Leaf-Miners Co-opt Microorganisms to Enhance their Nutritional Environment
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Organisms make the best of their mother’s oviposition choices and utilize specific feeding options that meet energetic requirements and cope with environmental constraints. This is particularly true for leaf-miner insects that develop enclosed in the two epidermis layers of a single leaf for their entire larval life. Cytokinins (CKs) play a central role in plant physiology – including regulation of senescence and nutrient translocation – and, as such, can be the specific target of plant exploiters that manipulate plant primary metabolism. ‘Green-islands’ are striking examples of a CK-induced phenotype where green areas are induced by plant pathogens/insects in otherwise yellow senescent leaves. Here, we document how the leaf-miner caterpillar Phyllonorycter blancardella, working through an endosymbiotic bacteria, modifies phytohormonal profiles, not only on senescing (photosynthetically inactive) but also on normal (photosynthetically active) leaf tissues of its host plant (Malus domestica). This leaf physiological manipulation allows the insect to maintain sugar-rich green tissues and to create an enhanced nutritional microenvironment in an otherwise degenerating context. It also allows them to maintain a nutritional homeostasis even under distinct leaf environments. Our study also highlights that only larvae harboring bacterial symbionts contain significant amounts of CKs that are most likely not plant-derived. This suggests that insects are able to provide CKs to the plant through their symbiotic association, thus extending further the role of insect bacterial symbionts in plant-insect interactions.
KeywordsLeaf-miner Cytokinins Endophytic plant parasite Endosymbiont Hormonal manipulation
This work was supported by the ANR grant n° ANR-05-JCJC-0203-01 and the Région Centre grant ENDOFEED 201000047141 to David Giron. Further support was also provided by the National Centre of Scientific Research (CNRS) and the University François-Rabelais. We thank Laurent Ardouin for full access to his orchard and Jean-Philippe Christidès, Arnaud Lanoue, Gaëlle Glevarec, Elisabeth Huguet, Benoît St-Pierre and Nadine Imbault for their help with the laboratory work and helpful discussions. We also thank 3 anonymous referees and the editor for helpful comments on the manuscript.
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