Unravelling the complexity of plant-insect interactions: the hidden role played by herbivore-associated-organisms

Project Information

HerbivoreAssociatedOrganisms

Grant agreement ID: 655178

DOI

10.3030/655178

Project closed

EC signature date 5 March 2015

Start date 4 January 2016

End date 3 January 2018

Funded under

• EXCELLENT SCIENCE - Marie Skłodowska-Curie Actions

Total cost

€ 165 598,80

EU contribution

€ 165 598,80

Coordinated by

WAGENINGEN UNIVERSITY
Netherlands

Periodic Reporting for period 1 - HerbivoreAssociatedOrganisms (Unravelling the complexity of plant-insect interactions: the hidden role played by herbivore-associated-organisms)

Reporting period: 2016-01-04 to 2018-01-03

Summary of the context and overall objectives of the project

Plants interact with a suite of different organisms in nature, including herbivorous and carnivorous insects. It is now recognized that plants are not alone when interacting with other organisms because hidden players may modulate the strength of plant-insect interactions. In particular, there is growing evidence on the effects of microbial symbionts in plant responses towards herbivory. Plant-associated symbionts such as mycorrhizal fungi affect not only plant growth but also plant defences by inducing systemic resistance towards a wide range of attackers including aboveground herbivores. Herbivore-associated symbionts such as bacteria present in oral secretions can manipulate the physiology of plants to the benefit of their herbivore hosts. Carnivorous insects can also harbour symbionts but their role has not been investigated in a plant-insect perspective. Among carnivorous insects, parasitoids are a common group of insects whose larvae develop at the expense of the herbivorous host eventually killing it. It has been shown that parasitoids alter the physiology of their herbivorous host, and this in turn changes the way the herbivore interacts with the plant with consequences for species interactions across multiple trophic levels. The effect of parasitization of herbivores on plant responses has been assumed to be triggered by the parasitic wasp larvae feeding within the herbivore’s body. However, thousands of parasitoid species inject specific symbiotic viruses (polydnaviruses) into their hosts that manipulate herbivore physiology and immune responses. During oviposition, parasitoids also inject venoms which may synergize the effects of polydnaviruses and can be required for expression of viral genes in the caterpillar.
To unravel the role of parasitoid symbionts at the plant-insect interface and to raise awareness on the importance of these interactions, the HerbivoreAssociatedOrganisms project has developed several scientific objectives, training activities and dissemination practices. The first main research objective of this project was to explore whether parasitoid symbionts injected in the caterpillar affect plant phenotype to the extent that it influences the behaviour of other insect community members associated with the same plant. The second main research objective of this project was to investigate the molecular mechanisms underlying the ecology of plant-herbivore interactions induced by parasitoid symbionts. We concluded that parasitoid symbionts affect plant-insect interactions at different levels of biological organization, from plant gene expression to consequences for the wider plant-associated insect community.

Work performed from the beginning of the project to the end of the period covered by the report and main results achieved so far

In this project we experimentally manipulated the phenotype of Cabbage White caterpillars (Pieris brassicae) by injections of eggs, viral particles and venom isolated from the parasitoid Cotesia glomerata. After injections, the caterpillars were allowed to feed on wild cabbage plants to start induction of plant responses.
In the context of the first main research objective, we tested the hypothesis that virus-infected caterpillars induce plant phenotypic changes that affect the subsequent colonization of the plant by diamondback moths. We found evidence that the diamondback moth lays fewer eggs on leaves damaged by Cabbage White caterpillars injected with a combination of polydnaviruses and venom compared to control leaves, i.e. leaves damaged by caterpillars injected with phosphate-buffered saline. Another hypothesis tested was whether members of the forth trophic level (i.e. hyperparasitoids which are enemies of parasitoids) could exploit herbivore-induced plant volatiles released in response to feeding by polydnaviruses-infected caterpillars to locate their parasitoid hosts. We found behavioural evidence that the hyperparasitoid Lysibia nana is attracted to plant volatiles induced by caterpillars injected with viral symbionts and venom. We also carried out a semi-field experiment to test whether parasitoid symbionts impact plant fitness and the results of this experiment are still under progress.
In the context of the second main research objective, we tested the hypothesis that polydnaviruses alter caterpillar- and plant-defence related genes. We found that injection of polydnaviruses and venom downregulated transcript levels of key genes putatively involved in plant responses toward herbivory. Indeed, many elicitors that plants use in herbivore recognition have been identified in the oral secretions of caterpillars that come in contact with plant tissues during herbivore feeding. We also found that oral secretion collected from caterpillars injected with polydnavirus and venom had reduced transcriptional responses of plant genes involved in chemical defences (i.e. brassicaceous secondary metabolites). We found that polydnaviruses act in combination with venom mimicking the same effects induced by parasitization on transcriptional responses in caterpillars and plants.

Progress beyond the state of the art and expected potential impact (including the socio-economic impact and the wider societal implications of the project so far)

This project has revealed an exciting and remarkable effect of insect symbionts on plant-insect interactions by showing that symbionts of parasitoids: 1) play a key role in plant-mediated species interactions 2) affect caterpillar oral secretions and plant defensive responses to herbivory. We also demonstrate that, surprisingly, the parasitoid offspring itself developing within the herbivore’s body is not the major driver of parasitism-mediated effects on the induction of plant responses.
An important part of the HerbivoreAssociatedOrganisms project has been devoted to result dissemination and networking. The fellow has attended several key international conferences (including two held in the USA), two Dutch national conferences and has visited three international research institutes where talks about the project were given. A multidisciplinary approach was essential to carry out this project, and the laboratory led by Dr. Volkoff at the University of Montpellier in France has been the main collaborator. Collaboration with the group in Montpellier was not only important to develop the methodology, but also to establish links between plant-insect interactions (expertise of Dicke’s group) and herbivore-parasitoid interactions (expertise of Volkoff’s group). The fellow has visited the group twice, and a publications that involve both Dicke’s group and Volkoff’s group has been recently accepted.
In the short term, the main impacts of this project are to advance the state-of-the-art of fundamental research, although we appreciate important environmental, agricultural and socio-economic impacts in the long term. Polydnaviruses (and a wide array of parasitoid-derived toxins) can be potentially used to kill insect pests and/or enhance plant defences to replace conventional insecticides. Furthermore, the fact that hyperparasitoids locate their parasitoid hosts via herbivore-induced plant volatiles is relevant for biological control, a major sustainable method of insect control. Indeed, hyperparasitoids can disrupt biological control in greenhouses and a better understanding of hyperparasitoid foraging behaviour can be exploited to lure them away from the target crop. We visited the company Biobest Sustainable Crop Management (Belgium) and gave a presentation about hyperparasitoid host location in a biological pest control perspective and discussed potential application to attenuate the negative effect of hyperparasitoids.

a female parasitic wasps (Cotesia glomerata) attacking a caterpillar host (Pieris brassicae)