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Institut de Recherche sur la Biologie de l'Insecte

UMR 7261 Faculté des Sciences et Techniques

Avenue Monge, Parc Grandmont  

37200 TOURS (France)

The sedentary behaviour of endophagous arthropods (i.e.; living within plant tissues) makes them ideal systems for interpreting the ecological and evolutionary mechanisms of herbivory and related questions such as plant resistance or physiological manipulation. Such intimate associations are expected to facilitate close interactions between independent genomes leading to biochemical and hormonal cross-talks between arthropods and plants, setting the ground for altered plant gene expression and changes in plant hormone activity. Our group focuses on understanding the adaptive significance and evolution of endophagous life history modes by studying the intimate physiological, biochemical and molecular mechanisms used by leafminer insects to manipulate their host-plant environment and their fitness consequences for the insect (Figure 1). We aim to understand how plant and herbivores interact by focusing on nutritional benefits (plant nutrients) and costs (plant defensive compounds) but also on the ancestral and convergent role of hormones (cytokinins) and the pivotal role played by endosymbiotic bacteria (Wolbachia).

Figure 1. Host-plant manipulation induced by endophagous insects.

We also seek to identify insect effectors produced and involved in the plant manipulation and to estimate the impact of the internal-feeding strategy on major insect life history traits. Finally, our results highlight major similarities between leafminer and gall-inducer insects suggesting the existence of converging strategies used by these organisms to exploit their host-plant environment. We intend to pursue this type of work at the interface between molecular ecology, integrative physiology and behavioral ecology in order to unravel the similarities and differences in interactive patterns and signalling systems developed by various endophytophagous organisms, and to put the results in a life history context.

Figure 2. influence of Wolbachia on "green-island" formation.

Our recent findings reveal an unexpected capacity of leafminers to manipulate the plant physiology to their own advantages. Our results on the Malus domestica/Phyllonorycter blancardella plant-leaf mining system show:

(i) The ability of this leafminer caterpillar to manipulate its host plant in order to generate a microenvironment with all the nutrient supply (sugars and proteins) needed for its survival.

(ii) A decrease in plant defences compounds within the mined area. We recently identified major molecular steps on which the insect can act and the metabolic consequences for the phenylpropanoids pathway.

(iii) A large accumulation of cytokinins in the mined tissues which is responsible for the preservation of functional nutrient-rich green tissues at a time when leaves are otherwise turning yellow. This plant physiology manipulation is however not restricted to a specific time of the season but occurs at all stages of the plant ontogeny.

(iv) The primary role played by endosymbiotic bacteria (Wolbachia) in the synthesis of these cytokinins and in the induction of nutrient-rich tissues. Removing these bacteria results in the absence of "green-island" formation on leaves, increased compensatory larval feeding, and higher insect mortality (Figure 2.).

We are currently investigating more specifically the sugar profile of mined areas compared to unparasitized tissues. Indeed, sugars not only play an important role as energetic substrates for the insect but also as signal molecules within the plant. Amino acids profiles are also investigated. We also investigate the plant molecular reconfiguration at a larger scale and the plant signaling pathways involved. We are furthermore currently developing a new research project on insect effectors produced by various “reprogramers” of plants.

In addition, several sub-projects are on the run:

- Composition, dynamics and role of the insect microbiome. Collaborations: E. Huguet & F. Dedeine (IRBI - Tours), D. Bouchon (Ecology, Evolution and Symbiosis group – Poitiers)

- Impact of the plant reconfiguration on the endophytic community. Collaboration: S. Prado & B. Ney (Muséum National d’Histoire Naturelle – Paris)

- Cytokinin signal perception and transduction. Collaboration: G. Glevarec (BBV Plant Biology Department – Tours)  

Giron D, Frago E, Glevarec G, Pieterse CMJ & Dicke M. (2013). Cytokinins as key regulators in plant–microbe–insect interactions: connecting plant growth and defence . Functional Ecology 27(3), 599-609 doi:10.1111/1365-2435.12042

Body M, Kaiser W, Dubreuil G, Casas J & Giron D. (2013). Leaf-Miners Co-opt Microorganisms to Enhance their Nutritional Environment. Journal of Chemical Ecology 39(7), 969-977. doi: 10.1007/s10886-013-0307-y

Robert C, Veyrat N, Glauser G, Marti G, Doyen GR, Villard N, Gaillard MDP, Köllner TG, Giron D, Body M, Babst BA, Ferrieri RA, Turlings TCJ & Erb M.(2012)  A specialist root herbivore exploits defensive metabolites to locate nutritious tissues.Ecology Letters 15 (1), 55-64

Giron D. & Huguet E. (2011). A genomically tractable and ecologically relevant model herbivore for a model plant: new insights on mechanisms of insect-plant interactions and evolution. Molecular Ecology 20 (5), 990-994. DOI: 10.1111/j.1365-294X.2010.04902.x

Kaiser W., Huguet E., Casas J., Commin C. & Giron D. (2010) Plant green-island phenotype induced by leaf-miners is mediated by bacterial symbionts. Proceedings of The Royal Society London B, 277: 2311–2319.

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