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.

Plants under herbivore attack are able to initiate indirect defense by synthesizing and releasing complex blends of volatiles that attract natural enemies of the herbivore. However, little is known about how plants respond to infestation by multiple herbivores, particularly if these belong to different feeding guilds. Here, we report the interference by a phloem-feeding insect, the whitefly Bemisia tabaci, with indirect plant defenses induced by spider mites (Tetranychus urticae) in Lima bean (Phaseolus lunatus) plants. Additional whitefly infestation of spider-mite infested plants resulted in a reduced attraction of predatory mites (Phytoseiulus persimilis) compared to attraction to plants infested by spider mites only. This interference is shown to result from the reduction in (E)-␤-ocimene emission from plants infested by both spider mites and whiteflies. When using exogenous salicylic acid (SA) application to mimic B. tabaci infestation, we observed similar results in behavioral and chemical analyses. Phytohormone and gene-expression analyses revealed that B. tabaci infestation, as well as SA application, inhibited spider mite-induced jasmonic acid (JA) production and reduced the expression of two JA-regulated genes, one of which encodes for the P. lunatus enzyme ␤-ocimene synthase that catalyzes the synthesis of (E)-␤-ocimene. Remarkably, B. tabaci infestation concurrently inhibited SA production induced by spider mites. We therefore conclude that in dualinfested Lima bean plants the suppression of the JA signaling pathway by whitefly feeding is not due to enhanced SA levels.herbivore-induced plant volatiles ͉ induced plant defense ͉ insect-plant interactions ͉ phytohormones ͉ terpene synthase A n important indirect defense of plants against herbivores is the emission of plant volatiles that provide important foraging cues for natural enemies of the herbivore (1, 2). Attraction of parasitoids or predators by herbivore-induced plant volatiles (HIPVs) has been well-demonstrated in many plant species both in the laboratory (2) and in the field (3). With regard to the underlying mechanisms, it has been demonstrated that the octadecanoid pathway, with the plant hormone jasmonic acid (JA) as central component, plays an important role in regulating HIPV emission (4, 5), although the shikimic acid and ethylene pathways can play roles as well (6-10). For example, in Lima bean plants, a transient increase of endogenous JA in leaves is involved in the induced synthesis of HIPVs (11), and application of exogenous JA to leaves leads to the induction of a volatile blend similar to the HIPV blend induced by spider mites (12). Conversely, blocking JA synthesis or its action results in the reduction of volatile emission (7), and consequently interferes with the attraction of predators to herbivore-damaged plants (5). However, only few studies on indirect plant defense have considered plants attacked by multiple herbivore species (13-15), whereas this is a widespread phenomenon in nature (16,17). This is especially interesti...

Summary1. Plants face threats from a variety of herbivorous insects and can use induced responses to defend themselves against these attackers. Induced responses are mediated by signal transduction involving phytohormones, such as jasmonic acid (JA) and salicylic acid (SA). Cross-talk between signal transduction pathways triggered by attackers with contrasting feeding styles allows plants to fine-tune defences. A central question in this emerging field is to understand how responses to single attackers interfere with responses to other attackers, especially by integratively addressing molecular and ecological aspects. 2. We examined the plant-mediated interactions between the leaf-chewing Pieris brassicae and the phloem-sucking Brevicoryne brassicae, and their respective parasitoids Cotesia glomerata and Diaeretiella rapae, when feeding simultaneously, sequentially or in isolation on the brassicaceous ecological model plant Brassica oleracea. We analysed the underlying defence mechanisms in the plant. Levels of the phytohormones JA and SA transcriptional responses of a number of selected defence-related genes and secondary plant compounds were quantified at different time points during the single and multiple infestations. 3. The caterpillars developed faster and reached a larger body mass on plants previously attacked by aphids. Aphids initially developed faster on plants with caterpillars, although the moment of moulting to adults was independent of the presence of caterpillars. Both parasitoid species performed better under multiple-infestation scenarios than in single-herbivore situations. 4. On plants attacked by aphids, the JA levels were tenfold lower than on undamaged plants or plants with caterpillars. Additionally, the low transcript levels of LOX and MYC, genes coding for a JA biosynthesis-related enzyme and a transcription factor, respectively, in aphid-infested plants, suggest that the facilitation of the caterpillar performance was mediated by interference in signal transduction. Levels of carbon and nitrogen and secondary plant compounds (glucosinolates) did not differ significantly between treatments, suggesting that these compounds did not mediate the facilitation. 5. Our data show that the leaf chewer and phloem feeder asymmetrically interact not via competition as would be expected from interspecific herbivores but instead via facilitation; the phloem feeder attenuated JA-related plant defences, thus facilitating the growth and development of the leaf chewers. In linear bitrophic systems, interactions between JA and SA signalling pathways have been proposed to allow plants to fine-tune their defences, but if facilitation frequently occurs in interspecific interguild interactions among herbivores this may represent an important constraint for plant defences. Such a constraint might be reduced if, as in our model system, parasitoids also benefit from interactions between interguild hosts and nonhosts, but parasitoids are rarely considered in model molecular systems to assess the impact of herbiv...

Metabolic syndrome (MetS), characterized as obesity, insulin resistance, and non-alcoholic fatty liver diseases (NAFLD), is associated with vitamin D insufficiency/deficiency in epidemiological studies, while the underlying mechanism is poorly addressed. On the other hand, disorder of gut microbiota, namely dysbiosis, is known to cause MetS and NAFLD. It is also known that systemic inflammation blocks insulin signaling pathways, leading to insulin resistance and glucose intolerance, which are the driving force for hepatic steatosis. Vitamin D receptor (VDR) is highly expressed in the ileum of the small intestine, which prompted us to test a hypothesis that vitamin D signaling may determine the enterotype of gut microbiota through regulating the intestinal interface. Here, we demonstrate that high-fat-diet feeding (HFD) is necessary but not sufficient, while additional vitamin D deficiency (VDD) as a second hit is needed, to induce robust insulin resistance and fatty liver. Under the two hits (HFD+VDD), the Paneth cell-specific alpha-defensins including α-defensin 5 (DEFA5), MMP7 which activates the pro-defensins, as well as tight junction genes, and MUC2 are all suppressed in the ileum, resulting in mucosal collapse, increased gut permeability, dysbiosis, endotoxemia, systemic inflammation which underlie insulin resistance and hepatic steatosis. Moreover, under the vitamin D deficient high fat feeding (HFD+VDD), Helicobacter hepaticus, a known murine hepatic-pathogen, is substantially amplified in the ileum, while Akkermansia muciniphila, a beneficial symbiotic, is diminished. Likewise, the VD receptor (VDR) knockout mice exhibit similar phenotypes, showing down regulation of alpha-defensins and MMP7 in the ileum, increased Helicobacter hepaticus and suppressed Akkermansia muciniphila. Remarkably, oral administration of DEFA5 restored eubiosys, showing suppression of Helicobacter hepaticus and increase of Akkermansia muciniphila in association with resolving metabolic disorders and fatty liver in the HFD+VDD mice. An in vitro analysis showed that DEFA5 peptide could directly suppress Helicobacter hepaticus. Thus, the results of this study reveal critical roles of a vitamin D/VDR axis in optimal expression of defensins and tight junction genes in support of intestinal integrity and eubiosis to suppress NAFLD and metabolic disorders.