Under fire-simultaneous volatilome and transcriptome analysis unravels fine-scale responses of tansy chemotypes to dual herbivore attack

Background: Tansy plants (Tanacetum vulgare L.) are known for their high intraspecific chemical variation, especially of volatile organic compounds (VOC) from the terpenoid compound group. These VOCs are closely involved in plant-insect interactions and, when profiled, can be used to classify plants into groups known as chemotypes. Tansy chemotypes have been shown to influence plant-aphid interactions, however, to date no information is available on the response of different tansy chemotypes to simultaneous herbivory by more than one insect species. Results: Using a multi-cuvette system, we investigated the responses of five tansy chemotypes to feeding by sucking and/or chewing herbivores (aphids and caterpillars; Metopeurum fuscoviride Stroyan and Spodoptera littoralis Boisduval). Herbivory by caterpillars following aphid infestation led to a plant chemotype-specific change in the patterns of terpenoids stored in trichome hairs and in VOC emissions. The transcriptomic analysis of a plant chemotype represents the first de novo assembly of a transcriptome in tansy and demonstrates priming effects of aphids on a subsequent herbivory. Overall, we show that the five chemotypes do not react in the same way to the two herbivores. As expected, we found that caterpillar feeding increased VOC emissions, however, a priori aphid infestation only led to a further increase in VOC emissions for some chemotypes. Conclusions: We were able to show that different chemotypes respond to the double herbivore attack in different ways, and that pre-treatment with aphids had a priming effect on plants when they were subsequently exposed to a chewing herbivore. If neighbouring chemotypes in a field population react differently to herbivory/dual herbivory, this could possibly have effects from the individual level to the group level. Individuals of some chemotypes may respond more efficiently to herbivory stress than others, and in a group environment these louder chemotypes may affect the local insect community, including the natural enemies of herbivores, and other neighbouring plants.