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

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.

Rhizobacterial colonization of roots modulates plant volatile emission and enhances the attraction of a parasitoid wasp to host-infested plants.

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.

Antagonism between two root-associated beneficial Pseudomonas strains does not affect plant growth promotion and induced resistance against a leaf-chewing herbivore.

Plant growth-promoting microbes residing on the roots may cooperate or compete, thereby affecting their collective benefit to the host plant. Pseudomonas simiae WCS417r (formerly known as P. fluorescens WCS417r) and Pseudomonas fluorescens SS101 are well known for their ability to induce systemic resistance in Arabidopsis. Here, we evaluate how these species interact on the roots of Arabidopsis thaliana Col-0 and how their co-inoculation affects plant defense to the leaf-chewing herbivore Mamestra brassicae and plant growth promotion. WCS417r and SS101, applied individually to root tips or at two different positions along the roots, established similar population densities on Arabidopsis roots. When co-inoculated at the same position on the roots, however, WCS417r established significantly higher population densities than SS101. Both upon single inoculation and co-inoculation, the two pseudomonads induced the same level of induced systemic resistance against the caterpillar M. brassicae and the same increase in plant biomass. These results suggest that combined inoculation of both Pseudomonas strains does not significantly modify the plant's defensive capacity compared to individual inoculation, resulting in a similar effect on performance of the generalist herbivore M. brassicae.

Does drought stress modify the effects of plant-growth promoting rhizobacteria on an aboveground chewing herbivore?

Soil microbes have important effects on the interactions of plants with their environment, by promoting plant growth, inducing resistance to pests or by conferring tolerance to abiotic stress. However, their effects are variable and the factors responsible for this variation are mainly unknown. Our aim was to assess how drought stress modifies the effect of the nonpathogenic rhizobacterium Pseudomonas simiae WCS417r on plant growth and resistance against the generalist leaf-chewing caterpillar Mamestra brassicae. We studied Arabidopsis thaliana Col-0 plants, as well as mutants altered in the biosynthesis of the phytohormones jasmonic acid (JA) and abscisic acid (ABA). Caterpillars did not prefer rhizobacteria-treated plants, independently of drought stress. Rhizobacteria colonization had a variable effect on caterpillar performance, which ranged from positive in one experiment to neutral in a second one. Drought had a consistent negative effect on herbivore performance; however, it did not modify the effect of rhizobacteria on herbivore performance. The effect of drought on herbivore performance was JA-mediated (confirmed with the use of the dde2-2 mutant), but it was still present in the ABA-deficient mutant aba2-1. Plant biomass was reduced by both drought and herbivory but it was enhanced by rhizobacterial colonization. Pseudomonas simiae WCS417r is able to promote plant growth even when plants are suffering herbivory. Nevertheless, the microbial effect on the herbivore is variable, independently of drought stress. To get the best possible outcome from the rhizobacteria-plant mutualism it is important to understand which other factors may be responsible for its context-dependency.

Two-way plant mediated interactions between root-associated microbes and insects: from ecology to mechanisms.

Plants are members of complex communities and function as a link between above- and below-ground organisms. Associations between plants and soil-borne microbes commonly occur and have often been found beneficial for plant fitness. Root-associated microbes may trigger physiological changes in the host plant that influence interactions between plants and aboveground insects at several trophic levels. Aboveground, plants are under continuous attack by insect herbivores and mount multiple responses that also have systemic effects on belowground microbes. Until recently, both ecological and mechanistic studies have mostly focused on exploring these below- and above-ground interactions using simplified systems involving both single microbe and herbivore species, which is far from the naturally occurring interactions. Increasing the complexity of the systems studied is required to increase our understanding of microbe-plant-insect interactions and to gain more benefit from the use of non-pathogenic microbes in agriculture. In this review, we explore how colonization by either single non-pathogenic microbe species or a community of such microbes belowground affects plant growth and defense and how this affects the interactions of plants with aboveground insects at different trophic levels. Moreover, we review how plant responses to foliar herbivory by insects belonging to different feeding guilds affect interactions of plants with non-pathogenic soil-borne microbes. The role of phytohormones in coordinating plant growth, plant defenses against foliar herbivores while simultaneously establishing associations with non-pathogenic soil microbes is discussed.