Abstract

Glandular trichomes are epidermal structures that provide a first line of chemical defense against arthropod herbivores and other biotic threats. The most conspicuous structure on leaves of cultivated tomato (Solanum lycopersicum) is the type-VI glandular trichome (tVI-GT), which accumulates both flavonoids and volatile terpenoids. Although these classes of specialized metabolites are derived from distinct metabolic pathways, previous studies with a chalcone isomerase 1 (CHI1)-deficient mutant called anthocyanin free (af) showed that flavonoids are required for terpenoid accumulation in tVI-GTs. Here, we combined global transcriptomic and proteomic analyses of isolated trichomes as a starting point to show that the lack of CHI1 is associated with reduced levels of terpenoid biosynthetic transcripts and enzymes. The flavonoid deficiency in af trichomes also resulted in the upregulation of abiotic stress-responsive genes associated with DNA damage and repair. Several lines of biochemical and genetic evidence indicate that the terpenoid defect in af mutants is specific for the tVI-GT and is associated with the absence of bulk flavonoids rather than loss of CHI1 per se. A newly developed genome-scale model of metabolism in tomato tVI-GTs helped identify metabolic imbalances caused by the loss of flavonoid production. We provide evidence that flavonoid deficiency in this cell type leads to increased production of reactive oxygen species (ROS), which may impair terpenoid biosynthesis. Collectively, our findings support a role for flavonoids as ROS-scavenging antioxidants in glandular trichomes.

中文翻译：

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类黄酮缺乏会破坏番茄腺毛中的氧化还原稳态和萜类生物合成

摘要

腺毛是表皮结构，为节肢动物食草动物和其他生物威胁提供第一道化学防御。栽培番茄 ( Solanum lycopersicum )叶子上最显着的结构是 VI 型腺毛 (tVI-GT)，它积累了类黄酮和挥发性萜类化合物。尽管这些类别的特殊代谢物来自不同的代谢途径，但之前对查尔酮异构酶 1 (CHI1) 缺陷突变体的研究称为无花青素( af) 表明黄酮类化合物是 tVI-GT 中萜类化合物积累所必需的。在这里，我们将孤立毛状体的全球转录组学和蛋白质组学分析结合起来，以表明 CHI1 的缺乏与萜类生物合成转录物和酶的水平降低有关。毛状体中的类黄酮缺乏也导致与 DNA 损伤和修复相关的非生物应激反应基因的上调。几条生化和遗传证据表明，af突变体中的萜类化合物缺陷对 tVI-GT 具有特异性，并且与大量类黄酮的缺乏有关，而不是与 CHI1本身的损失有关. 一种新开发的番茄 tVI-GT 代谢基因组规模模型有助于确定由类黄酮产生损失引起的代谢失衡。我们提供的证据表明，这种细胞类型中的类黄酮缺乏会导致活性氧 (ROS) 的产生增加，这可能会损害萜类化合物的生物合成。总的来说，我们的研究结果支持黄酮类化合物作为腺毛中 ROS 清除抗氧化剂的作用。