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Insect-associated bacteria can mediate the intersection of insect and plant immunity. In this study, we aimed to evaluate the effects of single isolates or communities of gut-associated bacteria of Helicoverpa zea larvae on herbivore-induced defenses in tomato. We first identified bacterial isolates from the regurgitant of field-collected H. zea larvae by using a culture-dependent method and 16S rRNA gene sequencing. We identified 11 isolates belonging to the families Enterobacteriaceae, Streptococcaceae, Yersiniaceae, Erwiniaceae, and unclassified Enterobacterales. Seven different bacterial isolates, namely Enterobacteriaceae-1, Lactococcus sp., Klebsiella sp. 1, Klebsiella sp. 3, Enterobacterales, Enterobacteriaceae-2, and Pantoea sp., were selected based on their phylogenetic relationships to test their impacts on insect-induced plant defenses. We found that the laboratory population of H. zea larvae inoculated with individual isolates did not induce plant anti-herbivore defenses, whereas larvae inoculated with a bacterial community (combination of the 7 bacterial isolates) triggered increased polyphenol oxidase (PPO) activity in tomato, leading to retarded larval development. Additionally, field-collected H. zea larvae with an unaltered bacterial community in their gut stimulated higher plant defenses than the larvae with a reduced gut microbial community. In summary, our findings highlight the importance of the gut microbial community in mediating interactions between herbivores and their host plants. [ABSTRACT FROM AUTHOR]

Interactions between plants and natural enemies of insect herbivores influence plant productivity and survival by reducing herbivory. Plants attract natural enemies via herbivore‐induced plant volatiles (HIPVs), but how water availability (WA) influences HIPV‐mediated defences is unclear.We use tomato, Solanum lycopersicum, tomato fruitworm, Helicoverpa zea and two natural enemies, the parasitoid wasp, Microplitis croceipes and the predator spined soldier bug, Podisus maculiventris, to investigate the effect of WA on HIPV emission dynamics and associated plant defence.We show that low WA initially increases total HIPV emission by tomato on the first day of herbivore exposure and, in contrast, reduces HIPV emission on the second day. Low WA enhances HIPVs that are mostly found in tomato trichomes. Notably, some volatiles inhibited by low WA are known attractants of natural enemies. Evidence from Y‐tube and in‐cage behavioural assays indicates that changes in HIPV emissions by low WA compromise the ability of tomato plants to attract natural enemies.Synthesis. Based on our results, we propose a hypothesis where plants respond to low WA by enhancing repellent HIPV emissions and reducing the emission of HIPVs that attract natural enemies, which disrupts natural enemy‐mediated plant indirect defences, but enhances plant direct defence against herbivores. [ABSTRACT FROM AUTHOR]

Local adaptations of host plants to climatic conditions along an elevation gradient can affect insect-plant interactions. Using local accessions sampled from different elevations within South America, plant defense responses and herbivore growth were evaluated on two host plants: a) cherry tomato, Solanum lycopersicum var. cerasiforme, and b) wild tomato, Solanum pimpinellifolium. The elevational origin of the accessions ranged from 100 to 3000 m above sea level. We hypothesized a higher level of defensive compounds in plants originating from lower elevations and, consequently, stronger resistance to insect herbivory. Interestingly, plant resistance to insect herbivory, as demonstrated by a reduction in Helicoverpa zea growth, was stronger for middle and high-elevation accessions. Total phenolic content increased with elevation in both herbivore-damaged and undamaged leaves, augmenting plant resistance. However, an elevational gradient was not evident for plant defensive proteins (polyphenol oxidase and trypsin protease inhibitors) or the density of leaf trichomes. Tradeoffs between constitutive and induced defenses were evident in both tomato genotypes. Future studies should test the role of plasticity in plant defense systems in restricting or facilitating range expansion of insect herbivores with climate change. [ABSTRACT FROM AUTHOR]

Summary: Herbivore‐induced plant volatiles (HIPVs) are widely recognized as an ecologically important defensive response of plants against herbivory. Although the induction of this 'cry for help' has been well documented, only a few studies have investigated the inhibition of HIPVs by herbivores and little is known about whether herbivores have evolved mechanisms to inhibit the release of HIPVs.To examine the role of herbivore effectors in modulating HIPVs and stomatal dynamics, we conducted series of experiments combining pharmacological, surgical, genetic (CRISPR‐Cas9) and chemical (GC‐MS analysis) approaches.We show that the salivary enzyme, glucose oxidase (GOX), secreted by the caterpillar Helicoverpa zea on leaves, causes stomatal closure in tomato (Solanum lycopersicum) within 5 min, and in both tomato and soybean (Glycine max) for at least 48 h. GOX also inhibits the emission of several HIPVs during feeding by H. zea, including (Z)‐3‐hexenol, (Z)‐jasmone and (Z)‐3‐hexenyl acetate, which are important airborne signals in plant defenses.Our findings highlight a potential adaptive strategy where an insect herbivore inhibits plant airborne defenses during feeding by exploiting the association between stomatal dynamics and HIPV emission. [ABSTRACT FROM AUTHOR]

Silicon (Si) is a beneficial mineral that enhances plant protection against abiotic and biotic stresses, including insect herbivores. Si increases mechanical and biochemical defenses in a variety of plant species. However, the use of Si in agriculture remains poorly adopted despite its widely documented benefits in plant health. In this study, we tested the effect of Si supplementation on the induction of plant resistance against a chewing herbivore in crops with differential ability to accumulate this element. Our model system comprised the generalist herbivore fall armyworm (FAW) Spodoptera frugiperda and three economically important plant species with differential ability to uptake silicon: tomato (non-Si accumulator), soybean, and maize (Si-accumulators). We investigated the effects of Si supply and insect herbivory on the induction of physical and biochemical plant defenses, and herbivore growth using potted plants in greenhouse conditions. Herbivory and Si supply increased peroxidase (POX) activity and trichome density in tomato, and the concentration of phenolics in soybean. Si supplementation increased leaf Si concentration in all plants. Previous herbivory affected FAW larval weight gain in all plants tested, and the Si treatment further reduced weight gain of larvae fed on Si accumulator plants. Notably, our results strongly suggest that non-glandular trichomes are important reservoirs of Si in maize and may increase plant resistance to chewing herbivores. We conclude that Si offers transient resistance to FAW in soybean, and a more lasting resistance in maize. Si supply is a promising strategy in management programs of chewing herbivores in Si-accumulator plants. [ABSTRACT FROM AUTHOR]

Plants growing under reduced water availability can affect insect herbivores differently, in some instances benefitting them. However, the forces mediating these positive impacts remain mostly unclear. To identify how water availability impacts plant quality and multi-trophic interactions, we conducted manipulative field studies with two populations of the specialist herbivore Pieris rapae, and its host plant, Rorippa indica. We found that P. rapae larvae experienced higher survival on R. indica growing under low water availability compared with plants grown under high water availability. Higher survival of eggs and larvae was related to the reduced abundance of other herbivores and natural enemies. Water availability had differential impacts on other members of the herbivore community by altering plant quality. Low water availability decreased the quality of R. indica to most herbivores, as indicated by reduced abundance in the field and decreased relative growth rate in laboratory feeding assays. In contrast, P. rapae larval performance was not affected by sympatric R. indica grown under different water availability. These results indicate that local P. rapae populations possess physiological adaptations to overcome fluctuations in host quality. Our findings illustrate that reduced water availability is beneficial to a specialist herbivore but detrimental to most other herbivores. Our work highlights the complex effects of the arthropod communities associated with plants in determining the impacts of water availability on insect herbivores. [ABSTRACT FROM AUTHOR]

Animals have ubiquitous associations with microorganisms, but microbial community composition and population dynamics can vary depending upon many environmental factors, including diet. The bacterial communities present in caterpillar (Lepidoptera) guts are highly variable, even among individuals of a species. Across lepidopteran species, it is unclear if the variation in their gut bacterial communities is due to ingested bacteria with diets or responses of gut bacteria to their diet. In this study, we aimed to understand whether bacteria establish and persist in the lepidopteran gut or just pass through the gut with food. We also examined whether bacterial establishment in lepidopteran guts depended on diet. We conducted a series of experiments using axenic and gnotobiotic insect rearing methods to address these objectives. We found that bacteria were established and maintained without replacement through the larval instars of the fall armyworm (Spodoptera frugiperda) and corn earworm (Helicoverpa zea). Gut bacterial titers increased when larvae were fed gamma-irradiated corn leaves but decreased when fed a wheat germ artificial diet. However, bacterial titers of larvae fed on a pinto bean artificial diet were similar to those consuming intact plants. We also observed that microbial titers of fall armyworm and other folivorous larvae were positively related to the host body size throughout larval development. Collectively, these results suggest that the populations of bacteria present in caterpillar guts are not simply a transient community passing through the system, but rather are a dynamic component of the caterpillar gut. Sensitivity of bacterial populations to the type of diet fed to lepidopterans suggests that not all diets are equally useful for reducing variance in community structure and interpreting insect-microbe interactions. [ABSTRACT FROM AUTHOR]

Colorado potato beetle (CPB; Leptinotarsa decemlineata) has been detected in Xinjiang, China, since 1993 and has caused serious damage to potato production during its eastward expansion to new geographic ranges. Symbiotic bacteria often play an essential role for insects to exploit novel food sources and expand into otherwise inaccessible ecological niches. An important yet unresolved question is whether herbivore populations from different geographic ranges have distinct or equal abilities to adapt to plant-induced defenses. We examined whether two geographic CPB populations collected from Urumqi and Ili varied in triggering induced defenses in potato plants, and the results demonstrated that plants damaged by Ili CPB larvae showed higher levels/activities of the defensive protein polyphenol oxidase (PPO) than those damaged by Urumqi CPB larvae. Intriguingly, application of oral secretions (OS) from Ili CPB larvae triggered higher PPO activity in potato compared with the treatments by OS collected from Urumqi larvae. Moreover, higher counts of bacterial colonies were observed in Urumqi CPB larvae by traditional culturing and quantitative PCR. Comparing the gut bacterial composition of CPB individuals by 16S rRNA amplicon sequencing also revealed higher abundance and diversity of gut-associated bacteria in the Urumqi population than that in the Ili population. These results indicate that the gut bacteria of CPB larvae were geographically shaped during the process of invasion, which played an important role in mediating plant–insect interactions and possesses a great potential to drive further invasion. [ABSTRACT FROM AUTHOR]

Microplitis croceipes is a solitary parasitoid that specializes on noctuid larvae of Helicoverpa zea and Heliothis virescens. Both the parasitoid and its hosts are naturally distributed across a large part of North America. When parasitoids deposit their eggs into hosts, venom and polydnaviruses (PDVs) are also injected into the caterpillars, which can suppress host immune responses, thus allowing parasitoid larvae to develop. In addition, PDVs can regulate host oral cues, such as glucose oxidase (GOX). The purpose of this study was to determine if parasitized caterpillars differentially induce plant defenses compared to non-parasitized caterpillars using two different caterpillar host/plant systems. Heliothis virescens caterpillars parasitized by M. croceipes had significantly lower salivary GOX activity than non-parasitized caterpillars, resulting in lower levels of tomato defense responses, which benefited parasitoid performance by increasing the growth rate of parasitized caterpillars. In tobacco plants, parasitized Helicoverpa zea caterpillars had lower GOX activity but induced higher plant defense responses. The higher tobacco defense responses negatively affected parasitoid performance by reducing the growth rate of parasitized caterpillars, causing longer developmental periods, and reduced cocoon mass and survival of parasitoids. These studies demonstrate a species-specific effect in different plant-insect systems. Based on these results, plant perception of insect herbivores can be affected by parasitoids and lead to positive or negative consequences to higher trophic levels depending upon the particular host-plant system. [ABSTRACT FROM AUTHOR]

Plants possess a suite of traits that make them challenging to consume by insect herbivores. Plant tissues are recalcitrant, have low levels of protein, and may be well defended by chemicals. Insects use diverse strategies for overcoming these barriers, including co‐opting metabolic activities from microbial associates. In this review, we discuss the co‐option of bacteria and fungi in the herbivore gut. We particularly focus upon chewing, folivorous insects (Coleoptera and Lepidoptera) and discuss the impacts of microbial co‐option on herbivore performance and plant responses. We suggest that there are two components to microbial co‐option: fixed and plastic relationships. Fixed relationships are involved in integral dietary functions and can be performed by microbial enzymes co‐opted into the genome or by stably transferred associates. In contrast, the majority of gut symbionts appear to be looser and perform more facultative, context‐dependent functions. This more plastic, variable co‐option of bacteria likely produces a greater number of insect phenotypes, which interact differently with plant hosts. By altering plant detection of herbivory or mediating insect interactions with plant defensive compounds, microbes can effectively improve herbivore performance in real time within and between generations. [ABSTRACT FROM AUTHOR]

Plants can influence the effectiveness of microbial insecticides through numerous mechanisms. One of these mechanisms is the oxidation of plant phenolics by plant enzymes, such as polyphenol oxidases (PPO) and peroxidases (POD). These reactions generate a variety of products and intermediates that play important roles in resistance against herbivores. Oxidation of the catecholic phenolic compound chlorogenic acid by PPO enhances the lethality of the insect-killing bacterial pathogen, Bacillus thuringiensis var. kurstaki (Bt) to the polyphagous caterpillar, Helicoverpa zea. Since herbivore feeding damage often triggers the induction of higher activities of oxidative enzymes in plant tissues, here we hypothesized that the induction of plant defenses would enhance the lethality of Bt on those plants. We found that the lethality of a commercial formulation of Bt (Dipel® PRO DF) on tomato plants was higher if it was applied to plants that were induced by H. zea feeding or induced by the phytohormone jasmonic acid. Higher proportions of H. zea larvae killed by Bt were strongly correlated with higher levels of PPO activity in the leaflet tissue. Higher POD activity was only weakly associated with higher levels of Bt-induced mortality. While plant-mediated variation in entomopathogen lethality is well known, our findings demonstrate that plants can induce defensive responses that work in concert with a microbial insecticide/entomopathogen to protect against insect herbivores. [ABSTRACT FROM AUTHOR]

Summary: The underlying adaptive mechanisms by which insect strains are associated with specific plants are largely unknown. In this study, we investigated the role of herbivore‐induced defenses in the host plant association of fall armyworm (Spodoptera frugiperda) strains. We tested the expression of herbivore‐induced defense‐related genes and the activity of plant‐defensive proteins in maize and Bermuda grass upon feeding by fall armyworm strains. The rice strain caterpillars induced greater accumulation of proteinase inhibitors in maize than the corn strain caterpillars. In Bermuda grass, feeding by the corn strain suppressed induction of trypsin inhibitor activity whereas the rice strain induced greater activity levels. Differences in elicitation of these plant defenses by the two strains seems to be due to differences in the activity levels of the salivary enzyme phospholipase C. The levels of plant defense responses were negatively correlated with caterpillar growth, indicating a fitness effect. Our results indicate that specific elicitors in the saliva of fall armyworm stains trigger differential levels of plant defense responses that affect caterpillar growth and thus may influence host plant associations in field conditions. The composition and secretion of plant defense elicitors may have a strong influence in the host plant association of insect herbivores. [ABSTRACT FROM AUTHOR]

The perception of herbivory by plants is known to be triggered by the deposition of insect-derived factors such as saliva and oral secretions, oviposition materials, and even feces. Such insect-derived materials harbor chemical cues that may elicit herbivore and/or pathogen-induced defenses in plants. Several insect-derived molecules that trigger herbivore-induced defenses in plants are known; however, insect-derived molecules suppressing them are largely unknown. In this study, we identified two plant chitinases from fall armyworm (Spodoptera frugiperda) larval frass that suppress herbivore defenses while simultaneously inducing pathogen defenses in maize (Zea mays). Fall armyworm larvae feed in enclosed whorls of maize plants, where frass accumulates over extended periods of time in close proximity to damaged leaf tissue. Our study shows that maize chitinases, Pr4 and Endochitinase A, are induced during herbivory and subsequently deposited on the host with the feces. These plant chitinases mediate the suppression of herbivore-induced defenses, thereby increasing the performance of the insect on the host. Pr4 and Endochitinase A also trigger the antagonistic pathogen defense pathway in maize and suppress fungal pathogen growth on maize leaves. Frass-induced suppression of herbivore defenses by deposition of the plant-derived chitinases Pr4 and Endochitinase A is a unique way an insect can co-opt the plant's defense proteins for its own benefit. It is also a phenomenon unlike the induction of herbivore defenses by insect oral secretions in most host-herbivore systems. [ABSTRACT FROM AUTHOR]

Induced plant defenses in response to herbivore attack are modulated by cross-talk between jasmonic acid (JA)- and salicylic acid (SA)-signaling pathways. Oral secretions from some insect herbivores contain effectors that overcome these antiherbivore defenses. Herbivores possess diverse microbes in their digestive systems and these microbial symbionts can modify plant-insect interactions; however, the specific role of herbivore-associated microbes in manipulating plant defenses remains unclear. Here, we demonstrate that Colorado potato beetle (Leptinotarsa decem-lineata) larvae exploit bacteria in their oral secretions to suppress antiherbivore defenses in tomato (Solarium lycopersicum). We found that antibiotic-untreated larvae decreased production of JA and JA-responsive antiherbivore defenses, but increased SA accumulation and SA-responsive gene expression. Beetles benefit from down-regulating plant defenses by exhibiting enhanced larval growth. In SA-deficient plants, suppression was not observed, indicating that suppression of JA-regulated defenses depends on the SA-signaling pathway. Applying bacteria isolated from larval oral secretions to wounded plants confirmed that three microbial symbionts belonging to the genera Stenotrophomonas, Pseudo-monas, and Enterobacter are responsible for defense suppression. Additionally, reinoculation of these bacteria to antibiotic-treated larvae restored their ability to suppress defenses. Flagellin isolated from Pseudomonas sp. was associated with defense suppression. Our findings show that the herbivore exploits symbiotic bacteria as a decoy to deceive plants into incorrectly perceiving the threat as microbial. By interfering with the normal perception of herbivory, beetles can evade antiherbivore defenses of its host. [ABSTRACT FROM AUTHOR]

Defense priming is defined as increased readiness of defense induction. A growing body of literature indicates that plants (or intact parts of a plant) are primed in anticipation of impending environmental stresses, both biotic and abiotic, and upon the following stimulus, induce defenses more quickly and strongly. For instance, some plants previously exposed to herbivore-inducible plant volatiles ( HIPVs) from neighboring plants under herbivore attack show faster or stronger defense activation and enhanced insect resistance when challenged with secondary insect feeding. Research on priming of antiherbivore defense has been limited to the HIPV-mediated mechanism until recently, but significant advances were made in the past three years, including non- HIPV-mediated defense priming, epigenetic modifications as the molecular mechanism of priming, and others. It is timely to consider the advances in research on defense priming in the plant-insect interactions. [ABSTRACT FROM AUTHOR]

Insect oviposition on plants frequently precedes herbivory. Accumulating evidence indicates that plants recognize insect oviposition and elicit direct or indirect defenses to reduce the pressure of future herbivory. Most of the ovipositiontriggered plant defenses described thus far remove eggs or keep them away from the host plant or their desirable feeding sites. Here, we report induction of antiherbivore defense by insect oviposition which targets newly hatched larvae, not the eggs, in the system of tomato Solanum lycopersicum L., and tomato fruitworm moth Helicoverpa zea Boddie. When tomato plants were oviposited by H. zea moths, pin2, a highly inducible gene encoding protease inhibitor2, which is a representative defense protein against herbivorous arthropods, was expressed at significantly higher level at the oviposition site than surrounding tissues, and expression decreased with distance away from the site of oviposition. Moreover, more eggs resulted in higher pin2 expression in leaves, and both fertilized and unfertilized eggs induced pin2 expression. Notably, when quantified daily following deposition of eggs, pin2 expression at the oviposition site was highest just before the emergence of larvae. Furthermore, H. zea oviposition primed the wound-induced increase of pin2 transcription and a burst of jasmonic acid (JA); tomato plants previously exposed to H. zea oviposition showed significantly stronger induction of pin2 and higher production of JA upon subsequent simulated herbivory than without oviposition. Our results suggest that tomato plants recognize H. zea oviposition as a signal of impending future herbivory and induce defenses to prepare for this herbivory by newly hatched neonate larvae. [ABSTRACT FROM AUTHOR]

Although five different classes of insect herbivore-produced elicitors of plant volatiles have been identified, this is only a part of the complex, chemically mediated interactions between insect herbivores and their host plants. The defensive reactions of the plant, following physical injury by the herbivore, are influenced by a multitude of factors including, but not necessarily limited to, the elicitors and numerous other herbivore-associated molecules, as well as microbes on the plant surface that may alter plant defensive pathways. Ultimately, a thorough and accurate understanding of the chemical ecology of insect–plant interactions will require a more holistic approach, taking into consideration the ecological and physiological context in which a plant perceives and responds to herbivore-associated signals. [Copyright &y& Elsevier]

Abstract: Our understanding of induced resistance against herbivores has grown immeasurably during the last several decades. Based upon the emerging literature, we argue that induced resistance represents a continuum of phenotypes that is determined by the plant’s ability to integrate multiple suites of signals of plant and herbivore origin. We present a model that illustrates the range of signals arising from early detection through herbivore feeding, and then through subsequent plant generations. [Copyright &y& Elsevier]

Stomata play a central role in plant responses to abiotic and biotic stresses. Existing knowledge regarding the roles of stomata in plant stress is centered on abiotic stresses and plant–pathogen interactions, but how stomata influence plant–herbivore interactions remains largely unclear. Here, we summarize the functions of stomata in plant–insect interactions and highlight recent discoveries of how herbivores manipulate plant stomata. Because stomata are linked to interrelated physiological processes in plants, herbivory-induced changes in stomatal dynamics might have cellular, organismic, and/or even community-level impacts. We summarize our current understanding of how stomata mediate plant responses to herbivory and environmental stimuli, propose how herbivores may influence these responses, and identify key knowledge gaps in plant–herbivore interactions. Plant stomata are emerging as important mediators of interactions between plants and herbivores. Several components in the oral secretions of herbivores, such as enzymes and phytohormones, that can trigger herbivory-induced stomatal closure have been identified. Recent evidence suggests that herbivory-induced stomatal changes play important roles in mediating interactions among plants, herbivores, pathogens, and the environment. [ABSTRACT FROM AUTHOR]

Chewing herbivores cause massive damage when crushing plant tissues with their mandibles, thus releasing a vast array of cues that may be perceived by the plant to mobilize defenses. Besides releasing damage cues in wounded tissues, herbivores deposit abundant cues from their saliva, regurgitant and feces that trigger herbivore specific responses in plants. Herbivores can manipulate the perception mechanisms and defense signals to suppress plant defenses by secreting effectors and/or by exploiting their associated oral microbes. Recent studies indicate that both the composition of herbivore cues and the plant's ability to recognize them are highly dependent upon the specific plant–herbivore system. There is a growing amount of work on identifying herbivore elicitors and effectors, but the most significant bottleneck in the discipline is the identification and characterization of plant receptors that perceive these herbivore-specific cues. [ABSTRACT FROM AUTHOR]

• Low water availability decreases plant tolerance to herbivory. • Low water availability increases plant resistance to herbivory. • Water availability causes physiological tradeoffs between plant defense strategies against herbivores. Water availability is an important factor that influences plant-insect interactions. While the influence of water limitation on plant resistance traits has received much attention, how water availability affects plant tolerance to herbivory is rarely tested. Here we show that lower water availability reduced tolerance capacity of tomato plants as measured by above ground regrowth and flower development after herbivory. In contrast to a reduced ability to tolerate herbivory, lower water availability increased the constitutive and induced levels of two defensive proteins, trypsin protease inhibitor and polyphenol oxidase, indicative of an increased investment on resistance under water limitation. The increase in defense proteins was paralleled with lower performance of a specialist caterpillar, Manduca sexta, and lower consumption of plant tissues. Although the performance of generalist, Helicoverpa zea , was unaffected by water availability, we observed a high mortality of H. zea that suggests strong resistance of tomato against H. zea. The findings revealed an unexpected case where water limitation decreases tolerance but increases resistance of a plant, suggesting a potential tradeoff between these strategies. This plasticity may benefit herbaceous plants by balancing growth and defense under variable water availability. [ABSTRACT FROM AUTHOR]