A herbivore-induced plant volatile interferes with host plant and mate location in moths through suppression of olfactory signalling pathways

Abstract

BackgroundPlants under herbivore attack release volatiles that attract natural enemies, and herbivores in turn avoid such plants. Whilst herbivore-induced plant volatile blends appeared to reduce the attractiveness of host plants to herbivores, the volatiles that are key in this process and particularly the way in which deterrence is coded in the olfactory system are largely unknown. Here we demonstrate that herbivore-induced cotton volatiles suppress orientation of the moth Spodoptera littoralis to host plants and mates.ResultsWe found that (E)-4,8-dimethyl-1,3,7-nonatriene (DMNT), an induced volatile, is key in herbivore deterrence: DMNT suppressed plant odour- and pheromone-induced behaviours. We then dissected the neurophysiological basis of this interaction. DMNT-responding glomeruli were also activated by other plant compounds, suggesting that S. littoralis possesses no segregated olfactory circuit dedicated exclusively to DMNT. Instead, DMNT suppressed responses to the main pheromone component, (Z)-9-(E)-11-tetradecenyl acetate, and primarily to (Z)-3-hexenyl acetate, a host plant attractant.ConclusionOur study shows that olfactory sensory inhibition, which has previously been reported without reference to an animal’s ecology, can be at the core of coding of ecologically relevant odours. As DMNT attracts natural enemies and deters herbivores, it may be useful in the development or enhancement of push-pull strategies for sustainable agriculture.Electronic supplementary materialThe online version of this article (doi:10.1186/s12915-015-0188-3) contains supplementary material, which is available to authorized users.

Survey of conspecific herbivore‐induced volatiles from apple as possible attractants for Pandemis pyrusana (Lepidoptera: Tortricidae)

“…Yet it remains unclear why male and female leafroller moths would be attracted to these binary blends of a benzenoid volatile and acetic acid. Previous studies with plant‐feeding Lepidoptera (primarily noctuids and pyralids) have correlated the presence of larval feeding on a host plant with the repulsion of the conspecific adults . However, this response has not always occurred in field studies .…”

Host Plant Species Differentiation in a Polyphagous Moth: Olfaction is Enough

“…(E)-DMNT inhibits male attraction towards the sex pheromone (Hatano et al 2015) and is part of a volatile blend that is responsible for the avoidance of herbivore-induced cotton plants by ovipositing females (Zakir et al 2013b). The investigation of its neural representation in the antennal lobe evidenced that (E)-DMNT inhibits overall antennal lobe activation by the sex pheromone and by an attractive synthetic blend mimicking host plant odor (Hatano et al 2015). Whether this pattern reflects the neural mechanism responsible for avoidance of unsuitable plants by S. littoralis can only be confirmed by replicating the experiment with other behavioural antagonists.…”

“…In contrast to the ecological aspects, studies on the olfactory basis of host plant perception and attraction in S. littoralis have, to date, mostly focused on a single model host plant: cotton Hatano et al 2015;Kromann et al 2015;Saveer et al 2012). Indeed, GC-EAD active plant volatiles have only been described for cotton plus two non-hosts with a negative impact on S. littoralis reproductive behaviour: a toxic plant and a gymnosperm (Binyameen et al 2013).…”

Pest Control Compounds Targeting Insect Chemoreceptors: Another Silent Spring?

“…Several recent studies have identified natural odorants that interfere with responses to sex pheromones, at the molecular, neurophysiological, and behavioral levels. For instance, (E)-4,8-dimethyl-1,3,7-nonatriene (DMNT), a herbivore-induced plant volatile, interferes with the detection of both sex pheromone and host-derived attractants in the Egyptian cotton leaf worm, Spodoptera littoralis (Lepidoptera), reducing attraction to both sex pheromones and host attractants (Hatano et al, 2015). Because DMNT also attracts natural enemies of herbivores it might be a good target for sustainable agricultural pest control.…”