Controlled hydroxylations of diterpenoids allow for plant chemical defense without autotoxicity

Li J, Halitschke R, Li D, Paetz C, Su H, Heiling S, Xu S, Baldwin IT

Abstract

Plants make a variety of molecules that serve to protect them against hungry insects. Li et al. analyzed the balance between plants defending themselves and plants poisoning themselves. In wild tobacco (Nicotiana attenuata), two cytochrome P450 enzymes work within the biosynthetic pathway of 17-hydroxygeranyllinalool diterpene glycosides to help prevent the accumulation of toxic diterpene derivatives. Those same diterpene derivatives are formed in an insect herbivore after ingestion and cause toxicity by inhibiting sphingolipid biosynthesis in both plant and insect.Science, this issue p. 255Many 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 Nicotiana attenuata 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.