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

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          Abstract

          Background

          Plants 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.

          Results

          We 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.

          Conclusion

          Our 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 material

          The online version of this article (doi:10.1186/s12915-015-0188-3) contains supplementary material, which is available to authorized users.

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          Most cited references68

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          Defensive function of herbivore-induced plant volatile emissions in nature.

          Herbivore attack is known to increase the emission of volatiles, which attract predators to herbivore-damaged plants in the laboratory and agricultural systems. We quantified volatile emissions from Nicotiana attenuata plants growing in natural populations during attack by three species of leaf-feeding herbivores and mimicked the release of five commonly emitted volatiles individually. Three compounds (cis-3-hexen-1-ol, linalool, and cis-alpha-bergamotene) increased egg predation rates by a generalist predator; linalool and the complete blend decreased lepidopteran oviposition rates. As a consequence, a plant could reduce the number of herbivores by more than 90% by releasing volatiles. These results confirm that indirect defenses can operate in nature.
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            Insect host location: a volatile situation.

            Locating a host plant is crucial for a phytophagous (herbivorous) insect to fulfill its nutritional requirements and to find suitable oviposition sites. Insects can locate their hosts even though the host plants are often hidden among an array of other plants. Plant volatiles play an important role in this host-location process. The recognition of a host plant by these olfactory signals could occur by using either species-specific compounds or specific ratios of ubiquitous compounds. Currently, most studies favor the second scenario, with strong evidence that plant discrimination is due to central processing of olfactory signals by the insect, rather than their initial detection. Furthermore, paired or clustered olfactory receptor neurons might enable fine-scale spatio-temporal resolution of the complex signals encountered when ubiquitous compounds are used.
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              Caterpillar-induced nocturnal plant volatiles repel conspecific females.

              Plants respond to insect herbivory by synthesizing and releasing complex blends of volatile compounds, which provide important host-location cues for insects that are natural enemies of herbivores. The effects of these volatile blends on herbivore behaviour have been investigated to only a limited extent, in part because of the assumption that herbivore-induced volatile emissions occur mainly during the light phase of the photoperiod. Because many moths-whose larvae are some of the most important insect herbivores-are nocturnal, herbivore-induced plant volatiles have not hitherto been considered to be temporally available as host-location cues for ovipositing females. Here we present chemical and behavioural assays showing that tobacco plants (Nicotiana tabacum) release herbivore-induced volatiles during both night and day. Moreover, several volatile compounds are released exclusively at night and are highly repellent to female moths (Heliothis virescens). The demonstration that tobacco plants release temporally different volatile blends and that lepidopteran herbivores use induced plant signals released during the dark phase to choose sites for oviposition adds a new dimension to our understanding of the role of chemical cues in mediating tritrophic interactions.
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                Author and article information

                Contributors
                edhatano@gmail.com
                saveer.ahmed@vanderbilt.edu
                felipe.borrero@slu.se
                martin.strauch@lfb.rwth-aachen.de
                zakirali@ciitvehari.edu.pk
                marie.bengtsson@slu.se
                rickard.ignell@slu.se
                peter.anderson@slu.se
                paul.becher@slu.se
                peter.witzgall@slu.se
                teun.dekker@slu.se
                Journal
                BMC Biol
                BMC Biol
                BMC Biology
                BioMed Central (London )
                1741-7007
                16 September 2015
                16 September 2015
                2015
                : 13
                : 75
                Affiliations
                [ ]Department of Plant Protection Biology, Swedish University of Agricultural Sciences, Box 102, 23053 Alnarp, Sweden
                [ ]Present address: Department of Biological Sciences, Vanderbilt University, Nashville, TN 37235 USA
                [ ]Biological Control Laboratory, Colombian Corporation for Agricultural Research, Km 14 via Mosquera-Bogotá, Mosquera, Colombia
                [ ]Fachbereich Biologie, Universität Konstanz, 78457 Konstanz, Germany
                [ ]Present address: Institute of Imaging & Computer Vision, RWTH Aachen University, Kopernikusstr. 16, 52074 Aachen, Germany
                [ ]Present address: Department of Environmental Sciences, COMSATS Institute of Information Technology, Vehari, Pakistan
                Article
                188
                10.1186/s12915-015-0188-3
                4571119
                26377197
                7095f0e2-4c87-42fa-861a-8a66d7bd8ef5
                © Hatano et al. 2015

                Open AccessThis article is distributed under the terms of the Creative Commons Attribution 4.0 International License ( http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The Creative Commons Public Domain Dedication waiver ( http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated.

                History
                : 9 April 2015
                : 5 September 2015
                Categories
                Research Article
                Custom metadata
                © The Author(s) 2015

                Life sciences
                (e)-4,8-dimethyl-1,3,7-nonatriene,herbivore-induced plant volatiles,suppression,antennal lobe,spodoptera littoralis,oviposition choice,mating disruption,olfaction,orientation

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