Abstract

Recent studies are unravelling the impact of microorganisms from the roots and rhizosphere on interactions between plants and herbivorous insects and are gradually changing our perception of the microorganisms’ capacity to affect plant defenses, but the reverse effect has seldom been investigated. Our study aimed at determining how plant herbivory influences the dynamics of root and rhizosphere microbial community assemblages and whether potential changes in root metabolites and chemical elements produced during herbivory can be related to microbial community diversity. We conducted our study on oilseed rape (Brassica napus) and its major belowground herbivore, the cabbage root fly (Delia radicum). We further assessed the influence of initial soil microbial diversity on these interactions. Different microbial diversities based on a common soil matrix were obtained through a removal-recolonization method. Root and rhizosphere sampling targeted different stages of the herbivore development corresponding to different perturbation intensities. Root bacterial communities were more affected by herbivory than some rhizosphere bacterial phyla and fungal communities, which seemed more resistant to this perturbation. Root herbivory enhanced the phylum of γ-Proteobacteria in the roots and rhizosphere, as well as the phylum of Firmicutes in the rhizosphere. Herbivory tended to decrease most root amino acids and sugars, and it increased trehalose, indolyl glucosinolates and sulfur. Higher abundances of four bacterial genera (Bacillus, Paenibacillus, Pseudomonas and Stenotrophomonas) were associated following herbivory to the increase of trehalose and some sulfur-containing compounds. Further research would help to identify the biological functions of the microbial genera impacted by plant infestation and their potential implications in plant defense.

Highlights

  • Interactions between plants and herbivorous insects are known to influence the evolution of plant defense mechanisms such as defensive and toxic metabolites or volatiles attracting natural enemies of the pest (Fürstenberg-Hägg et al, 2013; Nishida, 2014)

  • Metabolites and Chemical Elements For each sampling time, two different analyses were performed on metabolites and chemical elements, taking into account the plant treatment, the soil microbial diversity, and the interaction between both factors, as well as soil biological replicates

  • Our study showed that infestation of Oilseed Rape (OSR) by a belowground herbivore increased root bacterial alpha-diversity, while it had no effect on rhizosphere bacteria and very little on fungi

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Summary

Introduction

Interactions between plants and herbivorous insects are known to influence the evolution of plant defense mechanisms such as defensive and toxic metabolites or volatiles attracting natural enemies of the pest (Fürstenberg-Hägg et al, 2013; Nishida, 2014). Since the 90’s, the positive relationship between an ecosystem’s stability and its diversity was addressed in different systems and in grasslands facing different abiotic stresses (Ives and Carpenter, 2007) It seemed that the recovery of an ecosystem following a stress could be conditioned by the ecosystem’s initial diversity prior to this stress. An ecosystem with high plant diversity that suffers a drought will better recover than an ecosystem with a low plant diversity (Tilman and Downing, 1994; van Ruijven and Berendse, 2010) Effects of such stresses were investigated on resistance (the ability to sustain a perturbation or stress) and resilience (the capacity to come back to a stable state) of different soil processes such as nitrogen and carbon cycles, organic matter decomposition, or respiration (Griffiths and Philippot, 2013). This question has never been addressed for microbial communities of agroecosystem plants confronted to insect herbivory

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