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The recent invasion of the fall armyworm (FAW) into Asia not only has had a major impact on maize yield but is feared to also pose a risk to rice production. We hypothesized that the brown planthopper (BPH) may aggravate this risk based on a recently discovered mutualism between the planthopper and the rice striped stem borer. Here we show that BPH may indeed facilitate a shift of FAW to rice. FAW females were found to strongly prefer to oviposit on BPH-infested rice plants, which emitted significantly elevated levels of five volatile compounds. A synthetic mixture of these compounds had a potent stimulatory effect on ovipositing females. Although FAW caterpillars exhibited relatively poor growth on both uninfested and BPH-infested rice, a considerable portion completed their development on young plants. Moreover, FAW were found to readily pupate and survive in exceedingly moist soils typical for rice cultivation, further highlighting FAW's potential to switch to rice. We conclude that BPH, by changing the bouquet of volatiles emitted by rice plants, may greatly facilitate this switch. These findings, together with a current increase of nonflooded upland rice in Asia, warrant careful monitoring and specific control measures against FAW to safeguard Asian rice production., (© 2024 The Author(s). Plant, Cell & Environment published by John Wiley & Sons Ltd.)

Plant viral diseases compromise the growth and yield of the crop globally, and they tend to be more serious under extreme temperatures and drought climate changes. Currently, regulatory dynamics during plant development and in response to virus infection at the plant cell level remain largely unknown. In this study, single-cell RNA sequencing on 23 226 individual cells from healthy and tomato chlorosis virus-infected leaves was established. The specific expression and epigenetic landscape of each cell type during the viral infection stage were depicted. Notably, the mesophyll cells showed a rapid function transition in virus-infected leaves, which is consistent with the pathological changes such as thinner leaves and decreased chloroplast lamella in virus-infected samples. Interestingly, the F-box protein SKIP2 was identified to play a pivotal role in chlorophyll maintenance during virus infection in tomato plants. Knockout of the SlSKIP2 showed a greener leaf state before and after virus infection. Moreover, we further demonstrated that SlSKIP2 was located in the cytomembrane and nucleus and directly regulated by ERF4. In conclusion, with detailed insights into the plant responses to viral infections at the cellular level, our study provides a genetic framework and gene reference in plant-virus interaction and breeding in the future research., (© 2024 John Wiley & Sons Ltd.)

Plants recognize and respond to feeding by herbivorous insects by upregulating their local and systemic defenses. While defense induction by aboveground herbivores has been well studied, far less is known about local and systemic defense responses against attacks by belowground herbivores. Here, we investigated and compared the responses of the maize transcriptome to belowground and aboveground mechanical damage and infestation by two well-adapted herbivores: the soil-dwelling western corn rootworm Diabrotica virgifera virgifera (Coleoptera: Chrysomelidae) and the leaf-chewing fall armyworm Spodoptera frugiperda (Lepidoptera: Noctuidae). In responses to both herbivores, maize plants were found to alter local transcription of genes involved in phytohormone signaling, primary and secondary metabolism. Induction by real herbivore damage was considerably stronger and modified the expression of more genes than mechanical damage. Feeding by the corn rootworm had a strong impact on the shoot transcriptome, including the activation of genes involved in defense and development. By contrast, feeding by the fall armyworm induced only few transcriptional changes in the roots. In conclusion, feeding by a leaf chewer and a root feeder differentially affects the local and systemic defense of maize plants. Besides revealing clear differences in how maize plants respond to feeding by these specialized herbivores, this study reveals several novel genes that may play key roles in plant-insect interactions and thus sets the stage for in depth research into the mechanism that can be exploited for improved crop protection., Significance Statement: Extensive transcriptomic analyses revealed a clear distinction between the gene expression profiles in maize plants upon shoot and root attack, locally as well as distantly from the attacked tissue. This provides detailed insights into the specificity of orchestrated plant defense responses, and the dataset offers a molecular resource for further genetic studies on maize resistance to herbivores and paves the way for novel strategies to enhance maize resistance to pests., Competing Interests: The authors declare no conflict of interest., (© 2022 The Authors. Plant Direct published by American Society of Plant Biologists and the Society for Experimental Biology and John Wiley & Sons Ltd.)

Plant communication in response to insect herbivory has been increasingly studied, whereas that involving pathogen attack has received much less attention. We tested for communication between potato (Solanum tuberosum) plants in response to leaf infection by the fungal pathogen Sclerotinia sclerotiorum. To this end, we measured the total amount and composition of volatile organic compounds (VOCs) produced by control and infected emitter plants, as well as tested for induced resistance of receiver plants exposed to VOCs from emitters. We further tested for changes in the expression of defensive genes due to pathogen infection. Fungal infection did not significantly affect the total amount or composition of VOCs produced by emitter plants. Correspondingly, we found no evidence of higher resistance to the pathogen in receiver plants exposed to VOCs from infected emitters relative to control emitters. Molecular analyses indicated that pathogen infection drove a down-regulation of genes coding for VOC precursors, potentially explaining the absence of pathogen effects on VOC emissions and thus of communication. Overall, these results indicate no evidence of airborne communication between potato plants in response to fungal infection and point at pathogen inhibition of VOC emissions as a likely explanation for this result., (© 2020 John Wiley & Sons Ltd.)

Herbivore-induced plant volatiles (HIPVs) are important cues for female parasitic wasps to find hosts. Here, we investigated the possibility that HIPVs may also serve parasitoids as cues to locate mates. To test this, the odour preferences of four braconid wasps - the gregarious parasitoid Cotesia glomerata (L.) and the solitary parasitoids Cotesia marginiventris (Cresson), Microplitis rufiventris Kokujev and Microplitis mediator (Haliday) - were studied in olfactometers. Each species showed attraction to pheromones but in somewhat different ways. Males of the two Cotesia species were attracted to virgin females, whereas females of M. rufiventris were attracted to virgin males. Male and female M. mediator exhibited attraction to both sexes. Importantly, female and male wasps of all four species were strongly attracted by HIPVs, independent of mating status. In most cases, male wasps were also attracted to intact plants. The wasps preferred the combination of HIPVs and pheromones over plant odours alone, except M. mediator, which appears to mainly use HIPVs for mate location. We discuss the ecological contexts in which the combined use of pheromones and HIPVs by parasitoids can be expected. To our knowledge, this is the first study to show that braconid parasitoids use HIPVs and pheromones in combination to locate mates., (© 2016 John Wiley & Sons Ltd.)

The co-occurrence of different antagonists on a plant can greatly affect infochemicals with ecological consequences for higher trophic levels. Here we investigated how the presence of a plant pathogen, the powdery mildew Erysiphe cruciferarum, on Brassica rapa affects (1) plant volatiles emitted in response to damage by a specialist herbivore, Pieris brassicae; (2) the attraction of the parasitic wasp Cotesia glomerata and (3) the performance of P. brassicae and C. glomerata. Plant volatiles were significantly induced by herbivory in both healthy and mildew-infected plants, but were quantitatively 41% lower for mildew-infected plants compared to healthy plants. Parasitoids strongly preferred Pieris-infested plants to dually-infested (Pieris + mildew) plants, and preferred dually infested plants over only mildew-infected plants. The performance of P. brassicae was unaffected by powdery mildew, but C. glomerata cocoon mass was reduced when parasitized caterpillars developed on mildew-infected plants. Thus, avoidance of mildew-infested plants may be adaptive for C. glomerata parasitoids, whereas P. brassicae caterpillars may suffer less parasitism on mildew-infected plants in nature. From a pest management standpoint, the concurrent presence of multiple plant antagonists can affect the efficiency of specific natural enemies, which may in turn have a negative impact on the regulation of pest populations., (© 2016 John Wiley & Sons Ltd.)

Plant defences vary in space and time, which may translate into specific herbivore-foraging patterns and feeding niche differentiation. To date, little is known about the effect of secondary metabolite patterning on within-plant herbivore foraging. We investigated how variation in the major maize secondary metabolites, 1,4-benzoxazin-3-one derivatives (BXDs), affects the foraging behaviour of two leaf-chewing herbivores. BXD levels varied substantially within plants. Older leaves had higher levels of constitutive BXDs while younger leaves were consistently more inducible. These differences were observed independently of plant age, even though the concentrations of most BXDs declined markedly in older plants. Larvae of the well-adapted maize pest Spodoptera frugiperda preferred and grew better on young inducible leaves irrespective of plant age, while larvae of the generalist Spodoptera littoralis preferred and tended to grow better on old leaves. In BXD-free mutants, the differences in herbivore weight gain between old and young leaves were absent for both species, and leaf preferences of S. frugiperda were attenuated. In contrast, S. littoralis foraging patterns were not affected. In summary, our study shows that plant secondary metabolites differentially affect performance and foraging of adapted and non-adapted herbivores and thereby likely contribute to feeding niche differentiation., (© 2014 John Wiley & Sons Ltd.)

Upon attack by leaf herbivores, many plants reallocate photoassimilates below ground. However, little is known about how plants respond when the roots themselves come under attack. We investigated induced resource allocation in maize plants that are infested by the larvae Western corn rootworm Diabrotica virgifera virgifera. Using radioactive (11) CO(2), we demonstrate that root-attacked maize plants allocate more new (11) C carbon from source leaves to stems, but not to roots. Reduced meristematic activity and reduced invertase activity in attacked maize root systems are identified as possible drivers of this shoot reallocation response. The increased allocation of photoassimilates to stems is shown to be associated with a marked thickening of these tissues and increased growth of stem-borne crown roots. A strong quantitative correlation between stem thickness and root regrowth across different watering levels suggests that retaining photoassimilates in the shoots may help root-attacked plants to compensate for the loss of belowground tissues. Taken together, our results indicate that induced tolerance may be an important strategy of plants to withstand belowground attack. Furthermore, root herbivore-induced carbon reallocation needs to be taken into account when studying plant-mediated interactions between herbivores., (© 2014 John Wiley & Sons Ltd.)

Volatile organic compounds emitted by plants represent the largest part of biogenic volatile organic compounds (BVOCs) released into our atmosphere. Plant volatiles are formed through many biochemical pathways, constitutively and after stress induction. In recent years, our understanding of the functions of these molecules has made constant and rapid progress. From being considered in the past as a mere waste of carbon, BVOCs have now emerged as an essential element of an invisible language that is perceived and exploited by the plants' enemies, the enemies of plant enemies, and neighbouring plants. In addition, BVOCs have important functions in protecting plants from abiotic stresses. Recent advances in our understanding of the role of BVOC in direct and indirect defences are driving further attention to these emissions. This special issue gathers some of the latest and most original research that further expands our knowledge of BVOC. BVOC emissions and functions in (1) unexplored terrestrial (including the soil) and marine environments, (2) in changing climate conditions, and (3) under anthropic pressures, or (4) in complex trophic communities are comprehensively reviewed. Stepping up from scientific awareness, the presented information shows that the manipulation and exploitation of BVOC is a realistic and promising strategy for agricultural applications and biotechnological exploitations., (© 2014 John Wiley & Sons Ltd.)

Insect herbivores trigger various biochemical changes in plants, and as a consequence, affect other organisms that are associated with these plants. Such plant-mediated indirect effects often involve herbivore-induced plant volatiles (HIPVs) that can be used as cues for foraging herbivores and their natural enemies, and are also known to affect pollinator attraction. In tightly co-evolved systems, the different trophic levels are expected to display adaptive response to changes in HIPVs caused by native herbivores. But what if a new herbivore invades such a system? Current literature suggests that exotic herbivores have the potential to affect HIPV production, and that plant responses to novel herbivores are likely to depend on phylogenetic relatedness between the invader and the native species. Here we review the different ways exotic herbivores can disrupt chemically mediated interactions between plants and the key users of HIPVs: herbivores, pollinators, and members of the third (i.e. predators and parasitoids) and fourth (i.e. hyperparasitoids) trophic levels. Current theory on insect invasions needs to consider that disruptive effects of invaders on infochemical networks can have a short-term impact on the population dynamics of native insects and plants, as well as exerting potentially negative consequences for the functioning of native ecosystems., (© 2014 John Wiley & Sons Ltd.)

Volatile organic compounds (VOCs) released by soil microorganisms influence plant growth and pathogen resistance. Yet, very little is known about their influence on herbivores and higher trophic levels. We studied the origin and role of a major bacterial VOC, 2,3-butanediol (2,3-BD), on plant growth, pathogen and herbivore resistance, and the attraction of natural enemies in maize. One of the major contributors to 2,3-BD in the headspace of soil-grown maize seedlings was identified as Enterobacter aerogenes, an endophytic bacterium that colonizes the plants. The production of 2,3-BD by E. aerogenes rendered maize plants more resistant against the Northern corn leaf blight fungus Setosphaeria turcica. On the contrary, E. aerogenes-inoculated plants were less resistant against the caterpillar Spodoptera littoralis. The effect of 2,3-BD on the attraction of the parasitoid Cotesia marginiventris was more variable: 2,3-BD application to the headspace of the plants had no effect on the parasitoids, but application to the soil increased parasitoid attraction. Furthermore, inoculation of seeds with E. aerogenes decreased plant attractiveness, whereas inoculation of soil with a total extract of soil microbes increased parasitoid attraction, suggesting that the effect of 2,3-BD on the parasitoid is indirect and depends on the composition of the microbial community., (© 2013 John Wiley & Sons Ltd.)

Plants respond to herbivory by reprogramming their metabolism. Most research in this context has focused on locally induced compounds that function as toxins or feeding deterrents. We developed an ultra-high-pressure liquid chromatography time-of-flight mass spectrometry (UHPLC-TOF-MS)-based metabolomics approach to evaluate local and systemic herbivore-induced changes in maize leaves, sap, roots and root exudates without any prior assumptions about their function. Thirty-two differentially regulated compounds were identified from Spodoptera littoralis-infested maize seedlings and isolated for structure assignment by microflow nuclear magnetic resonance (CapNMR). Nine compounds were quantified by a high throughput direct nano-infusion tandem mass spectrometry/mass spectrometry (MS/MS) method. Leaf infestation led to a marked local increase of 1,3-benzoxazin-4-ones, phospholipids, N-hydroxycinnamoyltyramines, azealic acid and tryptophan. Only few changes were found in the root metabolome, but 1,3-benzoxazin-4-ones increased in the vascular sap and root exudates. The role of N-hydroxycinnamoyltyramines in plant-herbivore interactions is unknown, and we therefore tested the effect of the dominating p-coumaroyltyramine on S. littoralis. Unexpectedly, p-coumaroyltyramine was metabolized by the larvae and increased larval growth, possibly by providing additional nitrogen to the insect. Taken together, this study illustrates that herbivore attack leads to the induction of metabolites that can have contrasting effects on herbivore resistance in the leaves and roots., (© 2012 Blackwell Publishing Ltd.)

Plants attacked by leaf herbivores release volatile organic compounds (VOCs) both locally from the wounded site and systemically from non-attacked tissues. These volatiles serve as attractants for predators and parasitoids. This phenomenon is well described for plant leaves, but systemic induction of VOCs in the roots has remained unstudied. We assessed the spatial and temporal activation of the synthesis and release of (E)-β-caryophyllene (EβC) in maize roots upon feeding by larvae of Diabrotica virgifera virgifera, as well as the importance of systemically produced EβC for the attraction of the entomopathogenic nematode Heterorhabditis megidis. The production of EβC was found to be significantly stronger at the site of attack than in non-attacked tissues. A weak, but significant, increase in transcriptional activity of the EβC synthase gene tps23 and a corresponding increase in EβC content were observed in the roots above the feeding site and in adjacent roots, demonstrating for the first time that herbivory triggers systemic production of a volatile within root systems. In belowground olfactometers, the nematodes were significantly more attracted towards local feeding sites than systemically induced roots. The possible advantages and disadvantages of systemic volatile signalling in roots are discussed., (© 2011 Blackwell Publishing Ltd.)

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., (© 2011 Blackwell Publishing Ltd.)