Chemical ecology of nectar-mosquito interactions: recent advances and future directions.

Mosquitoes, males and females, rely on sugar-rich resources, including floral nectar as a primary source of sugar to meet their energy and nutritional needs. Despite advancements in understanding mosquito host-seeking and blood-feeding preferences, significant gaps in our knowledge of the chemical ecology mediating mosquito-nectar associations remain. The influence of such association with nectar on mosquito behavior and the resulting effects on their fitness are also not totally understood. It is significant that floral nectar frequently acts as a natural habitat for various microbes (e.g. bacteria and yeast), which substantially alter nectar characteristics, influencing the nutritional ecology of flower-visiting insects, such as mosquitoes. The role of nectar-inhabiting microbes in shaping the nectar-mosquito interactions remains, however, under-researched. This review explores recent advances in understanding the role of such multitrophic interactions on the fitness and life history traits of mosquitoes and outlines future directions for research toward their control as disease vectors.

Comparative analysis of sorghum (C4) and rice (C3) plant headspace volatiles induced by artificial herbivory.

Acute stress responses include release of defensive volatiles from herbivore-attacked plants. Here we used two closely related monocot species, rice as a representative C3 plant, and sorghum as a representative C4 plant, and compared their basal and stress-induced headspace volatile organic compounds (VOCs). Although both plants emitted similar types of constitutive and induced VOCs, in agreement with the close phylogenetic relationship of the species, several mono- and sesquiterpenes have been significantly less abundant in headspace of sorghum relative to rice. Furthermore, in spite of generally lower VOC levels, some compounds, such as the green leaf volatile (Z)-3-hexenyl acetate and homoterpene DMNT, remained relatively high in the sorghum headspace, suggesting that a separate mechanism for dispersal of these compounds may have evolved in this plant. Finally, a variable amount of several VOCs among three sorghum cultivars of different geographical origins suggested that release of VOCs could be used as a valuable resource for the increase of sorghum resistance against herbivores.

This paper shows how genetically related plants with similar volatile toolboxes define their own species identity in the ecological space.

Impact of endophytic colonization by entomopathogenic fungi on the behavior and life history of the tobacco peach aphid Myzus persicae var. nicotianae.

Entomopathogenic fungi can adopt an endophytic lifestyle and provide protection against insect herbivores and plant pathogens. So far, most studies have focused on Beauveria bassiana to increase plant resistance against abiotic and biotic stresses, while only little is known for other entomopathogenic fungi. In this study, we investigated whether root inoculation of sweet pepper (Capsicum annuum L.) by the entomopathogenic fungi Akanthomyces muscarius ARSEF 5128 and B. bassiana ARSEF 3097 can improve resistance against the tobacco peach aphid Myzus persicae var. nicotianae. First, dual-choice experiments were performed to test the hypothesis that the fungi deter aphids via modifying plant volatile profiles. Next, we tested the hypothesis that endophytic colonization negatively affects aphid life history traits, such as fecundity, development and mortality rate. Aphids were significantly attracted to the odor of plants inoculated with A. muscarius over non-inoculated plants. Plants inoculated with A. muscarius emitted significantly higher amounts of ß-pinene than non-inoculated plants, and significantly higher amounts of indole than B. bassiana-inoculated and non-inoculated plants. Inoculation with the fungal strains also caused significantly higher emission of terpinolene. Further, both aphid longevity and fecundity were significantly reduced by 18% and 10%, respectively, when feeding on plants inoculated with A. muscarius, although intrinsic rate of population increase did not differ between inoculated and non-inoculated plants. Sweet pepper plants inoculated with B. bassiana ARSEF 3097 did not elicit a significant behavioral response nor affected the investigated life history traits. We conclude that endophytic colonization by entomopathogenic fungi has the potential to alter olfactory behavior and performance of M. persicae var. nicotianae, but effects are small and depend on the fungal strain used.

Wild potato ancestors as potential sources of resistance to the aphid Myzus persicae.

BACKGROUND: Plant resistance to insects can be reduced by crop domestication which means their wild ancestors could provide novel sources of resistance. Thus, crossing wild ancestors with domesticated crops can potentially enhance their resistance against insects. However, a prerequisite for this is identification of sources of resistance. Here, we investigated the response of three wild potato (Solanum stoloniferum Schltdl.) accessions and cultivated potato (Solanum tuberosum) to aphid (Myzus persicae Sulzer) herbivory. RESULTS: Results revealed that there was a significant reduction in aphid survival and reproduction on wild potato accessions (CGN18333, CGN22718, CGN23072) compared to cultivated (Desiree) potato plants. A similar trend was observed in olfactometer bioassay; the wild accessions had a repellent effect on adult aphids. In contrast, among the tested wild potato accessions, the parasitoid Diaeretiella rapae (M'Intosh) was significantly attracted to volatiles from CGN18333. Volatile analysis showed that wild accessions emitted significantly more volatiles compared to cultivated potato. Principal component analysis (PCA) of volatile data revealed that the volatile profiles of wild and cultivated potato are dissimilar. ß-Bisabolene, (E)-ß-farnesene, trans-α-bergamotene, d-limonene, (E,E)-4,8,12-trimethyl-1,3,7,11-tridecatetraene (TMTT), and p-cymen-7-ol were the main volatiles contributing to the emitted blends, suggesting possible involvement in the behavioural response of both M. persicae and D. rapae. CONCLUSION: Our findings show that the tested wild accessions have the potential to be used to breed aphid-resistant potatoes. This opens new opportunities to reduce the aphid damage and to enhance the recruitment of natural enemies. © 2022 The Authors. Pest Management Science published by John Wiley & Sons Ltd on behalf of Society of Chemical Industry.

Effects of cis-Jasmone Treatment of Brassicas on Interactions With Myzus persicae Aphids and Their Parasitoid Diaeretiella rapae.

There is a need to develop new ways of protecting plants against aphid attack. Here, we investigated the effect of a plant defence activator, cis-jasmone (CJ), in a range of cultivars of Brassica napus, Brassica rapa and Brassica oleracea. Plants were sprayed with cis-jasmone or blank formulation and then tested with peach potato aphids (Myzus persicae Sulzer) (Hemiptera: Aphididae) and their parasitoid Diaeretiella rapae (M'Intosh) (Hymenoptera: Braconidae). CJ treated plants had significantly lower aphid settlement than control plants in a settlement bioassay. Conversely, in a foraging bioassay, D. rapae parasitoids spent a significantly longer time foraging on CJ treated plants. Our results reveal that CJ treatment makes plants less attractive to and less suitable for M. persicae but more attractive to D. rapae in a range of brassica cultivars. It is likely that these effects are due to changes in volatile emission indicating activation of defence and presence of conspecific competitors to aphids but presence of prey to parasitoids. Increases in volatile emission were found in CJ induced plants but varied with genotype. Among the synthetic volatile compounds that were induced in the headspace of CJ treated brassica cultivars, methyl isothiocyanate, methyl salicylate and cis-jasmone were most repellent to aphids. These results build on earlier studies in Arabidopsis and show that tritrophic interactions are influenced by CJ in a wide range of brassica germplasm. The implication is that CJ is a promising treatment that could be used in brassica crops as part of an integrated pest management system.

Evolutionary ecology: Plant volatile profile changes after escaping specialist insects.

Considerable debate surrounds the role of plant volatiles in plant defence against insects. A new study provides evidence for evolutionary changes in an invasive plant that support the defensive role of plant volatiles.

The Pupal Parasitoid Trichopria drosophilae Is Attracted to the Same Yeast Volatiles as Its Adult Host.

There is increasing evidence that microorganisms, particularly fungi and bacteria, emit volatile compounds that mediate the foraging behaviour of insects and therefore have the potential to affect key ecological relationships. However, to what extent microbial volatiles affect the olfactory response of insects across different trophic levels remains unclear. Adult parasitoids use a variety of chemical stimuli to locate potential hosts, including those emitted by the host's habitat, the host itself, and microorganisms associated with the host. Given the great capacity of parasitoids to utilize and learn odours to increase foraging success, parasitoids of eggs, larvae, or pupae may respond to the same volatiles the adult stage of their hosts use when locating their resources, but compelling evidence is still scarce. In this study, using Saccharomyces cerevisiae we show that Trichopria drosophilae, a pupal parasitoid of Drosophila species, is attracted to the same yeast volatiles as their hosts in the adult stage, i.e. acetate esters. Parasitoids significantly preferred the odour of S. cerevisiae over the blank medium in a Y-tube olfactometer. Deletion of the yeast ATF1 gene, encoding a key acetate ester synthase, decreased attraction of T. drosophilae, while the addition of synthetic acetate esters to the fermentation medium restored parasitoid attraction. Bioassays with individual compounds revealed that the esters alone were not as attractive as the volatile blend of S. cerevisiae, suggesting that other volatile compounds also contribute to the attraction of T. drosophilae. Altogether, our results indicate that pupal parasitoids respond to the same volatiles as the adult stage of their hosts, which may aid them in locating oviposition sites.

Herbivore-induced and constitutive volatiles are controlled by different oxylipin-dependent mechanisms in rice.

Despite the importance of volatile organic compounds (VOCs) for plants, control mechanisms for their basal and stress-induced biosynthesis and release remain unclear. We sampled and characterized headspace and internal leaf volatile pools in rice (Oryza sativa), after a simulated herbivory treatment, which triggers an endogenous jasmonate burst. Certain volatiles, such as linalool, were strongly upregulated by simulated herbivory stress. In contrast, other volatiles, such as ß-caryophyllene, were constitutively emitted and fluctuated according to time of day. Transcripts of the linalool synthase gene transiently increased 1-3 h after exposure of rice to simulated herbivory, whereas transcripts of caryophyllene synthase peaked independently at dawn. Unexpectedly, although emission and accumulation patterns of rice inducible and constitutive VOCs were substantially different, both groups of volatiles were compromised in jasmonate-deficient hebiba mutants, which lack the allene oxide cyclase (AOC) gene. This suggests that rice employs at least two distinct oxylipin-dependent mechanisms downstream of AOC to control production of constitutive and herbivore-induced volatiles. Levels of the JA precursor, 12-oxo-phytodienoic acid (OPDA), were correlated with constitutive volatile levels suggesting that OPDA or its derivatives could be involved in control of volatile emission in rice.

Evaluation of African Maize Cultivars for Resistance to Fall Armyworm Spodoptera frugiperda (J. E. Smith) (Lepidoptera: Noctuidae) Larvae.

The fall armyworm (FAW) has recently invaded and become an important pest of maize in Africa causing yield losses reaching up to a third of maize annual production. The present study evaluated different aspects of resistance of six maize cultivars, cropped by farmers in Kenya, to FAW larvae feeding under laboratory and field conditions. We assessed the arrestment and feeding of FAW neonate larvae in no-choice and choice experiments, development of larvae-pupae, food assimilation under laboratory conditions and plant damage in a field experiment. We did not find complete resistance to FAW feeding in the evaluated maize cultivars, but we detected differences in acceptance and preference when FAW larvae were given a choice between certain cultivars. Moreover, the smallest pupal weight and the lowest growth index were found on 'SC Duma 43' leaves, which suggests an effect of antibiosis of this maize hybrid against FAW larvae. In contrast, the highest growth index was recorded on 'Rachar' and the greatest pupal weight was found on 'Nyamula' and 'Rachar'. The density of trichomes on the leaves of these maize cultivars seems not to be directly related to the preference of neonates for feeding. Plant damage scores were not statistically different between cultivars in the field neither under natural nor artificial infestation. However, plant damage scores in 'Nyamula' and 'Jowi' tended to be lower in the two last samplings of the season compared to the two initial samplings under artificial infestation. Our study provides insight into FAW larval preferences and performance on some African maize cultivars, showing that there are differences between cultivars in these variables; but high levels of resistance to larvae feeding were not found.

Identification and application of bacterial volatiles to attract a generalist aphid parasitoid: from laboratory to greenhouse assays.

BACKGROUND: Recent studies have shown that microorganisms emit volatile compounds that affect insect behaviour. However, it remains largely unclear whether microbes can be exploited as a source of attractants to improve biological control of insect pests. In this study, we used a combination of coupled gas chromatography-electroantennography (GC-EAG) and Y-tube olfactometer bioassays to identify attractive compounds in the volatile extracts of three bacterial strains that are associated with the habitat of the generalist aphid parasitoid Aphidius colemani, and to create mixtures of synthetic compounds to find attractive blends for A. colemani. Subsequently, the most attractive blend was evaluated in two-choice cage experiments under greenhouse conditions. RESULTS: GC-EAG analysis revealed 20 compounds that were linked to behaviourally attractive bacterial strains. A mixture of two EAG-active compounds, styrene and benzaldehyde applied at a respective dose of 1 µg and 10 ng, was more attractive than the single compounds or the culture medium of the bacteria in Y-tube olfactometer bioassays. Application of this synthetic mixture under greenhouse conditions resulted in significant attraction of the parasitoids, and outperformed application of the bacterial culture medium. CONCLUSION: Compounds isolated from bacterial blends were capable of attracting parasitoids both in laboratory and greenhouse assays, indicating that microbial cultures are an effective source of insect attractants. This opens new opportunities to attract and retain natural enemies of pest species and to enhance biological pest control.

Ethylene functions as a suppressor of volatile production in rice.

We examined the role of ethylene in the production of rice (Oryza sativa) volatile organic compounds (VOCs), which act as indirect defense signals against herbivores in tritrophic interactions. Rice plants were exposed to exogenous ethylene (1 ppm) after simulated herbivory, which consisted of mechanical wounding supplemented with oral secretions (WOS) from the generalist herbivore larva Mythimna loreyi. Ethylene treatment highly suppressed VOCs in WOS-treated rice leaves, which was further corroborated by the reduced transcript levels of major VOC biosynthesis genes in ethylene-treated rice. In contrast, the accumulation of jasmonates (JA), known to control VOCs in higher plants, and transcript levels of primary JA response genes, including OsMYC2, were not largely affected by ethylene application. At the functional level, flooding is known to promote internode elongation in young rice via ethylene signaling. Consistent with the negative role of ethylene on VOC genes, the accumulation of VOCs in water-submerged rice leaves was suppressed. Furthermore, in mature rice plants, which naturally produce less volatiles, VOCs could be rescued by the application of the ethylene perception inhibitor 1-methylcyclopropene. Our data suggest that ethylene acts as an endogenous suppressor of VOCs in rice plants during development and under stress.

Behavioural and Electrophysiological Responses of Female Anopheles gambiae Mosquitoes to Volatiles from a Mango Bait.

Attractive Toxic Sugar Baits (ATSB) are used in a "lure-and-kill" approach for management of the malaria vector Anopheles gambiae, but the active chemicals were previously unknown. Here we collected volatiles from a mango, Mangifera indica, juice bait which is used in ATSBs in Tanzania and tested mosquito responses. In a Y-tube olfactometer, female mosquitoes were attracted to the mango volatiles collected 24-48 h, 48-72 h and 72-96 h after preparing the bait but volatiles collected at 96-120 h were no longer attractive. Volatile analysis revealed emission of 23 compounds in different chemical classes including alcohols, aldehydes, alkanes, benzenoids, monoterpenes, sesquiterpenes and oxygenated terpenes. Coupled GC-electroantennogram (GC-EAG) recordings from the antennae of An. gambiae showed robust responses to 4 compounds: humulene, (E)-caryophyllene, terpinolene and myrcene. In olfactometer bioassays, mosquitoes were attracted to humulene and terpinolene. (E)-caryophyllene was marginally attractive while myrcene elicited an avoidance response with female mosquitoes. A blend of humulene, (E)-caryophyllene and terpinolene was highly attractive to females (P < 0.001) when tested against a solvent blank. Furthermore, there was no preference when this synthetic blend was offered as a choice against the natural sample. Our study has identified the key compounds from mango juice baits that attract An. gambiae and this information may help to improve the ATSBs currently used against malaria vectors.

Sweet Scents: Nectar Specialist Yeasts Enhance Nectar Attraction of a Generalist Aphid Parasitoid Without Affecting Survival.

Floral nectar is commonly inhabited by microorganisms, mostly yeasts and bacteria, which can have a strong impact on nectar chemistry and scent. Yet, little is known about the effects of nectar microbes on the behavior and survival of insects belonging to the third trophic level such as parasitoids. Here, we used five nectar-inhabiting yeast species to test the hypothesis that yeast species that almost solely occur in nectar, and therefore substantially rely on floral visitors for dispersal, produce volatile compounds that enhance insect attraction without compromising insect life history parameters, such as survival. Experiments were performed using two nectar specialist yeasts (Metschnikowia gruessii and M. reukaufii) and three generalist species (Aureobasidium pullulans, Hanseniaspora uvarum, and Sporobolomyces roseus). Saccharomyces cerevisiae was included as a reference yeast. We compared olfactory responses of the generalist aphid parasitoid Aphidius ervi (Haliday) (Hymenoptera: Braconidae) when exposed to these microorganisms inoculated in synthetic nectar. Nectar-inhabiting yeasts had a significant impact on nectar chemistry and produced distinct volatile blends, some of which were attractive, while others were neutral or repellent. Among the different yeast species tested, the nectar specialists M. gruessii and M. reukaufii were the only species that produced a highly attractive nectar to parasitoid females, which simultaneously had no adverse effects on longevity and survival of adults. By contrast, parasitoids that fed on nectars fermented with the reference strain, A. pullulans, H. uvarum or S. roseus showed shortest longevity and lowest survival. Additionally, nectars fermented by A. pullulans or S. roseus were consumed significantly less, suggesting a lack of important nutrients or undesirable changes in the nectar chemical profiles. Altogether our results indicate that nectar-inhabiting yeasts play an important, but so far largely overlooked, role in plant-insect interactions by modulating the chemical composition of nectar, and may have important ecological consequences for plant pollination and biological control of herbivorous insects.

Priming of cowpea volatile emissions with defense inducers enhances the plant's attractiveness to parasitoids when attacked by caterpillars.

BACKGROUND: The manipulation of herbivore-induced volatile organic compounds (HI-VOCs) via the application of the inducers benzo(1,2,3)thiadiazole-7-carbothioic acid S-methyl ester (BTH) and laminarin (ß-1,3-glucan) is known to enhance the attractiveness of caterpillar-damaged cotton and maize plants to parasitoids. To test if this is also the case for legumes, we treated cowpea (Vigna unguiculata var. unguiculata) with these inducers and studied the effects on HI-VOC emissions and the attraction of three generalist endoparasitoids. RESULTS: After the inducers had been applied and the plants subjected to either real or mimicked herbivory by Spodoptera littoralis caterpillars, females of the parasitoids Campoletis sonorensis and Microplitis rufiventris showed a strong preference for BTH-treated plants, whereas Cotesia females were strongly attracted to both BTH- and laminarin-treated plants with real or mimicked herbivory. Treated plants emitted more of certain HI-VOCs, but considerably less indole and linalool and less of several sesquiterpenes. Multivariate data analysis revealed that enhanced wasp attraction after treatment was correlated with high relative concentrations of nonanal, α-pinene, (E)-ß-ocimene and (E)-4,8-dimethyl-1,3,7-nonatriene (DMNT), and with low relative concentrations of indole, (S)-linalool and (E)-ß-farnesene. Inducer treatments had no significant effect on leaf consumption by the caterpillars. CONCLUSION: Our findings confirm that treating cowpea plants with inducers can enhance their attractiveness to biological control agents. © 2017 Society of Chemical Industry.

Oral Secretions Affect HIPVs Induced by Generalist (Mythimna loreyi) and Specialist (Parnara guttata) Herbivores in Rice.

Plants synthesize variable mixtures of herbivore-induced plant volatiles (HIPVs) as part of their evolutionary conserved defense. To elucidate the impact of chewing herbivores with different level of adaptation on HIPV profiles in rice, we measured HIPVs released from rice seedlings challenged by either the generalist herbivore Mythimna loreyi (MYL) or the specialist Parnara guttata (PAG). Both herbivores markedly elicited the emission of HIPVs, mainly on the second and third days after attack compared to control plants. In addition, side-by-side HIPV comparisons using MYL and PAG caterpillars revealed that generalist feeding induced comparably more HIPVs relative to specialist, particularly on day two as highlighted by multivariate analysis (PLS-DA) of emitted HIPVs, and further confirmed in mimicked herbivory experiments. Here, mechanically wounded plants treated with water (WW) released more VOCs than untreated controls, and on top of this, oral secretions (OS) from both herbivores showed differential effects on volatile emissions from the wounded plants. Similar to actual herbivory, MYL OS promoted higher amounts of HIPVs relative to PAG OS, thus supporting disparate induction of rice indirect defenses in response to generalist and specialist herbivores, which could be due to the differential composition of their OS. (196 words).

cis-Jasmone Elicits Aphid-Induced Stress Signalling in Potatoes.

Elicitation of plant defense signaling that results in altered emission of volatile organic compounds (VOCs) offers opportunities for protecting plants against arthropod pests. In this study, we treated potato, Solanum tuberosum L., with the plant defense elicitor cis-jasmone (CJ), which induces the emission of defense VOCs and thus affects the behavior of herbivores. Using chemical analysis, electrophysiological and behavioral assays with the potato-feeding aphid Macrosiphum euphorbiae, we showed that CJ treatment substantially increased the emission of defense VOCs from potatoes compared to no treatment. Coupled GC-electroantennogram (GC-EAG) recordings from the antennae of M. euphorbiae showed robust responses to 14 compounds present in induced VOCs, suggesting their behavioral role in potato/aphid interactions. Plants treated with CJ and then challenged with M. euphorbiae were most repellent to alate M. euphorbiae. Principal component analysis (PCA) of VOC collections suggested that (E)-2-hexenal, (E,E)-4,8,12-trimethyl-1,3,7,11-tridecatetraene (TMTT), (E)-ß-farnesene, (E)-4,8-dimethyl-1,3,7-nonatriene (DMNT), methyl salicylate (MeSA), CJ, and methyl benzoate (MeBA) were the main VOCs contributing to aphid behavioral responses, and that production of TMTT, (E)-ß-farnesene, CJ, and DMNT correlated most strongly with aphid repellency. Our findings confirm that CJ can enhance potato defense against aphids by inducing production of VOCs involved in aphid-induced signalling.

Plant strengtheners enhance parasitoid attraction to herbivore-damaged cotton via qualitative and quantitative changes in induced volatiles.

BACKGROUND: Herbivore-damaged plants release a blend of volatile organic compounds (VOCs) that differs from undamaged plants. These induced changes are known to attract the natural enemies of the herbivores and therefore are expected to be important determinants of the effectiveness of biological control in agriculture. One way of boosting this phenomenon is the application of plant strengtheners, which has been shown to enhance parasitoid attraction in maize. It is unclear whether this is also the case for other important crops. RESULTS: The plant strengtheners BTH [benzo (1,2,3) thiadiazole-7-carbothioic acid S-methyl ester] and laminarin were applied to cotton plants, and the effects on volatile releases and the attraction of three hymenopteran parasitoids, Cotesia marginiventris, Campoletis sonorensis and Microplitis rufiventris, were studied. After treated and untreated plants were induced by real or simulated caterpillar feeding, it was found that BTH treatment increased the attraction of the parasitoids, whereas laminarin had no significant effect. BTH treatment selectively increased the release of two homoterpenes and reduced the emission of indole, the latter of which had been shown to interfere with parasitoid attraction in earlier studies. Canonical variate analyses of the data show that the parasitoid responses were dependent on the quality rather than the quantity of volatile emission in this tritrophic interaction. CONCLUSION: Overall, these results strengthen the emerging paradigm that induction of plant defences with chemical elicitors such as BTH could provide a sustainable and environmentally friendly strategy for biological control of pests by enhancing the attractiveness of cultivated plants to natural enemies of insect herbivores.

The prospect of applying chemical elicitors and plant strengtheners to enhance the biological control of crop pests.

An imminent food crisis reinforces the need for novel strategies to increase crop yields worldwide. Effective control of pest insects should be part of such strategies, preferentially with reduced negative impact on the environment and optimal protection and utilization of existing biodiversity. Enhancing the presence and efficacy of native biological control agents could be one such strategy. Plant strengthener is a generic term for several commercially available compounds or mixtures of compounds that can be applied to cultivated plants in order to 'boost their vigour, resilience and performance'. Studies into the consequences of boosting plant resistance against pests and diseases on plant volatiles have found a surprising and dramatic increase in the plants' attractiveness to parasitic wasps. Here, we summarize the results from these studies and present new results from assays that illustrate the great potential of two commercially available resistance elicitors. We argue that plant strengtheners may currently be the best option to enhance the attractiveness of cultivated plants to biological control agents. Other options, such as the genetic manipulation of the release of specific volatiles may offer future solutions, but in most systems, we still miss fundamental knowledge on which key attractants should be targeted for this approach.

The maize lipoxygenase, ZmLOX10, mediates green leaf volatile, jasmonate and herbivore-induced plant volatile production for defense against insect attack.

Fatty acid derivatives are of central importance for plant immunity against insect herbivores; however, major regulatory genes and the signals that modulate these defense metabolites are vastly understudied, especially in important agro-economic monocot species. Here we show that products and signals derived from a single Zea mays (maize) lipoxygenase (LOX), ZmLOX10, are critical for both direct and indirect defenses to herbivory. We provide genetic evidence that two 13-LOXs, ZmLOX10 and ZmLOX8, specialize in providing substrate for the green leaf volatile (GLV) and jasmonate (JA) biosynthesis pathways, respectively. Supporting the specialization of these LOX isoforms, LOX8 and LOX10 are localized to two distinct cellular compartments, indicating that the JA and GLV biosynthesis pathways are physically separated in maize. Reduced expression of JA biosynthesis genes and diminished levels of JA in lox10 mutants indicate that LOX10-derived signaling is required for LOX8-mediated JA. The possible role of GLVs in JA signaling is supported by their ability to partially restore wound-induced JA levels in lox10 mutants. The impaired ability of lox10 mutants to produce GLVs and JA led to dramatic reductions in herbivore-induced plant volatiles (HIPVs) and attractiveness to parasitoid wasps. Because LOX10 is under circadian rhythm regulation, this study provides a mechanistic link to the diurnal regulation of GLVs and HIPVs. GLV-, JA- and HIPV-deficient lox10 mutants display compromised resistance to insect feeding, both under laboratory and field conditions, which is strong evidence that LOX10-dependent metabolites confer immunity against insect attack. Hence, this comprehensive gene to agro-ecosystem study reveals the broad implications of a single LOX isoform in herbivore defense.