Can soil microbial diversity influence plant metabolites and life history traits of a rhizophagous insect? A demonstration in oilseed rape

Abstract

Interactions between plants and phytophagous insects play an important part in shaping the biochemical composition of plants. Reciprocally plant metabolites can influence major life history traits in these insects and largely contribute to their fitness. Plant rhizospheric microorganisms are an important biotic factor modulating plant metabolites and adaptation to stress. While plant-insects or plant-microorganisms interactions and their consequences on the plant metabolite signature are well-documented, the impact of soil microbial communities on plant defenses against phytophagous insects remains poorly known. In this study, we used oilseed rape (Brassica napus) and the cabbage root fly (Delia radicum) as biological models to tackle this question. Even though D. radicum is a belowground herbivore as a larva, its adult life history traits depend on aboveground signals. We therefore tested whether soil microbial diversity influenced emergence rate and fitness but also fly oviposition behavior, and tried to link possible effects to modifications in leaf and root metabolites. Through a removal-recolonization experiment, 3 soil microbial modalities ("high," "medium," "low") were established and assessed through amplicon sequencing of 16S and 18S ribosomal RNA genes. The "medium" modality in the rhizosphere significantly improved insect development traits. Plant-microorganism interactions were marginally associated to modulations of root metabolites profiles, which could partly explain these results. We highlighted the potential role of plant-microbial interaction in plant defenses against Delia radicum. Rhizospheric microbial communities must be taken into account when analyzing plant defenses against herbivores, being either below or aboveground.

Influence of Belowground Herbivory on the Dynamics of Root and Rhizosphere Microbial Communities

“…Herbivory tended to decrease root AAs and CPOs, which is consistent with the results of Hopkins et al (1999), van Leur et al (2008, and Lachaise et al (2017). Herbivory increased glycerate and trehalose, a sugar assumed to play a role in plant defenses against aphid infestation (Singh et al, 2011).…”

“…As described in Lachaise et al (2017), this mixture was sterilized at 35 kGy and left 2 months to stabilize before inoculation while the remaining unsterilized soil with no silica was ground and sieved at 2 mm before being suspended in water. Following the detailed protocol of Lachaise et al (2017), this suspension was then undiluted (10 0 ) or diluted at 10 6 before inoculating the sterilized soil, hence creating the two levels of soil microbial diversity used in our experiment: respectively "high" and "low" initial soil microbial diversities, also referred to as soil microbial modalities (Figure 1). This dilution-inoculation method was performed three times in order to obtain three soil biological replicates per soil microbial FIGURE 1 | Experimental design.…”

“…Recent studies are unraveling the impact of microorganisms from the rhizosphere on plant-insect interactions and are gradually changing our perception of the microorganisms' capacity to affect plant defenses (Pineda et al, 2017). A single strain or a whole microbial community has been shown to increase plant defenses, which in turn can negatively impact insect fitness (Hol et al, 2010;Pangesti et al, 2015a,b;Lachaise et al, 2017). However, the reverse effect has seldom been investigated while herbivore attacks on plants could represent important perturbations for belowground microbial communities.…”

The promises and challenges of research on plant–insect–microbe interactions

“…In an elegant study, Lachaise et al . () manipulated the soil microbial diversity through dilution series to test whether it could affect the composition in plant metabolites (measured in both roots and leaves) and the life‐history traits of a herbivore insect in the oilseed rape ( Brassica napus )–cabbage root fly ( Delia radicum ) system. While soil microbial diversity marginally influenced root metabolite profiles, insect development traits were significantly improved with an intermediate level of diversity.…”

“…A major challenge is therefore to understand the abiotic factors governing such context-dependency and its underlying mechanisms (de Bobadilla et al, 2017;Karley et al, 2017). Another important challenge is that in the real world these beneficial microbes function in a whole (rhizosphere/phyllosphere) community (i.e., phytobiome), urging a shift toward studies that can shed light on how the effectiveness of these microbes in enhancing pest resistance is modulated in a community context (Lachaise et al, 2017). A fascinating emerging direction of research is the role of microbially produced and induced volatile organic compounds (VOCs) in plant-insect interactions (Rasmann et al, 2017), that can both deter herbivores (Sword et al, 2017) and attract their natural enemies (Coppola et al, 2017).…”