Variation in plant‐mediated interactions between rhizobacteria and caterpillars: potential role of soil composition

Abstract

Selected strains of non-pathogenic rhizobacteria can trigger induced systemic resistance (ISR) in plants against aboveground insect herbivores. However, the underlying mechanisms of plant-mediated interactions between rhizobacteria and herbivorous insects are still poorly understood. Using Arabidopsis thaliana Col-0-Pseudomonas fluorescens WCS417r as a model system, we investigated the performance and the molecular mechanisms underlying plant-mediated effects of rhizobacteria on the generalist caterpillar Mamestra brassicae and the specialist Pieris brassicae. Rhizobacteria colonisation of Arabidopsis roots resulted in decreased larval weight of M. brassicae, whereas no effect was observed on larval weight of P. brassicae. Using a jasmonic acid (JA)-impaired mutant (dde2-2), we confirmed the importance of JA in rhizobacteria-mediated ISR against M. brassicae. Interestingly, in some experiments we also observed rhizobacteria-induced systemic susceptibility to M. brassicae. The role of soil composition in the variable outcomes of microbe-plant-insect interactions was then assessed by comparing M. brassicae performance and gene transcription in plants grown in potting soil or a mixture of potting soil and sand in a 1:1 ratio. In a mixture of potting soil and sand, rhizobacteria treatment had a consistent negative effect on M. brassicae, whereas the effect was more variable in potting soil. Interestingly, at 24 h post-infestation (hpi) rhizobacteria treatment primed plants grown in a mixture of potting soil and sand for stronger expression of the JA- and ethylene-regulated genes PDF1.2 and HEL, respectively. Our study shows that soil composition can modulate rhizobacteria-plant-insect interactions, and is a factor that should be considered when studying these belowground-aboveground interactions.

Jasmonic Acid and Ethylene Signaling Pathways Regulate Glucosinolate Levels in Plants During Rhizobacteria-Induced Systemic Resistance Against a Leaf-Chewing Herbivore

“…WCS417r was quantified in wild type plants and mutants to confirm that the colonization met the required threshold for ISR of 10 5 cfu.g −1 root (Raaijmakers et al 1995). The rhizobacteria quantification was done following the method described in Pangesti et al (2015), with slight modification. Roots were harvested, weighed, and shaken vigorously for 1 min in 10 ml of 10 mM MgSO 4 containing 0.5 g of glass beads (425–600 μm, Sigma-Aldrich).…”

“…Previous studies have found that this rhizobacterium triggers an enhanced expression of the JA-regulated gene LOX2 and the JA/ET-regulated genes PDF1.2 and HEL upon feeding by the generalist caterpillars M. brassicae and Spodoptera exigua (Pangesti et al 2015; Van Oosten et al 2008). However, whether the JA-regulated MYC2-branch or the JA/ET-regulated ORA59-branch is modulating plant defense in rhizobacteria-mediated ISR against insects is unknown.…”

“…The influence of beneficial microbes on plant defense and growth is mediated by their effect on plant signaling pathways that not only regulate microbial colonization but also trigger significant changes in plant gene expression, metabolism, and physiology (Cartieaux et al 2008; Van de Mortel et al 2012; Verhagen et al 2004; Weston et al 2012). Interestingly, several species of root-associated microbes from the genera Pseudomonas , Bacillus , and Trichoderma enhance plant immunity, through a mechanism called induced systemic resistance (ISR), known to inhibit growth and development of various insect herbivores and pathogens (Pangesti et al 2015; Pineda et al 2010; Song et al 2013; Valenzuela-Soto et al 2010). Intact JA and ET hormonal signaling pathways are required to induce ISR by several root-associated microbes such as P. fluorescens WCS417r against pathogens (Pieterse et al 1998).…”

Architecture and Dynamics of the Jasmonic Acid Gene Regulatory Network

“…Mamestra brassicae eggs were obtained from the laboratory of Entomology at Wageningen University where they were reared as described previously (Pangesti et al, 2015). Per 5-week-old Arabidopsis plant, one freshly hatched first-instar (L1) larva was directly placed on a leaf using a fine paintbrush.…”

Causes and consequences of soil bacterial rarity

“…Subsequently cDNA was diluted by a factor of 1:20 with RNase free water. For RT-qPCR analysis specific primers were used for 5 genes involved in the 3 main plant defence pathways regulated by ET, JA or SA respectively: VSP2 (At5g24770; JA-dependent) (Anderson et al 2004), PDF1.2 (At5g44420; JA-and ET-dependent), PR1 (At2g14610; SAdependent) , HEL (At3g04720; ET-dependent) (Pangesti et al 2015) and CYP79B3, involved in glucosinolate synthesis and inducible by jasmonic acid treatment (At2g22330; JA-dependent) (Lemarié et al 2015) (for all primer sequences see Supplementary Information Table S2). In addition, the expression of the reference genes FBOX (At5g15710) (Remans et al 2008) and GAPDH (At3g04120) ) was assessed for normalization.…”