RESUMEN
Caterpillar salivary glucose oxidase (GOX) can function as both an elicitor or as an effector of plant defense responses depending upon the system. Treatment with GOX reduces the stomatal aperture of tomato and soybean leaves, thereby reducing the emission of volatile organic compounds (VOCs), that are important indirect defense responses of plants by attracting natural enemies of the caterpillars. Here we examined the effect of fungal GOX (fungal glucose oxidases have been used to determine specificity in defense response elicitation) on stomatal closure of maize leaves and on the volatile emission pattern whole maize plants. We also used salivary gland homogenate from wild-type and CRISPR-Cas9 Helicoverpa zea mutants deficient in GOX activity to determine the effect caterpillar saliva with and without GOX had on maize volatile emission. Collecting volatiles at 2-hour intervals allowed us to examine the changes in emission over time. Fungal GOX reduced the stomatal aperture in maize leaves, which may have influenced the observed significant reduction in total green leaf volatile (GLV) emission. Furthermore, fungal GOX significantly increased the emission of several key terpenes: linalool, DMNT, and Z-ß-farnesene from maize, while salivary gland homogenate from wild type (WT; GOX+) H. zea increased the emission of α-pinene, ß-pinene, and ocimene compared to H. zea unable to synthesize GOX. This study addressed a significant knowledge gap about the effect of GOX on maize volatiles and provides a baseline for further research on the effect of GOX on the regulation of terpene synthase genes and their relation to terpene volatile emission.
Asunto(s)
Mariposas Nocturnas , Terpenos , Animales , Terpenos/farmacología , Zea mays/fisiología , Glucosa Oxidasa , Hojas de la PlantaRESUMEN
Insect herbivores face multiple challenges to their ability to grow and reproduce. Plants can produce a series of defenses that disrupt and damage the herbivore digestive system, which are heightened upon injury by insect feeding. Additionally, insects face threats from virulent microorganisms that can incur their own set of potential costs to hosts. Microorganisms that invade through the digestive system may function in concert with defenses generated by plants, creating combined assailments on host insects. In our study, we evaluated how tomato defenses interact with an enteric bacterial isolate, Serratia marcescens, in the corn earworm (Helicoverpa zea). We performed bioassays using different tomato cultivars that were induced by methyl jasmonate and larvae orally inoculated with a S. marcescens isolate. Untreated corn earworm larval mortality was low on constitutive tomato, while larvae inoculated with S. marcescens exhibited > 50% mortality within 5 days. Induction treatments elevated both control mortality (~ 45%) and in combination with S. marcescens (> 95%). Larvae also died faster when encountering induced defenses and Serratia. Using a tomato mutant, foliar polyphenol oxidase activity likely had stronger impacts on S. marcescens-mediated larval mortality. Induction treatments also elevated the number of bacterial colony-forming units in the hemolymph of larvae inoculated with Serratia. Larval mortality by S. marcescens was low (< 10%) on artificial diets. Our results demonstrate that plant chemical defenses enhance larval mortality from an opportunistic gut microbe. We propose that the combined damage from both the plant and microbial agent overwhelm the herbivore to increase mortality rates and expedite host death.
Asunto(s)
Mariposas Nocturnas , Solanum lycopersicum , Animales , Zea mays , Larva/microbiología , BacteriasRESUMEN
Insect guts often harbor an abundance of bacteria. Many of these members are commensal, but some may emerge as opportunistic pathogens when the host is under stress. In this study, we evaluated how dietary nutritional concentration mediates a shift from commensal to pathogenic, and if host species influences those interactions. We used the lepidopterans (Noctuidae) fall armyworm (Spodoptera frugiperda), beet armyworm (Spodoptera exigua), and corn earworm (Helicoverpa zea) as hosts and a Serratia strain initially isolated from healthy fall armyworm. Diet concentration was altered by bulk reduction in nutritional content with dilution using cellulose. Our experiments revealed that low nutrient diet increased mortality from Serratia for beet armyworm and corn earworm. However, for fall armyworm, little mortality was observed in any of the diet combinations. Dietary nutrition and oral inoculation with Serratia did not change the expression of two antimicrobial peptides in fall and beet armyworm, suggesting that other mechanisms that mediate mortality were involved. Our results have implications for how pathogens may persist as commensals in the digestive tract of insects. These findings also suggest that diet plays a very important role in the switch from commensal to pathogen. Finally, our data indicate that the host response to changing conditions is critical in determining if a pathogen may overtake its host and that these three lepidopteran species have different responses to opportunistic enteric pathogens.
Asunto(s)
Mariposas Nocturnas , Serratia , Animales , Celulosa , Dieta , Larva/fisiología , Spodoptera/microbiología , Zea maysRESUMEN
Gut microbiota can have diverse impacts on hosts, the nature of which often depend on the circumstances. For insect gut microbes, the quality and nature of host diets can be a significant force in swinging the pendulum from inconsequential to functionally important. In our study, we addressed whether beneficial microbes in one species impart similar functions to related species under identical conditions. Using fall armyworm (Spodoptera frugiperda), beet armyworm (Spodoptera exigua), and other noctuid hosts, we implemented an axenic rearing strategy and manipulated gut bacterial populations and dietary conditions. Our results revealed that some gut Enterococcus and Enterobacter isolates can facilitate utilization of a poor diet substrate by fall armyworm, but this was not the case for other more optimized diets. While Enterococcus provided benefits to fall armyworm, it was decidedly antagonistic to beet armyworm (Spodoptera exigua) under identical conditions. Unique isolates and bacterial introductions at early growth stages were critical to how both larval hosts performed. Our results provide robust evidence of the roles in which bacteria support lepidopteran larval growth, but also indicate that the directionality of these relationships can differ among congener hosts. IMPORTANCE Insects have intimate relationships with gut microbiota, where bacteria can contribute important functions to their invertebrate hosts. Lepidopterans are important insect pests, but how they engage with their gut bacteria and how that translates to impacts on the host are lacking. Here we demonstrate the facultative nature of gut microbiota in lepidopteran larvae and the importance of diet in driving mutualistic or antagonistic relationships. Using multiple lepidopteran species, we uncover that the same bacteria that can facilitate exploitation of a challenging diet in one host severely diminishes larval performance of another larval species. Additionally, we demonstrate the beneficial functions of gut microbiota on the hosts are not limited to one lineage, but rather multiple isolates can facilitate the exploitation of a suboptimal diet. Our results illuminate the context-dependent nature of the gut microbiomes in invertebrates, and how host-specific microbial engagement can produce dramatically different interactions.
Asunto(s)
Microbioma Gastrointestinal , Animales , Bacterias , Larva/microbiología , Spodoptera/microbiología , SimbiosisRESUMEN
Bacterial gut symbionts of insect herbivores can impact their host through different mechanisms. However, in most lepidopteran systems we lack experimental examples to explain how specific members of the gut bacterial community influence their host. We used fall armyworm (Spodoptera frugiperda) as a model system to address this objective. We implemented axenic and gnotobiotic techniques using two semi-artificial diets with pinto bean and wheat germ-based components. Following an initial screen of bacterial isolates representing different genera, larvae inoculated with Enterococcus FAW 2-1 exhibited increased body mass on the pinto bean diet, but not on the wheat germ diet. We conducted a systematic bioassay screening of Enterococcus isolated from fall armyworm, revealing they had divergent effects on the hosts' usage pinto bean diet, even among phylogenetically similar isolates. Dilution of the pinto bean diet revealed that larvae performed better on less-concentrated diets, suggesting the presence of a potential toxin. Collectively, these results demonstrate that some gut microorganisms of lepidopterans can benefit the host, but the dietary context is key towards understanding the direction of the response and magnitude of the effect. We provide evidence that gut microorganisms may play a wider role in mediating feeding breadth in lepidopteran pests, but overall impacts could be related to the environmental stress and the metabolic potentials of the microorganisms inhabiting the gut.
Asunto(s)
Bacterias , Dieta , Animales , Enterococcus , Larva/microbiología , Spodoptera/fisiologíaRESUMEN
Insects frequently confront different microbial assemblages. Bacteria inhabiting an insect gut are often commensal, but some can become pathogenic when the insect is compromised from different stressors. Herbivores are often confronted by various forms of plant resistance, but how defenses generate opportunistic microbial infections from residents in the gut are not well understood. In this study, we evaluated the pathogenic tendencies of Serratia isolated from the digestive system of healthy fall armyworm larvae (Spodoptera frugiperda) and how it interfaces with plant defenses. We initially selected Serratia strains that varied in their direct expression of virulence factors. Inoculation of the different isolates into the fall armyworm body cavity indicated differing levels of pathogenicity, with some strains exhibiting no effects while others causing mortality 24 h after injection. Oral inoculations of pathogens on larvae provided artificial diets caused marginal (< 7%) mortality. However, when insects were provided different maize genotypes, mortality from Serratia increased and was higher on plants exhibiting elevated levels of herbivore resistance (< 50% mortality). Maize defenses facilitated an initial invasion of pathogenic Serratia into the larval hemocoel¸ which was capable of overcoming insect antimicrobial defenses. Tomato and soybean further indicated elevated mortality due to Serratia compared to artificial diets and differences between plant genotypes. Our results indicate plants can facilitate the incipient emergence of pathobionts within gut of fall armyworm. The ability of resident gut bacteria to switch from a commensal to pathogenic lifestyle has significant ramifications for the host and is likely a broader phenomenon in multitrophic interactions facilitated by plant defenses.
Asunto(s)
Serratia , Zea mays , Animales , Herbivoria , Larva , SpodopteraRESUMEN
Koinobiont endoparasitoid wasps whose larvae develop inside a host insect alter several important facets of host physiology, potentially causing cascading effects across multiple trophic levels. For instance, the hijacking of the host immune responses may have effects on how insects interact with host plants and microbial associates. However, the parasitoid regulation of insect-plant-microbiome interactions is still understudied. In this study, we used the fall armyworm (FAW), Spodoptera frugiperda, and the braconid parasitoid Cotesia marginiventris to evaluate impacts of parasitism on the gut microbiome of FAW larvae, and respective maize plant defense responses. The level of reactive oxygen species and the microbial community in larval gut underwent significant changes in response to parasitism, leading to a significant reduction of Enterococcus, while elevating the relative abundance of Pseudomonas. FAW with parasitism had lower glucose oxidase (GOX) activity in salivary glands and triggered lower defense responses in maize plants. These changes corresponded to effects on plants, as Pseudomonas inoculated larvae had lower activity of salivary GOX and triggered lower defense responses in maize plants. Our results demonstrated that parasitism had cascading effects on microbial associates across trophic levels and also highlighted that insect gut bacteria may contribute to complex interrelationships among parasitoids, herbivores, and plants.
RESUMEN
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.
RESUMEN
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.
Asunto(s)
Mariposas Nocturnas , Compuestos Orgánicos Volátiles , Animales , Herbivoria , Insectos , Estomas de PlantasRESUMEN
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.
Asunto(s)
Dieta , Microbioma Gastrointestinal , Larva/microbiología , Spodoptera/microbiología , Animales , Bacterias/aislamiento & purificación , Interacciones Microbiota-Huesped , Larva/crecimiento & desarrollo , Spodoptera/crecimiento & desarrolloRESUMEN
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.
Asunto(s)
Mariposas Nocturnas/fisiología , Nicotiana/parasitología , Solanum lycopersicum/parasitología , Avispas/fisiología , Animales , Femenino , Glucosa Deshidrogenasas/metabolismo , Glucosa Oxidasa/metabolismo , Interacciones Huésped-Parásitos , Larva/metabolismo , Solanum lycopersicum/metabolismo , Oviposición/fisiología , Parásitos , Enfermedades de las Plantas/parasitología , Extractos Vegetales/química , Extractos Vegetales/metabolismo , Hojas de la Planta/química , Hojas de la Planta/metabolismo , Especificidad de la Especie , Nicotiana/metabolismoRESUMEN
Plants produce suites of defenses that can collectively deter and reduce herbivory. Many defenses target the insect digestive system, with some altering the protective peritrophic matrix (PM) and causing increased permeability. The PM is responsible for multiple digestive functions, including reducing infections from potential pathogenic microbes. In our study, we developed axenic and gnotobiotic methods for fall armyworm (Spodoptera frugiperda) and tested how particular members present in the gut community influence interactions with plant defenses that can alter PM permeability. We observed interactions between gut bacteria with plant resistance. Axenic insects grew more but displayed lower immune-based responses compared with those possessing Enterococcus, Klebsiella, and Enterobacter isolates from field-collected larvae. While gut bacteria reduced performance of larvae fed on plants, none of the isolates produced mortality when injected directly into the hemocoel. Our results strongly suggest that plant physical and chemical defenses not only act directly upon the insect, but also have some interplay with the herbivore's microbiome. Combined direct and indirect, microbe-mediated assaults by maize defenses on the fall armyworm on the insect digestive and immune system reduced growth and elevated mortality in these insects. These results imply that plant-insect interactions should be considered in the context of potential mediation by the insect gut microbiome.
Asunto(s)
Enterobacteriaceae/fisiología , Inmunidad de la Planta , Spodoptera/microbiología , Zea mays/inmunología , Zea mays/parasitología , Animales , Quitinasas/metabolismo , Genotipo , Herbivoria/fisiología , Interacciones Huésped-Patógeno , Spodoptera/crecimiento & desarrollo , Spodoptera/ultraestructura , Síndrome , Tricomas/metabolismo , Zea mays/genética , Zea mays/ultraestructuraRESUMEN
Insect herbivory induces plant defense responses that are often modulated by components in insect saliva, oral secretions or regurgitant, frass, or oviposition fluids. These secretions contain proteins and small molecules that act as elicitors or effectors of plant defenses. Several non-protein elicitors have been identified from insect oral secretions, whereas studies of insect saliva have focused mainly on protein identification. Yet, insect saliva may also contain non-protein molecules that could activate defense responses in plants. The goal of this study was to identify non-protein plant defense elicitors present in insect saliva. We used the fall armyworm (FAW), Spodoptera frugiperda and its host plants tomato, maize, and rice as a model system. We tested the effect of protein-digested saliva or non-protein components on herbivore-induced defense responses in maize, rice and tomato. We identified phytohormones in FAW saliva using high performance liquid chromatography coupled with mass spectrometry. The results of this study show that non-protein components in FAW saliva modulated defense responses in different plant species. The saliva of this insect contains benzoic acid, and the phytohormones jasmonic acid, salicylic acid, and abscisic acid at concentrations of <5 ng per µl of saliva. Plant treatment with similar phytohormone quantities detected in FAW saliva upregulated the expression of a maize proteinase inhibitor gene in maize, and down-regulated late herbivore-induced defenses in tomato plants. We conclude that FAW saliva is a complex fluid that, in addition to known enzymatic plant defense elicitors, contains phytohormones and other small molecules.
Asunto(s)
Reguladores del Crecimiento de las Plantas/análisis , Saliva/química , Zea mays/metabolismo , Animales , Cromatografía Líquida de Alta Presión , Regulación de la Expresión Génica de las Plantas/efectos de los fármacos , Herbivoria , Larva/metabolismo , Solanum lycopersicum/metabolismo , Solanum lycopersicum/parasitología , Espectrometría de Masas , Reguladores del Crecimiento de las Plantas/farmacología , Hojas de la Planta/metabolismo , Hojas de la Planta/parasitología , Proteínas de Plantas/genética , Proteínas de Plantas/metabolismo , Saliva/metabolismo , Spodoptera/crecimiento & desarrollo , Zea mays/parasitologíaRESUMEN
Obligate symbioses occur when organisms require symbiotic relationships to survive. Some parasitic wasps of caterpillars possess obligate mutualistic viruses called "polydnaviruses." Along with eggs, wasps inject polydnavirus inside their caterpillar hosts where the hatching larvae develop inside the caterpillar. Polydnaviruses suppress the immune systems of their caterpillar hosts, which enables egg hatch and wasp larval development. It is unknown whether polydnaviruses also manipulate the salivary proteins of the caterpillar, which may affect the elicitation of plant defenses during feeding by the caterpillar. Here, we show that a polydnavirus of the parasitoid Microplitis croceipes, and not the parasitoid larva itself, drives the regulation of salivary enzymes of the caterpillar Helicoverpa zea that are known to elicit tomato plant-defense responses to herbivores. The polydnavirus suppresses glucose oxidase, which is a primary plant-defense elicitor in the saliva of the H. zea caterpillar. By suppressing plant defenses, the polydnavirus allows the caterpillar to grow at a faster rate, thus improving the host suitability for the parasitoid. Remarkably, polydnaviruses manipulate the phenotypes of the wasp, caterpillar, and host plant, demonstrating that polydnaviruses play far more prominent roles in shaping plant-herbivore interactions than ever considered.
Asunto(s)
Interacciones Huésped-Parásitos/inmunología , Larva/inmunología , Lepidópteros/inmunología , Inmunidad de la Planta/inmunología , Polydnaviridae/fisiología , Solanum lycopersicum/inmunología , Avispas/fisiología , Animales , Glucosa Oxidasa/metabolismo , Herbivoria , Larva/parasitología , Larva/virología , Lepidópteros/parasitología , Lepidópteros/virología , Conducta Predatoria , Simbiosis , Integración Viral , Replicación ViralRESUMEN
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.
Asunto(s)
Cynodon/inmunología , Cynodon/parasitología , Inmunidad de la Planta , Spodoptera/fisiología , Zea mays/inmunología , Zea mays/parasitología , Animales , Peso Corporal , Glucosa Oxidasa/metabolismo , Proteínas de Insectos/metabolismo , Larva/crecimiento & desarrollo , Hojas de la Planta/parasitología , Saliva/enzimología , Especificidad de la Especie , Fosfolipasas de Tipo C/metabolismoRESUMEN
Lepidopteran larvae secrete saliva on plant tissues during feeding. Components in the saliva may aid in food digestion, whereas other components are recognized by plants as cues to elicit defense responses. Despite the ecological and economical importance of these plant-feeding insects, knowledge of their saliva composition is limited to a few species. In this study, we identified the salivary proteins of larvae of the fall armyworm (FAW), Spodoptera frugiperda; determined qualitative and quantitative differences in the salivary proteome of the two host races-corn and rice strains-of this insect; and identified changes in total protein concentration and relative protein abundance in the saliva of FAW larvae associated with different host plants. Quantitative proteomic analyses were performed using labeling with isobaric tags for relative and absolute quantification followed by liquid chromatography-tandem mass spectrometry. In total, 98 proteins were identified (>99% confidence) in the FAW saliva. These proteins were further categorized into five functional groups: proteins potentially involved in (1) plant defense regulation, (2) herbivore offense, (3) insect immunity, (4) detoxification, (5) digestion, and (6) other functions. Moreover, there were differences in the salivary proteome between the FAW strains that were identified by label-free proteomic analyses. Thirteen differentially identified proteins were present in each strain. There were also differences in the relative abundance of eleven salivary proteins between the two FAW host strains as well as differences within each strain associated with different diets. The total salivary protein concentration was also different for the two strains reared on different host plants. Based on these results, we conclude that the FAW saliva contains a complex mixture of proteins involved in different functions that are specific for each strain and its composition can change plastically in response to diet type.
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Proteoma , Saliva/química , Spodoptera/química , Animales , Oryza , Proteómica , Especificidad de la Especie , Zea maysRESUMEN
Baculoviruses are food-borne microbial pathogens that are ingested by insects on contaminated foliage. Oxidation of plant-derived phenolics, activated by insect feeding, can directly interfere with infections in the gut. Since phenolic oxidation is an important component of plant resistance against insects, baculoviruses are suggested to be incompatible with plant defences. However, plants among and within species invest differently in a myriad of chemical and physical defences. Therefore, we hypothesized that among eight soybean genotypes, some genotypes would be able to maintain both high resistance against an insect pest and high efficacy of a baculovirus. Soybean constitutive (non-induced) and jasmonic acid (JA)-induced (anti-herbivore response) resistance was measured against the fall armyworm Spodoptera frugiperda (weight gain, leaf consumption and utilization). Indicators of phenolic oxidation were measured as foliar phenolic content and peroxidase activity. Levels of armyworm mortality inflicted by baculovirus (SfMNPV) did not vary among soybean genotypes when the virus was ingested with non-induced foliage. Ingestion of the virus on JA-induced foliage reduced armyworm mortality, relative to non-induced foliage, on some soybean genotypes. Baculovirus efficacy was lower when ingested with foliage that contained higher phenolic content and defensive properties that reduced armyworm weight gain and leaf utilization. However, soybean genotypes that defended the plant by reducing consumption rate and strongly deterred feeding upon JA-induction did not reduce baculovirus efficacy, indicating that these defences may be more compatible with baculoviruses to maximize plant protection. Differential compatibility of defence traits with the third trophic level highlights an important cost/trade-off associated with plant defence strategies.
Asunto(s)
Herbivoria , Spodoptera , Animales , Variación Genética , Hojas de la PlantaRESUMEN
Insect gut-associated microbes modulating plant defenses have been observed in beetles and piercing-sucking insects, but the role of caterpillar-associated bacteria in regulating plant induced defenses has not been adequately examined. We identified bacteria from the regurgitant of field-collected Helicoverpa zea larvae using 16S ribosomal RNA (rRNA) gene sequencing and matrix-assisted laser desorption/ionization time of flight (MALDI-TOF) mass spectrometry. A combination of biochemical, molecular, and confocal electron microscopy methods were used to determine the role of caterpillar-associated bacteria in mediating defenses in Solanum lycopersicum (tomato). Laboratory-reared H. zea inoculated with one of the bacteria identified in field-collected H. zea, Enterobacter ludwigii, induced expression of the tomato defense-related enzyme polyphenol oxidase and genes regulated by jasmonic acid (JA), whereas the salicylic acid (SA)-responsive pathogenesis-related gene was suppressed. Additionally, saliva and its main component glucose oxidase from inoculated caterpillars played an important role in elevating tomato anti-herbivore defenses. However, there were only low detectable amounts of regurgitant or bacteria on H. zea-damaged tomato leaves. Our results suggest that H. zea gut-associated bacteria indirectly mediate plant-insect interactions by triggering salivary elicitors. These findings provide a proof of concept that introducing gut bacteria to a herbivore may provide a novel approach to pest management through indirect induction of plant resistance.
Asunto(s)
Sistema Digestivo/microbiología , Enterobacter/fisiología , Lepidópteros/microbiología , Saliva/metabolismo , Solanum lycopersicum/inmunología , Animales , Catecol Oxidasa/metabolismo , Ciclopentanos , Glucosa Oxidasa/metabolismo , Herbivoria , Larva/microbiología , Solanum lycopersicum/enzimología , OxilipinasRESUMEN
Herbivore associated bacteria are vital mediators of plant and insect interactions. Host plants play an important role in shaping the gut bacterial community of insects. Colorado potato beetles (CPB; Leptinotarsa decemlineata) use several Solanum plants as hosts in their natural environment. We previously showed that symbiotic gut bacteria from CPB larvae suppressed jasmonate (JA)-induced defenses in tomato. However, little is known about how changes in the bacterial community may be involved in the manipulation of induced defenses in wild and cultivated Solanum plants of CPB. Here, we examined suppression of JA-mediated defense in wild and cultivated hosts of CPB by chemical elicitors and their symbiotic bacteria. Furthermore, we investigated associations between the gut bacterial community and suppression of plant defenses using 16 S rRNA amplicon sequencing. Symbiotic bacteria decreased plant defenses in all Solanum hosts and there were different gut bacterial communities in CPB fed on different host plants. When larvae were reared on different hosts, defense suppression differed among host plants. These results demonstrate that host plants influence herbivore gut bacterial communities and consequently affect the herbivore's ability to manipulate JA-mediated plant defenses. Thus, the presence of symbiotic bacteria that suppress plant defenses might help CPB adapt to host plants.
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Fenómenos Fisiológicos Bacterianos , Escarabajos/microbiología , Microbioma Gastrointestinal , Solanum/microbiología , Simbiosis , Animales , Escarabajos/metabolismo , Ciclopentanos/metabolismo , Herbivoria , Larva/microbiología , Oxilipinas/metabolismo , Ácido Salicílico/metabolismo , Solanum/metabolismoRESUMEN
Mechanical damage caused by insect feeding along with components present in insect saliva and oral secretions are known to induce jasmonic acid-mediated defense responses in plants. This study investigated the effects of bacteria from oral secretions of the fall armyworm Spodoptera frugiperda on herbivore-induced defenses in tomato and maize plants. Using culture-dependent methods, we identified seven different bacterial isolates belonging to the family Enterobacteriacea from the oral secretions of field-collected caterpillars. Two isolates, Pantoea ananatis and Enterobacteriaceae-1, downregulated the activity of the plant defensive proteins polyphenol oxidase and trypsin proteinase inhibitors (trypsin PI) but upregulated peroxidase (POX) activity in tomato. A Raoultella sp. and a Klebsiella sp. downregulated POX but upregulated trypsin PI in this plant species. Conversely, all of these bacterial isolates upregulated the expression of the herbivore-induced maize proteinase inhibitor (mpi) gene in maize. Plant treatment with P. ananatis and Enterobacteriaceae-1 enhanced caterpillar growth on tomato but diminished their growth on maize plants. Our results highlight the importance of herbivore-associated microbes and their ability to mediate insect plant interactions differently in host plants fed on by the same herbivore.