Abstract

Beneficial root-associated microbes modify the physiological status of their host plants and affect direct and indirect plant defense against insect herbivores. While the effects of these microbes on direct plant defense against insect herbivores are well described, knowledge of the effect of the microbes on indirect plant defense against insect herbivores is still limited. In this study, we evaluate the role of the rhizobacterium Pseudomonas fluorescens WCS417r in indirect plant defense against the generalist leaf-chewing insect Mamestra brassicae through a combination of behavioral, chemical, and gene-transcriptional approaches. We show that rhizobacterial colonization of Arabidopsis thaliana roots results in an increased attraction of the parasitoid Microplitis mediator to caterpillar-infested plants. Volatile analysis revealed that rhizobacterial colonization suppressed the emission of the terpene (E)-α-bergamotene and the aromatics methyl salicylate and lilial in response to caterpillar feeding. Rhizobacterial colonization decreased the caterpillar-induced transcription of the terpene synthase genes TPS03 and TPS04. Rhizobacteria enhanced both the growth and the indirect defense of plants under caterpillar attack. This study shows that rhizobacteria have a high potential to enhance the biocontrol of leaf-chewing herbivores based on enhanced attraction of parasitoids.Electronic supplementary materialThe online version of this article (doi:10.1007/s00442-015-3277-7) contains supplementary material, which is available to authorized users.

Highlights

  • Plants are exposed to attack by various insect herbivores and defend themselves directly, e.g., by producing toxic compounds, and indirectly, e.g., by emitting herbivoreinduced plant volatiles (HIPVs) that attract natural enemies of the herbivores (Clavijo McCormick et al 2012; Dicke and Baldwin 2010; Jensen et al 2002; Turlings et al 1995)

  • Data on M. brassicae larval weight were analyzed with a linear mixed model (LMM) with treatment as a fixed factor and experimental group as a random factor

  • Our study shows that P. fluorescens WCS417r colonization of A. thaliana roots results in an increased attraction of the parasitoid wasp M. mediator to host-infested plants, and an increase in larval weight of the herbivore

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Summary

Introduction

Plants are exposed to attack by various insect herbivores and defend themselves directly, e.g., by producing toxic compounds, and indirectly, e.g., by emitting herbivoreinduced plant volatiles (HIPVs) that attract natural enemies of the herbivores (Clavijo McCormick et al 2012; Dicke and Baldwin 2010; Jensen et al 2002; Turlings et al 1995). The effect of herbivore-induced plant volatiles (HIPVs) on the behavior of natural enemies has been widely studied in the context of interactions between one plant, one insect herbivore, and one natural enemy (Mumm and Dicke 2010). The exploration of such tritrophic interactions is being extended to interactions in more complex systems (Dicke et al 2009; Heil 2014; Pineda et al 2013). Reymond 2013; Soler et al 2007; Dam and Heil 2011; Zhang et al 2013) Belowground beneficial microbes such as mycorrhizae, rhizobia, and rhizobacteria constitute a fascinating functional group in the plant-associated community that can enhance plant growth and resistance against pathogens and herbivorous insects (Hartley and Gange 2009; Pineda et al 2010; Pozo and Azcon-Aguilar 2007). More recently, the effects of mutualistic microbes on the emission of HIPV and on natural enemies of herbivorous insects have been studied (Ballhorn et al 2013; Pineda et al 2013; Schausberger et al 2012)

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