Summary: 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.

The induction of plant defences and their subsequent suppression by insects is thought to be an important factor in the evolutionary arms race between plants and herbivores. Although insect oral secretions (OS) contain elicitors that trigger plant immunity, little is known about the suppressors of plant defences. The Arabidopsis thaliana transcriptome was analysed in response to wounding and OS treatment. The expression of several wound-inducible genes was suppressed after the application of OS from two lepidopteran herbivores, Pieris brassicae and Spodoptera littoralis. This inhibition was correlated with enhanced S. littoralis larval growth, pointing to an effective role of insect OS in suppressing plant defences. Two genes, an ERF/AP2 transcription factor and a proteinase inhibitor, were then studied in more detail. OS-induced suppression lasted for at least 48 h, was independent of the jasmonate or salicylate pathways, and was not due to known elicitors. Interestingly, insect OS attenuated leaf water loss, suggesting that insects have evolved mechanisms to interfere with the induction of water-stress-related defences.

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.

Determining links between plant defence strategies is important to understand plant evolution and to optimize crop breeding strategies. Although several examples of synergies and trade‐offs between defence traits are known for plants that are under attack by multiple organisms, few studies have attempted to measure correlations of defensive strategies using specific single attackers. Such links are hard to detect in natural populations because they are inherently confounded by the evolutionary history of different ecotypes. We therefore used a range of 20 maize inbred lines with considerable differences in resistance traits to determine if correlations exist between leaf and root resistance against pathogens and insects. Aboveground resistance against insects was positively correlated with the plant's capacity to produce volatiles in response to insect attack. Resistance to herbivores and resistance to a pathogen, on the other hand, were negatively correlated. Our results also give first insights into the intraspecific variability of root volatiles release in maize and its positive correlation with leaf volatile production. We show that the breeding history of the different genotypes (dent versus flint) has influenced several defensive parameters. Taken together, our study demonstrates the importance of genetically determined synergies and trade‐offs for plant resistance against insects and pathogens.

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.

Fall armyworm,Spodoptera frugiperda, is a serious invasive pest in Africa but “Push-Pull” companion cropping can substantially reduce infestation. Here, we elucidate the underpinning chemical ecology mechanisms. We hypothesized that companion crop volatiles repel herbivores (push) while attracting natural enemies (pull). Headspace volatiles collected from companion plants (Desmodium intortum, Desmodium uncinatum,BrachiariaMulato II) were used in bioassays and electrophysiological recordings withS. frugiperdaand parasitoid wasps. Insect populations, plant damage and herbivore parasitism were assessed in field plots. Coupled GC-electroantennogram (GC-EAG) recordings showed robust responses to certain aromatic and terpenoid volatile compounds. In wind tunnel bioassays, maize volatiles mixed withDesmodiumvolatiles were less attractive to moths than maize alone. In oviposition bioassays,S. frugiperdalaid significantly fewer eggs on maize whenDesmodiumvolatiles were present. Conversely, in an olfactometer bioassay, parasitoid wasps were attracted to the scent of bothDesmodiumspp. (intercrop) and theBrachiariaborder crop. Our data provide evidence of the mechanisms underpinning reducedS. frugiperdainfestation in the Push-Pull companion cropping system, i.e., volatiles from companion crops repelS. frugiperdawhile attracting its parasitoid natural enemies. These findings explain why Push-Pull field plots had fewerS. frugiperdalarvae and lower crop damage than monocropped maize.