Epigenetics and Defence Group, Department of Biotechnology, Faculty of Bioscience Engineering, Ghent University, Ghent, Belgium.
Department of Plant Biotechnology and Bioinformatics, Ghent University, Ghent, Belgium.
Plant Cell Environ. 2021 Sep;44(9):3122-3139. doi: 10.1111/pce.14119. Epub 2021 Jun 16.
Although many phenylpropanoid pathway-derived molecules act as physical and chemical barriers to pests and pathogens, comparatively little is known about their role in regulating plant immunity. To explore this research field, we transiently perturbed the phenylpropanoid pathway through application of the CINNAMIC ACID-4-HYDROXYLASE (C4H) inhibitor piperonylic acid (PA). Using bioassays involving diverse pests and pathogens, we show that transient C4H inhibition triggers systemic, broad-spectrum resistance in higher plants without affecting growth. PA treatment enhances tomato (Solanum lycopersicum) resistance in field and laboratory conditions, thereby illustrating the potential of phenylpropanoid pathway perturbation in crop protection. At the molecular level, transcriptome and metabolome analyses reveal that transient C4H inhibition in tomato reprograms phenylpropanoid and flavonoid metabolism, systemically induces immune signalling and pathogenesis-related genes, and locally affects reactive oxygen species metabolism. Furthermore, C4H inhibition primes cell wall modification and phenolic compound accumulation in response to root-knot nematode infection. Although PA treatment induces local accumulation of the phytohormone salicylic acid, the PA resistance phenotype is preserved in tomato plants expressing the salicylic acid-degrading NahG construct. Together, our results demonstrate that transient phenylpropanoid pathway perturbation is a conserved inducer of plant resistance and thus highlight the crucial regulatory role of this pathway in plant immunity.
虽然许多苯丙素途径衍生的分子作为物理和化学屏障来抵御害虫和病原体，但关于它们在调节植物免疫中的作用，人们知之甚少。为了探索这一研究领域，我们通过应用肉桂酸-4-羟化酶（C4H）抑制剂胡椒基酸（PA）暂时干扰苯丙素途径。通过涉及多种害虫和病原体的生物测定，我们表明，瞬时 C4H 抑制会在不影响生长的情况下引发高等植物的系统、广谱抗性。PA 处理增强了番茄（Solanum lycopersicum）在田间和实验室条件下的抗性，从而说明了苯丙素途径干扰在作物保护中的潜力。在分子水平上，转录组和代谢组分析表明，番茄中瞬时 C4H 抑制重新编程了苯丙素和类黄酮代谢，系统地诱导了免疫信号和与发病相关的基因，并局部影响了活性氧代谢。此外，C4H 抑制在根结线虫感染时启动细胞壁修饰和酚类化合物的积累。尽管 PA 处理诱导了植物激素水杨酸的局部积累，但在表达水杨酸降解 NahG 构建体的番茄植物中，仍保留了对 PA 的抗性表型。总之，我们的研究结果表明，瞬时苯丙素途径干扰是植物抗性的一种保守诱导剂，因此突出了该途径在植物免疫中的关键调节作用。
