The products of a single maize sesquiterpene synthase form a volatile defense signal that attracts natural enemies of maize herbivores

Abstract

Plants can defend themselves against herbivores by attracting natural enemies of the herbivores. The cues for attraction are often complex mixtures of herbivore-induced plant volatiles, making it difficult to demonstrate the role of specific compounds. After herbivory by lepidopteran larvae, maize releases a mixture of volatiles that is highly attractive to females of various parasitic wasp species. We identified the terpene synthase TPS10 that forms (E)-␤-farnesene, (E)-␣-bergamotene, and other herbivory-induced sesquiterpene hydrocarbons from the substrate farnesyl diphosphate. The corresponding gene is expressed in response to herbivore attack and is regulated at the transcript level. Overexpression of tps10 in Arabidopsis thaliana resulted in plants emitting high quantities of TPS10 sesquiterpene products identical to those released by maize. Using these transgenic Arabidopsis plants as odor sources in olfactometer assays showed that females of the parasitoid Cotesia marginiventris learn to exploit the TPS10 sesquiterpenes to locate their lepidopteran hosts after prior exposure to these volatiles in association with hosts. This dissection of the herbivore-induced volatile blend demonstrates that a single gene such as tps10 can be sufficient to mediate the indirect defense of maize against herbivore attack.parasitoid attraction ͉ plant defense signal ͉ terpene biosynthesis ͉ volatile terpenes I n the last two decades, researchers have frequently observed that herbivore damage to certain plants induces the emission of volatile organic compounds that attract natural enemies of the herbivores. Termed ''indirect defense,'' this phenomenon has been reported in Ͼ15 different plant species to date (1-4). For example, after damage by lepidopteran larvae to maize foliage, the plant releases a complex mixture of volatiles containing a large number of mono-and sesquiterpenes, lipoxygenase pathway products, and indole (5), with the mixture varying among cultivars and between maize and related species of the Poaceae (6, 7). The high number of compounds that make up this and other herbivore-induced volatile mixtures has so far impeded the identification of the compound(s) actually responsible for signaling herbivore enemies. Attempts to dissect the volatile signal emitted by herbivore-damaged leaves of lima bean (1) and maize (8), for instance, could not identify a specific compound responsible for enemy attraction, suggesting that mixtures constitute the active signal. However, the application of individual plant volatiles, such as methyl salicylate and the sesquiterpene alcohol nerolidol, in behavioral assays have been occasionally reported to attract parasitoids (9) and predatory mites (10-12).The volatile signal emitted by maize seedlings after attack by lepidopteran larvae attracts females of the parasitic braconid wasp Cotesia marginiventris (Hymenoptera), which oviposit in the larvae (5). To determine the role of specific volatiles in attracting C. marginiventris, we sought to learn more about the regulation of vola...

Volatile terpenoids: multiple functions, biosynthesis, modulation and manipulation by genetic engineering

“…This may include releasing a blend of specific floral volatile scents that attract predators of herbivores after being attacked (Kessler 2010;Peñuelas et al 2014)). In the model plant Arabidopsis, females of parasitoids Cotesia marginiventris use TPS10 (a sesquiterpene) to track their lepidopteran host by utilizing the floral scent (Schnee et al 2006). Arabidopsis has been shown to emit two terpenoids, (3,S)-(E)-nerolidol and its derivative (E)-4,8-dimethyl-1,3,7-nonatriene, when the strawberry nerolidol synthase gene was introduced into the plants, resulting in greater attraction of the predators of predatory mites (Kappers et al 2005).…”

“…The repellent/attraction properties of various terpenoid volatiles in petunia flower were observed via silencing the biosynthetic genes individually responsible for the production of scent compounds (Kessler et al 2013). Another example of floral scent engineering is the introduction of a maize sesquiterpene synthase gene (TPS10) into Arabidopsis, leading to the production of a significant amount of various sesquiterpenes that are exploited by the female parasitoid wasp C. marginiventris to navigate to their potential lepidopteran host (Schnee et al 2006;Delory et al 2016). Manipulation of genetic engineering for sesquiterpenes production seems a challenging task and is less successful compared with that for monoterpenes due to lack of suitable precursors.…”

Indirect Defense Responses to Herbivory in Grasses

“…The amount and composition of the volatile signal emitted by the plant is dependent on the type of herbivore cue. In maize, mechanical wounding of the leaves or infestation with aphids only induces a moderate response, whereas damage by larvae of the lepidopteran Spodoptera littoralis results in a far greater release Schnee et al, 2006). In maize, this increase in volatile production is due to larval elicitors like volicitin [N-(17-hydroxylinolenoyl)- L-Gln] that are formed in the larval gut and introduced into the leaf during larval feeding (Alborn et al, 1997;Spiteller et al, 2000;Tumlinson and Lait, 2005).…”

“…The terpene blends of maize are formed by at least six sesquiterpene synthases (Kö llner et al, 2004). Three of these enzymes, TPS1, TPS10, and TPS23, are strongly induced by herbivore damage and produce the major sesquiterpene components of herbivore-induced volatiles (Schnee et al, 2002(Schnee et al, , 2006Köllner et al, 2008a). These terpene synthases can also be induced by jasmonic acid treatment of the plant (T.G.…”

Exploiting scents of distress: the prospect of manipulating herbivore-induced plant odours to enhance the control of agricultural pests

“…In the first study [42 ], a linalool/nerolidol synthase gene from strawberry (FaNES1) was introduced into Arabidopsis thaliana, causing the transformed plants to constitutively release (3S)-(E)-nerolidol (and in some transformants (3E)-4,8-dimethyl-1,3,7-nonatriene), which rendered them attractive to predatory mites. In the other study [43 ], Arabidopsis was transformed with a maize terpene synthase gene (TPS10) that is responsible for emissions of the blend of sesquiterpenes that is typically released in response to caterpillar feeding. The transformed plant was attractive to parasitoid females that use induced maize volatiles to find their caterpillar hosts, but only after the wasps had learned to associate the sesquiterpene blend with the presence of hosts.…”