The Role of Indole and Other Shikimic Acid Derived Maize Volatiles in the Attraction of Two Parasitic Wasps

Abstract

After herbivore attack, plants release a plethora of different volatile organic compounds (VOCs), which results in odor blends that are attractive to predators and parasitoids of these herbivores. VOCs in the odor blends emitted by maize plants (Zea mays) infested by lepidopteran larvae are well characterized. They are derived from at least three different biochemical pathways, but the relative importance of each pathway for the production of VOCs that attract parasitic wasps is unknown. Here, we studied the importance of shikimic acid derived VOCs for the attraction of females of the parasitoids Cotesia marginiventris and Microplitis rufiventris. By incubating caterpillar-infested maize plants in glyphosate, an inhibitor of the 5-enolpyruvylshikimate-3-phospate (EPSP) synthase, we obtained induced odor blends with only minute amounts of shikimic acid derived VOCs. In olfactometer bioassays, the inhibited plants were as attractive to naive C. marginiventris females as control plants that released normal amounts of shikimic acid derived VOCs, whereas naive M. rufiventris females preferred inhibited plants to control plants. By adding back synthetic indole, the quantitatively most important shikimic acid derived VOC in induced maize odors, to inhibited plants, we showed that indole had no effect on the attraction of C. marginiventris and that M. rufiventris preferred blends without synthetic indole. Exposing C. marginiventris females either to odor blends of inhibited or control plants during oviposition experiences shifted their preference in subsequent olfactometer tests in favor of the experienced odor. Further learning experiments with synthetic indole showed that C. marginiventris can learn to respond to this compound, but that this does not affect its choices between natural induced blends with or without indole. We hypothesize that for naïve wasps the attractiveness of an herbivore-induced odor blend is reduced due to masking by nonattractive compounds, and that during oviposition experiences in the presence of complex odor blends, parasitoids strongly associate some compounds, whereas others are largely ignored.

A Maize (E)-β-Caryophyllene Synthase Implicated in Indirect Defense Responses against Herbivores Is Not Expressed in Most American Maize Varieties

“…This effect of associative learning was reflected in a significant treatment effect (F1.166 ¼ 34.04; P < 0.0001) and a significant treatment-experience interaction (F1.164 ¼ 13.49; P < 0.001). These results confirm that (E)-b-caryophyllene by itself is a key attractant for the nematodes, whereas above ground this bicyclic sesquiterpene olefin is a component of a blend of leaf volatiles produced after herbivore damage that can be perceived and learned as a host location cue by herbivore parasitoids, as has been found for several other volatiles within this blend (D'Alessandro et al, 2006;Schnee et al, 2006).…”

Differential Performance and Parasitism of Caterpillars on Maize Inbred Lines with Distinctly Different Herbivore-Induced Volatile Emissions

“…Green leaf volatiles or further compounds that are instantaneously released upon damage are important attractants of inexperienced C. marginiventris [51]. Some common volatiles derived from shikimic acid, notably indole, appear not to be involved in the attraction of naïve C. marginiventris to host infested maize plants [52]. The sesquiterpenes, which make up a major part of the volatile blend both in number and quantity, apparently are also not essential for the initial attraction of C. marginiventris [49].…”

Inhibition of lipoxygenase affects induction of both direct and indirect plant defences against herbivorous insects

“…This approach provides insight into the sensitivity of insects to plant metabolomic changes resulting from induction of the octadecanoid pathway. Recently, two inhibitors (glyphosate and fosmidomycin) of other pathways (the shikimic acid and the methylerythritol 4-phosphate pathways, respectively) were shown to be suitable tools with which to study induced indirect plant defences (Bruinsma and Dicke 2008; D’Alessandro et al 2006; D’Alessandro and Turlings 2006; Mumm et al 2008). …”