有抑制作用，并抑制致病性相关基因的表达。转录调控网络分析表明乙烯响应转录因子（ERF）可能正向调节苯丙素生物合成。因此，LrERF4 被克隆并在枯萎病易感的东方杂交百合“西伯利亚”中短暂过表达。 LrERF4的过度表达导致总黄酮、木质素、阿魏酸、根皮苷和槲皮素水平升高，而通过RNAi沉默LrERF4则产生相反的效果。 总之，苯丙素代谢在 L. regale 对抗镰刀菌枯萎病的防御反应中发挥着至关重要的作用，其中 LrERF4 充当苯丙烷生物合成的正调节因子。