Detecting the enemy or being manipulated by your attacker? Herbivore-derived elicitors of plant responses: an introduction to a Virtual Issue

Abstract

Plants have evolved unique ways of processing environmental information to adjust their physiology, metabolism and growth to various environmental conditions. One such environmental condition is the consumption of their tissues by herbivores. Plants respond to herbivory with significant transcriptional and metabolic reconfigurations. Some of the metabolic changes, specifically those to secondary metabolism, can mediate increased resistance to the attacking herbivores, mostly through the increased production of toxic, antidigestive, antinutritive and repellant compounds or, simply, by altered compound composition or diversity (Kessler & Baldwin, 2002). In all cases, plant responses can be strikingly specific to the attacking herbivore species or even the developmental stage of the attacker (Barrett & Heil, 2012). The question of how these responses can be so specific and the role of induced response to herbivory in driving population-, community- and ecosystem-dynamics is a major driver of research in plant physiology and molecular biology as well as plant and chemical ecology (Kessler & Kalske, 2018). In this Editorial, we introduce a Virtual Issue of New Phytologist articles that highlight some of these recent developments in the study of herbivore-derived elicitors of plant responses.

Research into the mechanisms underlying induced responses to herbivory has long focused on the molecular response patterns associated with wounded plant tissue, known as damage-associated molecular patterns (DAMPs). This involves a complex wound signaling network that is driven by crosstalk between plant hormones, including ethylene, jasmonates and salicylates (Tanaka & Heil, 2021). The extent to which each of the pathways is triggered relative to the others can explain the high specificity with which downstream metabolic responses are regulated. However, what are the primary triggers and how are alterations in responses regulated?

There is an increasing number of chemical elicitor compounds (compounds produced by organisms interacting with the plant) identified that either directly trigger or specifically alter standard wound responses. The most commonly studied elicitors are herbivore oral secretions and oviposition fluid-derived substances (Jones et al., 2022), and volatile organic compounds from neighboring plants (Kessler et al., 2023). Both represent diverse groups of chemicals that provide specific information about organisms interacting with the plant and even allow the prediction of oncoming future herbivory or pathogen infection.

The study of elicitor-mediated herbivory-associated molecular patterns (HAMPs) (Mithoefer & Boland, 2012) began with the identification of caterpillar saliva-derived β-glucosidase (Mattiacci et al., 1995) and a caterpillar regurgitant-derived fatty acid-amino acid conjugate, volicitin (Turlings et al., 2000), as elicitors of specifically induced volatile organic compounds. Shortly after, additional fatty acid-amino acid conjugates as well as inceptins, caelipherins and bruchins were identified as elicitors from various herbivore species and body fluids that triggered specific metabolic responses in plants (Kessler & Baldwin, 2002; Jones et al., 2022). Interestingly, not all plant species can perceive all elicitor compounds, nor do there seem to be elicitors that are widely distributed among herbivore species, suggesting coevolutionary interactions between plants and their attackers on both the perceptions and generation of herbivore-specific information (Schmelz et al., 2009; Louis et al., 2013). Central to the study of the ecological consequences and thus the function of elicitor compounds is the question of who is in the driver seat, plant or arthropod attacker, when it comes to manipulating each other's behavior through chemical signaling. Recent studies seemingly begin to paint the picture of a continuum from the plant manipulating its attacker to the attacker manipulating the plant through elicitor-mediated signaling, which can be interpreted as different stages in an evolutionary arms race to control plant signaling for fitness advantages for the respective interactors (Jones et al., 2022; Fig. 1).

The initial wave of identifying herbivore-derived elicitor compounds was biased toward oral secretions of chewing insect herbivores (Lepidoptera, Caelifera and Coleoptera), most notably because relatively large amounts of sample were necessary to identify active compounds through bioassay-guided fractionation out of a complex mix of oral compounds with unknown biosynthetic origins. Moreover, the ability of elicitor mixtures to fundamentally affect plant endogenous signaling and metabolic reconfigurations suggested potential benefits of the chemical information transfer to both interactor categories, plants and their attackers. Thus, almost immediately after the identification of the first herbivore-derived elicitors, two fundamental questions became apparent: (1) to what extent do the elicitor compounds allow plants to detect attacking herbivores and mount appropriate defense responses vs being metabolically manipulated to the advantage of the attacker (Jones et al., 2022)? And (2) what is the biosynthetic origin of the elicitor compounds? Some of the elicitor compounds, such as inseptins (Schmelz et al., 2006) and volicitin (Spiteller et al., 2000), were found to derive, at least in part, from plant tissue breakdown products. In addition, microbial endosymbionts of chewing herbivores have been hypothesized as the originators of parts or entire groups of predominantly Lepidoptera-derived elicitor compounds (Yamasaki et al., 2021).

Both plant-derived DAMPs and bacterial metabolites or conjugates are presumably unavoidable to the attacking insect and are thus ideal cues that allow plants to detect their attackers, suggesting that it is also a benefit to the plants to be able to detect elicitor compounds. For example, two new salivary gland proteins, tetranin 1 and 2 (Tet 1, 2), have recently been isolated from the salivary secretions of the two-spotted spider mite, Tetranychus urticae, and found to trigger jasmonate, salicylate and abscisic acid-mediated signaling. Thus, Tet1 and Tet2 are key elicitors allowing plants to detect the spider mites and to mount both direct and indirect defense responses (Iida et al., 2019). The structural and functional differences between Tet1 and Tet2 seem to allow for the fine-tuning of the plant responses specifically to T. urticae spider mites. While the functions of tetranins in the spider mites are currently not known, another recently identified spider mite-derived elicitor has been found to be crucial for the mites' own metabolism. TE16, a protein disulfide isomerase isolated from Tetranychus evansi spider mites, triggers reactive oxygen species (ROS) accumulation and subsequent hypersensitive response (HR) as well as jasmonate signaling-related responses and callus formation in Nicotiana benthamiana plants. Genetic silencing of Te16 expression in spider mites reduced their hatchability and survival, suggesting a crucial function of Te16 for spider mite metabolism and development. Reciprocally, expression of Te16 in N. benthamiana plants resulted in constitutively higher resistance of the plants to spider mites (Cui et al., 2024).

A highly attacker-specific elicitation of a rather general ROS-mediated response was also found in Arabidopsis, treated with the oral secretions of the generalist lepidopteran herbivore, Helicoverpa armigera (Chen et al., 2025). In this example, the oral secretion elicits BRI1-ASSOCIATED RECEPTOR KINASE1 and a BOTRYTIS-INDUCED KINASE1-mediated ROS burst that facilitates the hydrolyzation of glucosinolates and the resulting exposure of the attacker to the toxic hydrolysis products (Chen et al., 2025).

A similar cooption of essential herbivore metabolites as elicitors of plant responses has recently been identified in rice. Like most oviparous invertebrates and vertebrates, the development and fecundity of the planthopper species, Nilparavata lugens, depend on an essential and major yolk protein precursor called Vitellogenins (Vgs). Zeng et al. (2023) found that, similar to TE16 from spider mites, Vgs from planthoppers elicit major direct and indirect defense responses in rice plants. This utilization of compounds essential to the attacker by the plant to mount effective resistance has long been a core argument to understand the evolution of elicitor compound perception in plants.

The inducibility of plant metabolism in response to environmental cues is inherently manipulatable by an interacting organism that can change plant metabolism for its own benefits. A recent study by Yamasaki et al. (2021) supported the increasing notion that herbivore-derived elicitors, including those components derived from bacterial endosymbionts, can also allow the attacking herbivore to manipulate the plant to its own advantage. In this elegant study, the authors demonstrated that bacteria in the oral secretions of the tobacco cutworms, Spodoptera litura, inhibit the oxylipin signaling-dependent wound responses of Arabidopsis plants while inducing salicylic and abscisic acid-dependent responses. Such an attenuation of regular wound responses led to enhanced performance of the cutworms with an intact oral microbial flora in comparison with cutworms without their oral bacteria (Yamasaki et al., 2021).

A similar plant-manipulating function was found for specific compounds in the larval oral secretions of cotton bollworm, H. armigera. Chen et al. (2023) identified a venom R-like protein, highly accumulated secretory protein 1 (HAS1), in the caterpillars' oral secretions that suppresses wound-induced plant defense responses. HAS1 seems to directly bind and inhibit transcription factors regulating wound signaling and defense compound biosynthesis in cotton and Arabidopsis and so increases the performance of caterpillars on the plant (Chen et al., 2023).

The new findings make a continuum of plant performance outcomes from beneficial (in which the plant negatively affects herbivore performance and behavior) to disadvantageous (in which the herbivore manipulates the plant) more apparent (signaling arms race hypothesis; Jones et al., 2022). They also illustrate the key role of herbivore-derived elicitor-aided endogenous signaling as targets of natural selection in the evolutionary arms race between plants and their attackers. This does suggest that not only the different outcomes observed are indicative of different stages in that arms race but also the outcome of an interaction can be predicted to be a function of the intimacy/interdependence of the interacting plant and herbivore species.

Moreover, the high precision of elicitor-mediated chemical information allows plants to integrate different environmental cues and thus optimize their behavioral response to complex interactions for their own longer term advantage (chemical information hypothesis; Kessler, 2015). This way, chemical elicitors are a key part of the information that allows plants to adjust their metabolism to optimize their fitness outcome to an entire interaction community, including antagonist herbivores and pathogens as well as mutualists, such as pollinators, predators (indirect defenses) and microbial symbionts.

The commonly observed high specificity of elicitation on both the attacker's and the plant's side is a major prediction of the signaling arms race hypothesis. A number of studies, recently published in New Phytologist, would seem to support this hypothesis. For example, different host strains of the fall armyworm, Spodoptera frugiperda, induce different defense metabolism in maize and Bermuda grass. The differences seem to be associated with the S. frugiperda strain-specific expressions of the salivary enzyme, phospholipase C, which suggests that the specificity of elicitor compound production may determine herbivore-host plant association (Acevedo et al., 2018).

Similarly, elicitor compounds in Pieris spp. oviposition fluids have been known to induce HR-like necrosis in their Brassica spp. host plants, with the result that the eggs would desiccate and die. Griese et al. (2021) reported that egg-killing HR-like necrosis is host plant clade-specific and so is a likely subject of a signaling arms race. This conclusion is reiterated by the fact that the same type of oviposition-mediated elicitation can prime the plant for higher susceptibility to the emerging offspring in certain host plant–herbivore pairings (Stahl et al., 2023). Finally, in accordance with a signaling arms race hypothesis, plant responses should vary with the intimacy of the relationship between the plant and the eliciting herbivore. Indeed, coexistence histories, breadth of diet and feeding modes of 10 tested herbivore species were found to be the highest predictors for the specificity of herbivore-induced plant volatile (HIPV) emissions in native Brassica rapa (Danner et al., 2018).

In contrast to the signaling evolutionary arms race hypothesis, a major prediction of the chemical information hypothesis is that the integration of chemical signaling helps plants to optimize their responses to multiple attackers. Accordingly, Fernández de Bobadilla et al. (2021) found that Brassica nigra plants induce guild-specific defense responses when attacked by multiple herbivore species in the same feeding guild (e.g. piercing and sucking vs chewing herbivores). However, when exposed to attackers from multiple feeding guilds, plants integrate the available information to optimize their responses to a functionally diverse herbivore community (Fernández de Bobadilla et al., 2021).

The optimization of plant responses to a functionally diverse herbivore community relies on the precision of the chemical information available. It has become increasingly clear that a substantial part of this information is in the form of HIPVs produced in distal tissues of the same plant or neighboring plants (Kessler et al., 2023). While traditionally not considered elicitor compounds, it is becoming clear that the information transferred by HIPVs is ultimately elicited by the feeding of a herbivore and can be highly specific to the herbivory on the attacked emitter plant. Included in this Virtual Issue is one of the first papers published on the specificity of HIPV-mediated plant–plant communication (Moreira et al., 2018) as well as studies on the multiple functions of HIPV production (Kessler, 2018).

More recent studies explore the understanding of the mechanism of this specificity of HIPV-mediated plant–plant signal transduction. For example, cotton plants exposed to neighboring plants that were attacked by the generalist herbivore, S. frugiperda, were found to respond specifically to the de novo-induced HIPVs. More interestingly, the HIPVs seem to elicit defense gene expression and herbivore resistance that mirror defense expression in the herbivore-attacked emitter plants (Grandi et al., 2024). This finding suggests some sort of concerted processing and translation of chemical information into a standard HIPV signal or a fundamental role of HIPVs in signal transduction within and between plants in general. Potentially underlying similar mechanisms, volatile compounds emitted from Arabidopsis plants that received eggs of the specialist Pieris brassicae elicit a similar systemic acquired resistance (SAR) response in an unchallenged neighboring plant. This SAR provides cross-resistance with pathogens such as Pseudomonas syringae (Orlovskis & Reymond, 2020).

Alternatively, plants can take up herbivore-induced compounds emitted by neighboring plants and directly turn them into defense compounds, resulting in similar specific defense responses, yet through a fundamentally different mechanism. Herbivore damage to maize plants elicits highly specific HIPV emissions that include indole in its bouquet of compounds. Sorg et al. (2025) demonstrated that indole does not only elicit a change in the metabolism of undamaged neighboring plants but also gets directly converted into defensive benzoxazinoids, such as DIMBOA-glucoside.

These new findings on HIPV-mediated plant–plant communication suggest a greater role of volatile organic compounds in signaling in general and in the herbivore specificity of elicitor-mediated responses in plants.

The signaling arms race and chemical information hypothesis for elicitation are not mutually exclusive, but recent findings suggest that the integration of information for optimized responses (e.g. the chemical information hypothesis) as well as defense induction (e.g. induced defenses) or manipulation by the insects are three potential outcomes of an arms race continuum on herbivore elicitor-mediated signaling (Fig. 1). Within this framework, it becomes abundantly clear that arthropod oviposition, galling and mining insects are perceived by plants much like pathogens when observing the phytohormone induction of attacked plants (Raffa et al., 2020). These types of interactions also include the most striking examples of herbivores manipulating the plants to their own advantages. For example, galling insects are able to utilize phytohormone or phytohormone-like elicitor compounds to put plants on alternative developmental trajectories, providing high-quality food and shelter to the manipulating insect (Harris & Pitzschke, 2020). This is in stark contrast to the commonly observed, often specific, induced resistance responses that are mediated by chewing herbivore-derived elicitor compounds (Jones et al., 2022). The next steps in this line of research need to include a thorough investigation of the molecular mechanisms through which elicitor compounds affect primary and secondary metabolism. This will allow us to answer an even more fundamental question on the ecology and evolution of plant signaling mediation of biotic interactions – why are there so many different elicitor compounds, and do different categories of molecular and signaling mechanisms or specific elicitor compound classes mediate the three ecological outcomes of induced defense, manipulation by the attacker or optimization of the interaction network? Some of the recent publications featured in this collection (Iida et al., 2019; Yamasaki et al., 2021; Chen et al., 2023; Cui et al., 2024) have started us on a new path to understanding the complex ways of how plants perceive and respond to their environment.

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