Controlled hydroxylations of diterpenoids allow for plant chemical defense without autotoxicity

• Published in: Science (American Association for the Advancement of Science) Vol. 371; no. 6526; pp. 255 - 260
• Main Authors: Li, Jiancai, Halitschke, Rayko, Li, Dapeng, Paetz, Christian, Su, Haichao, Heiling, Sven, Xu, Shuqing, Baldwin, Ian T
• Format: Journal Article
• Language: English
• Published: United States The American Association for the Advancement of Science 15.01.2021
• Subjects: Animals; Biosynthesis; Chemical defense; Cytochrome; Cytochrome P-450 Enzyme System - genetics; Cytochrome P-450 Enzyme System - metabolism; Cytochrome P450; Cytochromes P450; Derivatives; Diterpenes; Diterpenes - metabolism; Glucosides - biosynthesis; Glycosides; Hazardous wastes; Herbivores; Herbivory; Hydroxylation; Ingestion; Insects; Landfills; Lipids; Manduca - enzymology; Manduca - physiology; Metabolites; Molecular modelling; Nicotiana - enzymology; Nicotiana - metabolism; Nicotiana attenuata; Oxidoreductases - antagonists & inhibitors; Oxidoreductases - metabolism; Sphingolipids - biosynthesis; Tobacco; Toxic wastes; Toxicity
• ISSN: 0036-8075; 1095-9203
• DOI: 10.1126/science.abe4713

Many plant specialized metabolites function in herbivore defense, and abrogating particular steps in their biosynthetic pathways frequently causes autotoxicity. However, the molecular mechanisms underlying their defense and autotoxicity remain unclear. Here, we show that silencing two cytochrome P450s involved in diterpene biosynthesis in the wild tobacco causes severe autotoxicity symptoms that result from the inhibition of sphingolipid biosynthesis by noncontrolled hydroxylated diterpene derivatives. Moreover, the diterpenes' defensive function is achieved by inhibiting herbivore sphingolipid biosynthesis through postingestive backbone hydroxylation products. Thus, by regulating metabolic modifications, tobacco plants avoid autotoxicity and gain herbivore defense. The postdigestive duet that occurs between plants and their insect herbivores can reflect the plant's solutions to the "toxic waste dump" problem of using potent chemical defenses.