Bouneb, Mabrouk (2014) Tri-Trophic Interactions: Impact of Russet Mite on the Induced Defences of Tomato against Spider Mites. [Tesi di dottorato]

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Abstract

Plant and herbivores coexist for millions of years and have developed an arsenal of complex interactions. They can be mutually beneficial or antagonistic. In antagonistic interaction, plants have evolved a wide array of constitutive morphological, biochemical and molecular defences to defend themselves from herbivore attacks (Karban and Baldwin, 1997; Walling, 2000). In addition, plants can activate induced direct defences that often act systemically throughout the plant and are typically effective against a broad spectrum of invaders (Green and Ryan, 1972). Moreover, plants under herbivore attack synthesize and release complex blend of volatiles that attract the third trophic level, predators or parasitoids, resulting in increased attacks on herbivores (Turlings and Wäckers, 2004). This later response is known as indirect defence and include a third trophic carnivore to increase plant fitness and resistance against herbivory. Induced direct and indirect plan defences are mainly orchestrated in jasmonic acid, ethylene and salicylic acid signaling pathways. When plants are attacked by single herbivore species, JA/ethylene pathway commonly regulates plant response to wounding by herbivorous invader, whereas salicylic acid controls systemic acquired resistance (SAR) in pathogen-like induced response. However, in their natural environment plants are exposed simultaneously to multiple herbivory and the interactions are often more complex. Yet, infestations by multiple herbivores having similar or distinct feeding guilds elicited plant defences in different manner compared to single herbivore. Despite available reports from over 100 plant-herbivore systems concerning plant induced responses to herbivory (Agrawal, 1998), very few studies involved acarine herbivores. Therefore, more studies are required to understand plant-herbivore interaction in a more natural and complex system. The aim of this project was to enhance our understanding of the plant-herbivorous mites interaction in a context of multiple herbivory and to evaluate the effects of such interaction on the third-trophic level. To this goal, I analyzed the transcriptional changes of the main defence genes in tomato (Solanum lycopersicum) in response to simultaneous attack by spider mite (Tetranychus urticae) and eriophyoid russet mite (Aculops lycopersici) and single attack by the corresponding herbivores. The defence genes studied were: tomato lipoxygenase D (TomLoxD) and allene oxide synthase (AOS), two genes in the octadecanoid pathway upstream to jasmonic acid biosynthesis; wound induced proteinase inhibitor II (WIPI-II), a JA-responisive gene; pathogenesis related protein 1 (PR-1), a salicylic-dependent gene; geranylgeranyl pyrophosphate synthase 1 (GGPS1), a gene involved in terpene synthase. I also evaluated the consequence of the resulted interaction on olfactory choice of specialist and generalist predaceous phytoseiid, Phytoseiulus persimilis and Neoseiulus californicus, respectively. Here I report in dual infestation, that the eriophyoid russet mite suppresses the induction of upstream and downstream signals of JA triggred by spider mite in local and distant systemic tomato leaves. Russet mite and spider mite both induced PR-1. Due to this interaction, spider mites under dual infestation showed increased performance. Moreover, both specialist and generalist predatory mites were more attracted to tomato plants attacked by spider mites compared to dual attack. The olfactory choice of predatory mites was dependent on population density of russet mites and on the extent of damage. In correspondence with the observed olfactory choice, analysis of volatiles emitted from tomato plants in response to different mite herbivory revealed a clear decrease in total volatiles in plants under dual attack compared to spider mite-attacked plants. Predatory mites seem to respond to tomato volatiles emitted in response to different herbivory as a whole blend and not as specific compounds.

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