Root Herbivory Research Articles

Mycorrhizal‐herbivore interactions and the competitive release of subdominant tallgrass prairie species

Abstract Plant‐microbial‐herbivore interactions play a crucial role in the structuring and maintenance of plant communities and biodiversity, yet these relationships are complex. In grassland ecosystems, herbivores have the potential to greatly influence the survival, growth and reproduction of plants. However, few studies examine interactions of above‐ and below‐ground grazing and arbuscular mycorrhizal (AM) mycorrhizal symbiosis on plant community structure. We established experimental mesocosms containing an assemblage of eight tallgrass prairie grass and forb species in native prairie soil, maintained under mycorrhizal and nonmycorrhizal conditions, with and without native herbivorous soil nematodes, and with and without grasshopper herbivory. Using factorial analysis of variance and principal component analysis, we examined: (a) the independent and interacting effects of above‐ and below‐ground herbivores on AM symbiosis in tallgrass prairie mesocosms, (b) independent and interacting effects of above‐ and below‐ground herbivores and mycorrhizal fungi on plant community structure and (c) potential influences of mycorrhizal responsiveness of host plants on herbivory tolerance and concomitant shifts in plant community composition. Treatment effects were characterized by interactions between AM fungi and both above‐ground and below‐ground herbivores, while herbivore effects were additive. The dominance of mycorrhizal‐dependent C4 grasses in the presence of AM symbiosis was increased (p < 0.0001) by grasshopper herbivory but reduced (p < 0.0001) by nematode herbivory. Cool‐season C3 grasses exhibited a competitive release in the absence of AM symbiosis but this effect was largely reversed in the presence of grasshopper herbivory. Forbs showed species‐specific responses to both AM fungal inoculation and the addition of herbivores. Biomass of the grazing‐avoidant, facultatively mycotrophic forb Brickellia eupatorioides increased (p < 0.0001) in the absence of AM symbiosis and with grasshopper herbivory, while AM‐related increases in the above‐ground biomass of mycorrhizal‐dependent forbs Rudbeckia hirta and Salvia azurea were eradicated (p < 0.0001) by grasshopper herbivory. In contrast, nematode herbivory enhanced (p = 0.001) the contribution of Salvia azurea to total biomass. Synthesis. Our research indicates that arbuscular mycorrhizal symbiosis is the key driver of dominance of C4 grasses in the tallgrass prairie, with foliar and root herbivory being two mechanisms for maintenance of plant diversity.

Desiccation of undamaged grasses in the topsoil causes Namibia’s fairy circles – Response to Jürgens & Gröngröft (2023)

In a novel study, Getzin et al. (2022) have excavated 500 grasses at four regions of the Namib to systematically investigate the temporal process of how the young grasses die in fairy circles. Based on measurements of the root lengths, statistical testing, and comparative photo documentations the authors showed that sand termite herbivory did not cause the death of the freshly germinated grasses within fairy circles (FCs). Roots of those dead grasses were initially undamaged and even longer than those of the living grasses outside in the vegetation matrix, which is contrary to termite herbivory. The dying annual grasses within FCs had significantly higher root-to-shoot ratios than the vital grasses in the matrix, both of which can be attributed to the same grass-triggering rain event. This indicates that they died from water stress because the desiccating grasses invested biomass resources into roots, trying to reach the deeper soil layers with more moisture, but they failed.Jürgens and Gröngröft (2023) commented on our research findings. Here, we shed light on their statements by investigating the existing data evidence on the Namib fairy circles, which includes a thorough literature review about the proposed termite-feeding mechanism, as well as describing the properties of soil water within and around the FCs. Our review shows that there is no single study to date that has demonstrated with systematic field evidence in the form of root measurements and data from several regions of the Namib that the green germinating grasses within the FCs would be killed by root herbivory of sand termites.We emphasize that the top 10 cm of soil in the FCs is very susceptible to drying out. In this topsoil layer, the freshly germinated grasses with their 10 cm long roots die quickly after rainfall due to lack of water, because these small plants cannot reach and utilize the higher soil moisture content, which is only found in deeper soil layers below the dry topsoil. Based on 400 measurements of soil moisture during the rainy season 2024, we show that the topsoil in the FCs is significantly drier than in the matrix outside. Finally, we show that the soil physical conditions allow a very high hydraulic conductivity that supports the “uptake-diffusion feedback” during the first weeks after grass-triggering rainfall. During the first two weeks, the soil moisture at 20 cm depth ranged for several rainfall events between 9% and 18% within the FCs, hence way above the 6–8% threshold below which the hydraulic conductivity strongly declines. Even 20 days after rainfall, soil moisture was still above 8%. During this biologically active period, new grasses germinate after about five days, the large perennial grasses along the FC edge resprout and strongly draw water with their established root system at 20–30 cm depth, and the freshly germinated grasses in the FCs desiccate and die within 10–20 days. With our continuous soil moisture measurements, we argue that the quickly greening and competitively superior grasses on the FC edge, as well as the vital matrix grasses, draw soil water from the FCs. This rapid depletion of soil water and drying out of the topsoil leads to the death of the new grasses in the fairy circles.

Soil arthropod communities collected from agricultural soils influence wheat growth and modify phytohormone responses to aboveground herbivory in a microcosm experiment

Soil arthropods can affect plant growth and aboveground interactions directly via root herbivory and indirectly through nutrient cycling and interactions with soil microorganisms. Research on these effects of soil arthropods has focused on a few taxa within natural systems, largely neglecting agroecosystems and arthropod community-level effects. This study investigated the effects of soil arthropod communities from cereal-based agroecosystems on wheat plant growth and above-belowground interactions. Nutrient cycling and wheat growth were measured in a greenhouse microcosm experiment using field-collected agricultural soils from two rotational schemes with and without their soil arthropod communities. The effects of soil arthropods on aboveground phytohormones and colony growth of an aphid [Metopolophium festucae cerealium (Stroyan)] infesting the plants were measured. Wheat grown in soils with arthropod communities had significantly greater root (+ Arth mean: 0.15 ± 0.01 g; − Arth mean: 0.06 ± 0.01 g; F1,54 = 72.34, p < 0.001) and shoot biomass (+ Arth mean: 0.39 ± 0.03 g; − Arth mean: 0.24 ± 0.03 g; F1,54 = 17.61, p < 0.001), greater soil nitrate concentrations (+ Arth mean: 62.18 ± 4.76 mg NO3− - N kg−1 soil; − Arth mean: 13.06 ± 0.61 mg NO3− - N kg−1 soil; F1,54 = 99.89, p < 0.001), and altered root architecture compared to controls. Soil arthropod communities collected from the two rotational schemes differed significantly in abundance and diversity, but affected wheat growth similarly. Aphid colony growth (+ Arth mean: 30.50 ± 4.06; − Arth mean: 22.13 ± 3.36; χ21,27 = 21.19, p < 0.001), but not plant damage by aphids (+ Arth mean: 2.72 ± 0.17, − Arth mean: 2.69 ± 0.16; F1,27 = 0.02, p > 0.05), was significantly greater on wheat grown in soils with arthropods. Aphids, in turn, modified the effects of soil arthropods on root architecture and increased the abundance of soil arthropods. Wheat grown in soils with arthropods had increased levels of stress- and defense-related phytohormones in response to aphid herbivory, while phytohormones of wheat plants grown in soils without arthropods did not differ with aphid presence. Soil arthropod communities may help plants defend against herbivores aboveground by facilitating phytohormone induction while offsetting costs by increasing soil nutrients and modifying plant growth. By using taxonomically diverse field-collected soil arthropod communities from agroecosystems, this study showed that community-level effects on plant growth are more complex and dynamic than the effects of any single taxon, such as Collembola, illustrating that interactions within communities can produce emergent properties that alter the net effect of soil arthropods on plant growth. The results indicate that community-level effects of soil organisms should be considered as part of sustainable plant production and protection strategies.

Back to the 'roots' of research: a hypothesis-driven approach provides predictive understanding of plant-herbivore-microbe interactions.

This article is a Commentary on Böttner et al. (2023), 239: 1475–1489.

The Invasion of Alien Populations of Solanum elaeagnifolium in Two Mediterranean Habitats Modifies the Soil Communities in Different Ways.

We aimed to explore how the invasion of the alien plant Solanum elaeagnifolium affects soil microbial and nematode communities in Mediterranean pines (Pinus brutia) and maquis (Quercus coccifera). In each habitat, we studied soil communities from the undisturbed core of both formations and from their disturbed peripheral areas that were either invaded or not by S. elaeagnifolium. Most studied variables were affected by habitat type, while the effect of S. elaeagnifolium was different in each habitat. Compared to maquis, the soil in pines had higher silt content and lower sand content and higher water content and organic content, supporting a much larger microbial biomass (PLFA) and an abundance of microbivorous nematodes. The invasion of S. elaeagnifolium in pines had a negative effect on organic content and microbial biomass, which was reflected in most bacterivorous and fungivorous nematode genera. Herbivores were not affected. In contrast, in maquis, organic content and microbial biomass responded positively to invasion, raising the few genera of enrichment opportunists and the Enrichment Index. Most microbivores were not affected, while herbivores, mostly Paratylenchus, increased. The plants colonizing the peripheral areas in maquis probably offered a qualitative food source to microbes and root herbivores, which in pines was not sufficient to affect the much larger microbial biomass.

Tissue-specific plant toxins and adaptation in a specialist root herbivore

In coevolution between plants and insects, reciprocal selection often leads to phenotype matching between chemical defense and herbivore offense. Nonetheless, it is not well understood whether distinct plant parts are differentially defended and how herbivores adapted to those parts cope with tissue-specific defense. Milkweed plants produce a diversity of cardenolide toxins and specialist herbivores have substitutions in their target enzyme (Na+/K+-ATPase), each playing a central role in milkweed-insect coevolution. The four-eyed milkweed beetle (Tetraopes tetrophthalmus) is an abundant toxin-sequestering herbivore that feeds exclusively on milkweed roots as larvae and less so on milkweed leaves as adults. Accordingly, we tested the tolerance of this beetle's Na+/K+-ATPase to cardenolide extracts from roots versus leaves of its main host (Asclepias syriaca), along with sequestered cardenolides from beetle tissues. We additionally purified and tested the inhibitory activity of dominant cardenolides from roots (syrioside) and leaves (glycosylated aspecioside). Tetraopes' enzyme was threefold more tolerant of root extracts and syrioside than leaf cardenolides. Nonetheless, beetle-sequestered cardenolides were more potent than those in roots, suggesting selective uptake or dependence on compartmentalization of toxins away from the beetle's enzymatic target. Because Tetraopes has two functionally validated amino acid substitutions in its Na+/K+-ATPase compared to the ancestral form in other insects, we compared its cardenolide tolerance to that of wild-type Drosophila and CRISPR-edited Drosophila with Tetraopes' Na+/K+-ATPase genotype. Those two amino acid substitutions accounted for >50% of Tetraopes' enhanced enzymatic tolerance of cardenolides. Thus, milkweed's tissue-specific expression of root toxins is matched by physiological adaptations in its specialist root herbivore.

Diverse cropping systems lead to higher larval mortality of the cabbage root fly (Delia radicum)

Root herbivores pose a major threat to agricultural crops. They are difficult to control and their damage often goes unnoticed until the larvae reach their most devastating late instar stages. Crop diversification can reduce pest pressure, generally without compromising yield. We studied how different diversified cropping systems affected the oviposition and abundance of the specialist cabbage root fly Delia radicum, the most important root herbivore in Brassica crops. The cropping systems included a monoculture, pixel cropping, and four variations of strip cropping with varying intra- and interspecific crop diversity, fertilization and spatial configuration. Furthermore, we assessed whether there was a link between D. radicum and other macroinvertebrates associated with the same plants. Cabbage root fly oviposition was higher in strip cropping designs compared to the monoculture and was highest in the most diversified strip cropping design. Despite the large number of eggs, there were no consistent differences in the number of larvae and pupae between the cropping systems, indicative of high mortality of D. radicum eggs and early instars especially in the strip cropping designs. D. radicum larval and pupal abundance positively correlated with soil-dwelling predators and detritivores and negatively correlated with other belowground herbivores. We found no correlations between the presence of aboveground insect herbivores and the number of D. radicum on the roots. Our findings indicate that root herbivore presence is determined by a complex interplay of many factors, spatial configuration of host plants, and other organisms residing near the roots.

Natural rubber reduces herbivory and alters the microbiome below ground.

Laticifers are hypothesized to mediate both plant-herbivore and plant-microbe interactions. However, there is little evidence for this dual function. We investigated whether the major constituent of natural rubber, cis-1,4-polyisoprene, a phylogenetically widespread and economically important latex polymer, alters plant resistance and the root microbiome of the Russian dandelion (Taraxacum koksaghyz) under attack of a root herbivore, the larva of the May cockchafer (Melolontha melolontha). Rubber-depleted transgenic plants lost more shoot and root biomass upon herbivory than normal rubber content near-isogenic lines. Melolontha melolontha preferred to feed on artificial diet supplemented with rubber-depleted rather than normal rubber content latex. Likewise, adding purified cis-1,4-polyisoprene in ecologically relevant concentrations to diet deterred larval feeding and reduced larval weight gain. Metagenomics and metabarcoding revealed that abolishing biosynthesis of natural rubber alters the structure but not the diversity of the rhizosphere and root microbiota (ecto- and endophytes) and that these changes depended on M. melolontha damage. However, the assumption that rubber reduces microbial colonization or pathogen load is contradicted by four lines of evidence. Taken together, our data demonstrate that natural rubber biosynthesis reduces herbivory and alters the plant microbiota, which highlights the role of plant-specialized metabolites and secretory structures in shaping multitrophic interactions.

Density-Dependent Effects of Simultaneous Root and Floral Herbivory on Plant Fitness and Defense

Plants are attacked by multiple herbivores, and depend on a precise regulation of responses to cope with a wide range of antagonists. Simultaneous herbivory can occur in different plant compartments, which may pose a serious threat to plant growth and reproduction. In particular, plants often face co-occurring root and floral herbivory, but few studies have focused on such interactions. Here, we investigated in the field the combined density-dependent effects of root-chewing cebrionid beetle larvae and flower-chewing pierid caterpillars on the fitness and defense of a semiarid Brassicaceae herb. We found that the fitness impact of both herbivore groups was independent and density-dependent. Increasing root herbivore density non-significantly reduced plant fitness, while the relationship between increasing floral herbivore density and the reduction they caused in both seed number and seedling emergence was non-linear. The plant defensive response was non-additive with regard to the different densities of root and floral herbivores; high floral herbivore density provoked compensatory investment in reproduction, and this tolerance response was combined with aboveground chemical defense induction when also root herbivore density was high. Plants may thus prioritize specific trait combinations in response to varying combined below- and aboveground herbivore densities to minimize negative impacts on fitness.

Belowground crop responses to root herbivory are associated with the community structure of native arbuscular mycorrhizal fungi

There is growing interest in managing arbuscular mycorrhizal (AM) fungi in agriculture to support plant production. These fungi can support crop growth and nutrient uptake, but also affect plant-herbivore interactions. While our understanding of how AM fungi affect plant responses to herbivory advances, it is less clear how different naturally-occurring (native) fungal communities differentially influence crop responses to root-feeding insects.To explore this, plants (Sorghum bicolor) were grown in a glasshouse experiment without AM fungi (‘no AM fungi’) or with one of three natural soil inocula sourced either from a sclerophyll forest (‘forest inoculum’), a cropped field (‘field inoculum’), or a field in fallow (‘fallow inoculum’), while half the plants were subjected to a root herbivore (Dermolepida albohirtum). We assessed the effects of soil inoculum and root herbivory on root-colonising AM fungal diversity, plant growth, and nutrient content.Root herbivory did not affect AM fungal diversity or composition. Plants grown with the field or fallow inocula were both dominated by the genera Glomus and Claroideoglomus. These plants exhibited reduced biomass in response to inoculation, but were not impacted by root herbivory. In contrast, plants with the forest inoculum had AM fungal communities dominated by Paraglomus and Ambispora. When subjected to root herbivory, the forest inoculated plants and plants without AM fungi exhibited reductions of 44 % and 61 % in root biomass, and reductions of 65 % and 59 % in root phosphorus, respectively.Our study shows inoculation-driven plant responses to root herbivory that were associated with the community structure of their root-colonising AM fungi. Results suggest associations with communities dominated by Claroideoglomus and Glomus may mitigate the impacts of a root-feeding insect. More exploration of how natural assemblages of AM fungi mediate plant-herbivore interactions is needed if we are to effectively manage soil fungi in agriculture.

Silicon quantum dots promote radish resistance to root herbivores without impairing rhizosphere microenvironment health

Soil-applied silicon quantum dots (Si QDs) significantly increased radish taproot resistance against white grubs and simultaneously shaped a healthy rhizosphere microenvironment.

Soil contamination with potentially toxic elements and root herbivory: effects on root surface area and stem secondary xylem of young common beech (Fagus sylvatica L.)

Soil contamination with potentially toxic elements and root herbivory: effects on root surface area and stem secondary xylem of young common beech (Fagus sylvatica L.)

Specialist root herbivore modulates plant transcriptome and downregulates defensive secondary metabolites in a brassicaceous plant.

Summary Plants face attackers aboveground and belowground. Insect root herbivores can lead to severe crop losses, yet the underlying transcriptomic responses have rarely been studied.We studied the dynamics of the transcriptomic response of Brussels sprouts (Brassica oleracea var. gemmifera) primary roots to feeding damage by cabbage root fly larvae (Delia radicum), alone or in combination with aboveground herbivory by cabbage aphids (Brevicoryne brassicae) or diamondback moth caterpillars (Plutella xylostella). This was supplemented with analyses of phytohormones and the main classes of secondary metabolites; aromatic, indole and aliphatic glucosinolates.Root herbivory leads to major transcriptomic rearrangement that is modulated by aboveground feeding caterpillars, but not aphids, through priming soon after root feeding starts. The root herbivore downregulates aliphatic glucosinolates. Knocking out aliphatic glucosinolate biosynthesis with CRISPR‐Cas9 results in enhanced performance of the specialist root herbivore, indicating that the herbivore downregulates an effective defence.This study advances our understanding of how plants cope with root herbivory and highlights several novel aspects of insect–plant interactions for future research. Further, our findings may help breeders develop a sustainable solution to a devastating root pest.

Insecticide application did not reveal any impact of herbivory on plant roots in boreal forests

The levels of belowground herbivory in natural ecosystems remain practically undetermined, and nothing is known regarding the geographic and/or climatic variations in belowground herbivory. We endeavoured to narrow this knowledge gap by exploring the latitudinal changes in the intensity of background root herbivory in boreal forest ecosystems by conducting a herbivore exclusion experiment in 10 forested sites from 60°N to 69°N in northwestern Russia. We found no statistically significant differences in fine root biomass between diazinon-treated and control plots, nor did the differences show any latitudinal change. From biomass of root-feeding macrofauna we estimated that root herbivory in our sites averages 0.57 %. This low level of root herbivory could not be quantified reliably by herbivore exclusion experiments; therefore, we suggest that macroecological patterns in root herbivory are invoked from simultaneous measurements of the biomasses of fine roots and of root-feeders. More data on the efficiency of conversion of the food ingested by root-feeding invertebrates is needed to increase the accuracy of the suggested method of estimation of root herbivory.

Root herbivory reduces species richness and alters community structure of root-colonising arbuscular mycorrhizal fungi

Belowground insect herbivory is an important interaction that can shape ecological communities above- and belowground. A key component of belowground ecosystems are the arbuscular mycorrhizal (AM) fungi that associate with roots of most terrestrial plants. Despite the shared ecological significance of root herbivores and AM fungi, there is an absence of data on how insect root herbivory affects root-colonising AM fungal diversity. This study explored the impacts of root herbivory (from Dermolepida alborhirtum) on the diversity and community composition of AM fungi colonising plant roots (Dichanthium sericeum) and assessed the effects on plant growth and nutrient uptake. Belowground herbivory significantly altered AM fungal community structure and reduced species richness, potentially removing fungal taxa sensitive to root-herbivore disturbance. Meanwhile, herbivory also reduced root biomass and aboveground phosphorus. These findings demonstrate how belowground herbivores can directly shape AM fungal communities in plant roots.

Exploring interactions between Beauveria and Metarhizium strains through co-inoculation and responses of perennial ryegrass in a one-year trial.

Perennial ryegrass (Lolium perenne L.) possesses a high level of nutritional quality and is widely used as a forage species to establish permanent pastures in southern Chile. However, the productivity of most such pastures is limited by various environmental agents, such as insect pests and drought. In this context, our work stresses the need for elucidating the ability of fungal endophytes to establish interactions with plants, and to understand how these processes contribute to plant performance and fitness. Therefore, we evaluated the colonization and impact of two native strains of the endophytic insect-pathogenic fungus (EIPF) group isolated from permanent ryegrass pastures in southern Chile. Roots and seeds of ryegrass and scarabaeid larvae were collected from nine different ryegrass pastures in the Los Ríos region of southern Chile to specifically isolate EIPFs belonging to the genera Beauveria and Metarhizium. Fungal isolations were made on 2% water agar with antibiotics, and strains were identified by analyzing the entire internal transcribed spacer (ITS) 1-5.8S-ITS2 ribosomal DNA region. Four strains of Beauveria and 33 strains of Metarhizium were isolated only in scarabaeid larvae from ryegrass pastures across four sites. Experimental mini-pastures that were either not inoculated (control) or co-inoculated with conidia of the strains Beauveria vermiconia NRRL B-67993 (P55_1) and Metarhizium aff. lepidiotae NRRL B-67994 (M25_2) under two soil humidity levels were used. Ryegrass plants were randomly collected from the mini-pastures to characterize EIPF colonization in the roots by real-time PCR and fluorescence microscopy. Aboveground biomass was measured to analyze the putative impact of colonization on the mini-pastures’ aboveground phenotypic traits with R software using a linear mixed-effects model and the ANOVA statistical test. Seasonal variation in the relative abundance of EIPFs was observed, which was similar between both strains from autumn to spring, but different in summer. In summer, the relative abundance of both EIPFs decreased under normal moisture conditions, but it did not differ significantly under water stress. The aboveground biomass of ryegrass also increased from autumn to spring and decreased in summer in both the inoculated and control mini-pastures. Although differences were observed between moisture levels, they were not significant between the control and inoculated mini-pastures, except in July (fresh weight and leaf area) and October (dry weight). Our findings indicate that native strains of B. vermiconia NRRL B-67993 (P55_1) and M. aff. lepidiotae NRRL B-67994 (M25_2) colonize and co-exist in the roots of ryegrass, and these had little or no effect on the mini-pastures’ aboveground biomass; however, they could have other functions, such as protection against root herbivory by insect pests.

Leaf-chewing herbivores affect preference and performance of a specialist root herbivore

Plants interact with a diversity of phytophagous insects above- and belowground. By inducing plant defence, one insect herbivore species can antagonize or facilitate other herbivore species feeding on the same plant, even when they are separated in space and time. Through systemic plant-mediated interactions, leaf-chewing herbivores may affect the preference and performance of root-feeding herbivores. We studied how six different leaf-chewing herbivore species of Brassica oleracea plants affected oviposition preference and larval performance of the root-feeding specialist Delia radicum. We expected that female D. radicum flies would oviposit where larval performance was highest, in accordance with the preference–performance hypothesis. We also assessed how the different leaf-chewing herbivore species affected defence-related gene expression in leaves and primary roots of B. oleracea, both before and after infestation with the root herbivore. Our results show that leaf-chewing herbivores can negatively affect the performance of root-feeding D. radicum larvae, although the effects were relatively weak. Surprisingly, we found that adult D. radicum females show a strong preference to oviposit on plants infested with a leaf-chewing herbivore. Defence-related genes in primary roots of B. oleracea plants were affected by the leaf-chewing herbivores, but these changes were largely overridden upon local induction by D. radicum. Infestation by leaf herbivores makes plants more attractive for oviposition by D. radicum females, while decreasing larval performance. Therefore, our findings challenge the preference–performance hypothesis in situations where other herbivore species are present.

Flowers prepare thyselves: leaf and root herbivores induce specific changes in floral phytochemistry with consequences for plant interactions with florivores.

Summary The phenotypic plasticity of flowering plants in response to herbivore damage to vegetative tissues can affect plant interactions with flower‐feeding organisms. Such induced systemic responses are probably regulated by defence‐related phytohormones that signal flowers to alter secondary chemistry that affects resistance to florivores. Current knowledge on the effects of damage to vegetative tissues on plant interactions with florivores and the underlying mechanisms is limited.We compared the preference and performance of two florivores on flowering Brassica nigra plants damaged by one of three herbivores feeding from roots or leaves. To investigate the underlying mechanisms, we quantified expression patterns of marker genes for defence‐related phytohormonal pathways, and concentrations of phytohormones and glucosinolates in buds and flowers.Florivores displayed contrasting preferences for plants damaged by herbivores feeding on roots and leaves. Chewing florivores performed better on plants damaged by folivores, but worse on plants damaged by the root herbivore. Chewing root and foliar herbivory led to specific induced changes in the phytohormone profile of buds and flowers. This resulted in increased glucosinolate concentrations for leaf‐damaged plants, and decreased glucosinolate concentrations for root‐damaged plants.The outcome of herbivore–herbivore interactions spanning from vegetative tissues to floral tissues is unique for the inducing root/leaf herbivore and receiving florivore combination.

A Beneficial Plant-Associated Fungus Shifts the Balance toward Plant Growth over Resistance, Increasing Cucumber Tolerance to Root Herbivory.

Plants allocate their limited resources toward different physiological processes, dynamically adjusting their resource allocation in response to environmental changes. How beneficial plant-associated microbes influence this allocation is a topic that continues to interest plant biologists. In this study, we examined the effect of a beneficial fungus, Phialemonium inflatum, on investment in growth and anti-herbivore resistance traits in cucumber plants (Cucumis sativus). We inoculated cucumber seeds with P. inflatum spores and measured several growth parameters, including germination rate, above and belowground biomass, and number of flowers. We also examined plant resistance to adult and larval striped cucumber beetles (Acalymma vitattum), and quantified levels of defense hormones in leaves and roots. Our results indicate that P. inflatum strongly enhances cucumber plant growth and reproductive potential. Although fungus treatment did not improve plant resistance to cucumber beetles, inoculated plants were more tolerant to root herbivory, experiencing less biomass reduction. Together, these findings document how a beneficial plant-associated fungus shifts plant investment in growth over herbivore resistance, highlighting the importance of microbes in mediating plant-herbivore interactions. These findings also have important implications for agricultural systems, where beneficial microbes are often introduced or managed to promote plant growth or enhance resistance.

A beta-glucosidase of an insect herbivore determines both toxicity and deterrence of a dandelion defense metabolite.

Gut enzymes can metabolize plant defense compounds and thereby affect the growth and fitness of insect herbivores. Whether these enzymes also influence feeding preference is largely unknown. We studied the metabolization of taraxinic acid β-D-glucopyranosyl ester (TA-G), a sesquiterpene lactone of the common dandelion (Taraxacum officinale) that deters its major root herbivore, the common cockchafer larva (Melolontha melolontha). We have demonstrated that TA-G is rapidly deglucosylated and conjugated to glutathione in the insect gut. A broad-spectrum M. melolontha β-glucosidase, Mm_bGlc17, is sufficient and necessary for TA-G deglucosylation. Using cross-species RNA interference, we have shown that Mm_bGlc17 reduces TA-G toxicity. Furthermore, Mm_bGlc17 is required for the preference of M. melolontha larvae for TA-G-deficient plants. Thus, herbivore metabolism modulates both the toxicity and deterrence of a plant defense compound. Our work illustrates the multifaceted roles of insect digestive enzymes as mediators of plant-herbivore interactions.