Abstract

Beneficial soil microbes can promote plant growth and induce systemic resistance (ISR) in aboveground tissues against pathogens and herbivorous insects. Despite the increasing interest in microbial-ISR against herbivores, the underlying molecular and chemical mechanisms of this phenomenon remain elusive. Using Arabidopsis thaliana and the rhizobacterium Pseudomonas simiae WCS417r (formerly known as P. fluorescens WCS417r), we here evaluate the role of the JA-regulated MYC2-branch and the JA/ET-regulated ORA59-branch in modulating rhizobacteria-ISR to Mamestra brassicae by combining gene transcriptional, phytochemical, and herbivore performance assays. Our data show a consistent negative effect of rhizobacteria-mediated ISR on the performance of M. brassicae. Functional JA- and ET-signaling pathways are required for this effect, as shown by investigating the knock-out mutants dde2-2 and ein2-1. Additionally, whereas herbivory mainly induces the MYC2-branch, rhizobacterial colonization alone or in combination with herbivore infestation induces the ORA59-branch of the JA signaling pathway. Rhizobacterial colonization enhances the synthesis of camalexin and aliphatic glucosinolates (GLS) compared to the control, while it suppresses the herbivore-induced levels of indole GLS. These changes are associated with modulation of the JA-/ET-signaling pathways. Our data show that the colonization of plant roots by rhizobacteria modulates plant-insect interactions by prioritizing the JA/ET-regulated ORA59-branch over the JA-regulated MYC2-branch. This study elucidates how microbial plant symbionts can modulate the plant immune system to mount an effective defense response against herbivorous plant attackers.Electronic supplementary materialThe online version of this article (doi:10.1007/s10886-016-0787-7) contains supplementary material, which is available to authorized users.

Highlights

  • Plants as primary producers in terrestrial ecosystems are exposed to various attackers, with insect herbivores among the most important ones

  • The following treatments were compared: control plants infested with M. brassicae (CM), rhizobacteria-treated plants infested with M. brassicae (RM), as well as uninfested control plants (C) and rhizobacteria-treated plants (R) in wild type A. thaliana Col-0, and the mutants myc2 and ora59

  • We evaluated the effect of treatment on GLS levels in wild type A. thaliana Col-0, and in the mutants dde2-2, ein2-1, Fig 2 Projection to Latent Structures Discriminant Analysis (PLS-DA) comparison of Arabidopsis thaliana Col-0 GLS profiles in shoots of control plants (C), rhizobacteria-treated plants (R), control plants infested with Mamestra brassicae (CM), or rhizobacteria-treated plants infested with M. brassicae (RM)

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Summary

Introduction

Plants as primary producers in terrestrial ecosystems are exposed to various attackers, with insect herbivores among the most important ones. In Brassicaceous plants, including Arabidopsis thaliana, glucosinolates (GLS) are the main defensive compounds that confer plant resistance against insect herbivores (Beekwilder et al 2008; Howe and Jander 2008; Mewis et al 2006; Müller et al 2010). Feeding by specialist and generalist leaf-chewing insects triggers enhanced synthesis of aliphatic and indolic GLS (Kos et al 2012; Verhage et al 2011). More recent studies show that other compounds, such as camalexin, a brassicaceous indolic phytoalexin, contribute to plant resistance against herbivores (Kettles et al 2013; Kusnierczyk et al 2008; Prince et al 2014; Schlaeppi et al 2008). Unraveling how plant signaling pathways and crosstalk between pathways regulate the synthesis of defensive compounds in the context of multitrophic interactions has only just begun

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