Several soil-borne microbes such as mycorrhizal fungi and plant growth-promoting rhizobacteria can help plants to deal with biotic and abiotic stresses via plant growth promotion and induced resistance. Such beneficial belowground microbes interact in a bidirectional way via the plant with aboveground insects such as herbivores, their natural enemies and pollinators. The role of these interactions in natural and agricultural ecosystems is receiving increased attention, and the molecular and physiological mechanisms involved in these interactions should be the focus of more attention. Here, we review the recent discoveries on plant-mediated interactions between beneficial belowground microbes and aboveground insects.

Systemic resistance induced in plants by nonpathogenic rhizobacteria is typically effective against multiple pathogens. Here, we show that root-colonizing Pseudomonas fluorescens strain SS101 (Pf.SS101) enhanced resistance in Arabidopsis (Arabidopsis thaliana) against several bacterial pathogens, including Pseudomonas syringae pv tomato (Pst) and the insect pest Spodoptera exigua. Transcriptomic analysis and bioassays with specific Arabidopsis mutants revealed that, unlike many other rhizobacteria, the Pf.SS101-induced resistance response to Pst is dependent on salicylic acid signaling and not on jasmonic acid and ethylene signaling. Genome-wide transcriptomic and untargeted metabolomic analyses showed that in roots and leaves of Arabidopsis plants treated with Pf.SS101, approximately 1,910 genes and 50 metabolites were differentially regulated relative to untreated plants. Integration of both sets of "omics" data pointed to a prominent role of camalexin and glucosinolates in the Pf.SS101-induced resistance response. Subsequent bioassays with seven Arabidopsis mutants (myb51, cyp79B2cyp79B3, cyp81F2, pen2, cyp71A12, cyp71A13, and myb28myb29) disrupted in the biosynthesis pathways for these plant secondary metabolites showed that camalexin and glucosinolates are indeed required for the induction of Pst resistance by Pf. SS101. Also for the insect S. exigua, the indolic glucosinolates appeared to play a role in the Pf.SS101-induced resistance response. This study provides, to our knowledge for the first time, insight into the substantial biochemical and temporal transcriptional changes in Arabidopsis associated with the salicylic acid-dependent resistance response induced by specific rhizobacteria.

Summary 1.Plants have a complex immune system that defends them against attackers (e.g. herbivores and microbial pathogens) but that also regulates the interactions with mutualistic organisms (e.g. mycorrhizal fungi and plant growth-promoting rhizobacteria). Plants have to respond to multiple environmental challenges, so they need to integrate both signals associated with biotic and abiotic stresses in the most appropriate response to survive. 2. Beneficial microbes such as rhizobacteria and mycorrhizal fungi can help plants to 'deal' with pathogens and herbivorous insects as well as to tolerate abiotic stress. Therefore, beneficial microbes may play an important role in a changing environment, where abiotic and biotic stresses on plants are expected to increase. The effects of beneficial microbes on herbivores are highly context-dependent, but little is known on what is driving such dependency. Recent evidence shows that abiotic stresses such as changes in soil nutrients, drought and salt stress, as well as ozone can modify the outcome of plant-microbe-insect interactions. 3. Here, we review how abiotic stress can affect plant-microbe, plant-insect and plantmicrobe-insect interactions, and the role of the network of plant signal-transduction pathways in regulating such interactions. 4. Most of the studies on the effects of abiotic stress on plant-microbe-insect interactions show that the effects of microbes on herbivores (positive or negative) are strengthened under stressful conditions. We propose that, at least in part, this is due to the crosstalk of the different plant signalling pathways triggered by each stress individually. By understanding the cross-regulation mechanisms we may be able to predict the possible outcomes of plantmicrobe-insect interactions under particular abiotic stress conditions. We also propose that microbes can help plants to deal with insects mainly under conditions that compromise efficient activation of plant defences. 5. In the context of global change, it is crucial to understand how abiotic stresses will affect species interactions, especially those interactions that are beneficial for plants. The final aim of this review is to stimulate studies unravelling when these 'beneficial' microbes really benefit a plant.

Evolutionary theory of plant defences against herbivores predicts a trade-off between direct (anti-herbivore traits) and indirect defences (attraction of carnivores) when carnivore fitness is reduced. Such a trade-off is expected in plant species that kill herbivore eggs by exhibiting a hypersensitive response (HR)-like necrosis, which should then negatively affect carnivores. We used the black mustard (Brassica nigra) to investigate how this potentially lethal direct trait affects preferences and/or performances of specialist cabbage white butterflies (Pieris spp.), and their natural enemies, tiny egg parasitoid wasps (Trichogramma spp.). Both within and between black mustard populations, we observed variation in the expression of Pieris egg-induced HR. Butterfly eggs on plants with HR-like necrosis suffered lower hatching rates and higher parasitism than eggs that did not induce the trait. In addition, Trichogramma wasps were attracted to volatiles of egg-induced plants that also expressed HR, and this attraction depended on the Trichogramma strain used. Consequently, HR did not have a negative effect on egg parasitoid survival. We conclude that even within a system where plants deploy lethal direct defences, such defences may still act with indirect defences in a synergistic manner to reduce herbivore pressure.

Beneficial soil-borne microbes, such as mycorrhizal fungi or rhizobacteria, can affect the interactions of plants with aboveground insects at several trophic levels. While the mechanisms of interactions with herbivorous insects, that is, the second trophic level, are starting to be understood, it remains unknown how plants mediate the interactions between soil microbes and carnivorous insects, that is, the third trophic level. Using Arabidopsis thaliana Col-0 and the aphid Myzus persicae, we evaluate here the underlying mechanisms involved in the plant-mediated interaction between the non-pathogenic rhizobacterium Pseudomonas fluorescens and the parasitoid Diaeretiella rapae, by combining ecological, chemical and molecular approaches. Rhizobacterial colonization modifies the composition of the blend of herbivore-induced plant volatiles. The volatile blend from rhizobacteria-treated aphid-infested plants is less attractive to an aphid parasitoid, in terms of both olfactory preference behaviour and oviposition, than the volatile blend from aphid-infested plants without rhizobacteria. Importantly, the effect of rhizobacteria on both the emission of herbivore-induced volatiles and parasitoid response to aphid-infested plants is lost in an Arabidopsis mutant (aos/dde2-2) that is impaired in jasmonic acid production. By modifying the blend of herbivore-induced plant volatiles that depend on the jasmonic acid-signalling pathway, rootcolonizing microbes interfere with the attraction of parasitoids of leaf herbivores.

Soil-borne microbes affect aboveground herbivorous insects through a cascade of molecular and chemical changes in the plant, but knowledge of these microbe-plant-insect interactions is mostly limited to one or a few microbial strains. Yet, the soil microbial community comprises thousands of unique taxa interacting in complex networks, the so-called 'microbiome', which provides plants with multiple beneficial functions. There has been little exploration of the role and management of whole microbiomes in plant-insect interactions, calling for the integration of this complexity in aboveground-belowground research. Here, we propose holistic approaches to select soil microbiomes that can be used to protect plants from aboveground attackers.

Beneficial microbes, such as plant growth-promoting rhizobacteria and mycorrhizal fungi, may have a plant-mediated effect on insects aboveground. The plant growth-promoting rhizobacterium Pseudomonas fluorescens can induce systemic resistance in Arabidopsis thaliana against several microbial pathogens and chewing insects. However, the plant-mediated effect of these beneficial microbes on phloem-feeding insects is not well understood. Using Arabidopsis as a model, we here report that P. fluorescens has a positive effect on the performance (weight gain and intrinsic rate of increase) of the generalist aphid Myzus persicae, while no effect was recorded on the crucifer specialist aphid Brevicoryne brassicae. Additionally, transcriptional analyses of selected marker genes revealed that in the plant-microbe interaction with M. persicae, rhizobacteria (i) prime the plant for enhanced expression of LOX2, a gene involved in the jasmonic acid (JA)-regulated defence pathway, and (ii) suppress the expression of ABA1, a gene involved in the abscisic acid (ABA) signalling pathway, at several time points. In contrast, almost no effect of the plant-microbe interaction with B. brassicae was found at the transcriptional level. This study presents the first data on rhizobacteria-induced systemic susceptibility to an herbivorous insect, supporting the pattern proposed for other belowground beneficial microbes and aboveground phloem feeders. Moreover, we provide further evidence that at the transcript level, soil-borne microbes modify plant-aphid interactions.

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.