Evolutionary trade-offs in plant immunity: prioritizing antiviral priming by herbivore-induced plant volatiles over defense against herbivores.

Antipathogen defense; b-caryophyllene; vector-virus mutualism Plants respond to insect herbivory by producing and releasing distinctive blends of volatile compounds. These herbivore-induced plant volatiles (HIPVs) serve several roles, including direct defense through toxic or repellent effects on herbivores and indirect defense by attracting the herbivores' natural enemies (Bleeker et al. 2009; Veyrat et al. 2016). HIPVs also act as warning signals, informing undamaged tissues within the same plant and nearby plants of a pending insect attack (Heil and Bueno 2007). HIPVs are mostly composed of terpenes, fatty acid-derived compounds, and shikimic acid pathway metabolites. In response to certain HIPVs, neighboring plants enter a primed state, preparing for a future attack. As a result, when these primed plants are later attacked by the same herbivore, they can mount a faster and stronger defense response (Arimura et al. 2009). However, many specialized herbivores and pathogens can overcome, and often manipulate, these defenses to thrive on their specific host plants. Some insect vectors have evolved mutualisms with their viruses, e.g., some begomoviruses suppress terpenoid emissions that negatively affect their whitefly vectors (Bleeker et al. 2009). HIPV emissions vulnerable to manipulation include the generalist whitefly Bemisia tabaci-induced volatile blend (composed of the monoterpenes b-myrcene and q-cymene, and the sesquiterpene b-caryophyllene). These whitefly-induced volatiles prime salicylic acid-dependent defenses against pathogens in tomato plants while suppressing jasmonic acid-dependent defenses against herbivores, thus rendering neighboring tomato plants more susceptible to whiteflies (Zhang et al. 2019). This appears to be paradoxical and warrants further investigation. Although numerous species can attack plants simultaneously or sequentially, prior research has mostly focused on HIPV production in a single plant-herbivore or plant-pathogen interaction. Less is known about how plants respond to volatiles released by neighboring plants under simultaneous attack by multiple aggressors. Some studies suggest that plants may be able to distinguish volatile blends emitted by neighbors, attacked simultaneously by both viruses and their vectors, thereby priming appropriate defenses against each (Gong et al. 2023). A recent study by Zhang et al. (2026) examines the three-way interaction between tomato, the herbivorous whitefly B. tabaci, and the begomoviruses transmitted by this insect, namely, the tomato yellow leaf curl virus (TYLCV) and the papaya leaf curl China virus (PaLCuCNV). In this system, Zhang et al. (2026) investigated whether neighboring plants discriminate, through airborne cues, not only between herbivory but also between herbivory associated with virus risk. The group proved that the HIPV b-caryophyllene is induced earlier and more strongly after infestation by viruliferous whiteflies (insects harboring the virus) than after infestation by non-viruliferous whiteflies, whereas other volatiles in the same system, including methyl salicylate and b-myrcene, do not show the same distinctive early signature. The high b-caryophyllene level was a significant cue for neighboring plants to prime their defense mechanisms against the virus rather than the herbivore. The timing and context of b-caryophyllene release encode biologically specific information in this tri-trophic interaction, during vector-borne viral infection. Exposing neighboring plants to b-caryophyllene primes salicylic-acid-associated antiviral responses, including higher PR-1b and Ty-1 expressions, lowers virus accumulation under whitefly-mediated infection and enhances indirect defenses (Zhang et al. 2026). Zhang et al. (2026) used both synthetic b-caryophyllene and transgenic TPS12-overexpressing tomato lines to show that tomato lines constitutively emitting b-caryophyllene exhibit stronger resistance against viruses vectored by whiteflies. They further found that this is genotype-specific and only a subset of tomato genotypes exhibit significant viruliferous-whitefly-induced increases in b-caryophyllene emission and corresponding priming of PR-1b. This represents a conceptual shift from earlier interpretations of whitefly-induced volatile effects as those that largely favored the specialized insect herbivore (Zhang et al. 2019). In an earlier study from the same research group, volatile exposure was shown to suppress anti-whitefly defense while enhancing anti-pathogen defense in neighbors (Zhang et al. 2019), suggesting that plants were being manipulated to lower anti-herbivore defenses to the benefit of whiteflies. The present paper reinterprets that trade-off and shows that perhaps the plant is not being manipulated into making a mistake, but is instead making an adaptive allocation decision, prioritizing defense against the costlier threat of the virus. Rather than treating induced compounds simply as defense outputs, Zhang et al. (2026) show them as context-dependent signals, whose meaning depends on who is doing the attacking, what pathogen that attacker carries, and when the cue is released. The possibility that pathogens can also influence parasitoid foraging behavior was demonstrated by Martini et al. (2014), who reported for the first time that a parasitoid was "eavesdropping" on bacterial pathogen-mediated emission of methyl salicylate. Therefore, exploring the multitrophic relationships between plants, herbivores, pathogens, and parasitoids can help us understand the function of chemical signals in population regulation within an ecosystem. According to Zhang et al. (2026), the harm caused by begomoviruses, such as leaf stunting, yellowing, curling, and flower abortion, is more damaging and longer lasting than that caused by herbivores. This could be the reason why a plant would strategically favor antiviral defenses over anti-herbivore defenses when herbivores carry viruses. Plants may thus maximize their overall fitness under selection pressure from multiple invaders by using this trade-off mechanism to mitigate the effects of the more hazardous virus over herbivory. While there is evidence that b-caryophyllene has antimicrobial properties against certain bacterial species, which suggests possible direct viricidal effects, it remains unclear whether b-caryophyllene is directly viricidal or whether host physiology mediates its inhibitory effect on viral accumulation. Zhang et al. (2026) showed that, in the absence of a vector, exposure to b-caryophyllene alone does not activate antipathogen defenses. However, when viruliferous insects attack, antipathogen genes are upregulated, leading to reduced virus accumulation. No such upregulation of antipathogen genes was seen when b-caryophyllene was exposed to other host plants, such as tobacco and sweet pepper. b-caryophyllene thus does not act directly against viruses vectored by B. tabaci but rather enhances plant resistance to such pathogens through an indirect mechanism. The intricacy of plant defensive mechanisms in multiple-attacker situations was highlighted by the recent study of Zhang et al. (2026), which showed that b-caryophyllene is an airborne cue in the intricate interactions among plants, insect vectors, and related viruses. A fresh viewpoint on virus-vector mutualism is now available to investigate its potential use in the long-term control of insect-borne viruses. There is ongoing discussion on how HIPVs affect plant fitness when used for sustainable pest management. Hilgers et al. (2021) achieved the production of b-caryophyllene in the heterologous host Rhodobacter capsulatus and found that it significantly inhibited the growth of the destructive pathogen Sclerotinia sclerotiorum, causing white mold disease, and a devastating plant vascular wilt-causing fungus Fusarium oxysporum, indicating its applicability for the management of certain plant pathogenic fungi in agricultural crop production. Gao et al. (2024) demonstrated the increased stability of b-caryophyllene using nanoliposomes during a 14-day storage period, and its effective insecticidal activity against B. tabaci, which outperformed thiamethoxam, a widely used insecticide for whitefly management. Zhang et al. (2026) found that when plants are exposed to b-caryophyllene and infested with viruliferous whiteflies, their seed production increases, they attract parasitoids, and their virus load decreases. Importantly, a recent study cautions against the use of b-caryophyllene to develop kairomone-based insect lures, as it attracts the cacao mirid bug Helopeltis bakeri (Tavera et al. 2023). However, b-caryophyllene is a highly pleiotropic ecological signal; as a terpene negatively impacting pests such as Spodoptera litura (Mahajan et al. 2022) and Myzus persicae (Chohan et al. 2023); as an alternative to methyl eugenol for the concurrent use of the male annihilation technique and sterile insect technique in fruit fly (Bactrocera zonata) management (ul Haq et al. 2024); as a lure for parasitoids (Zhang et al. 2020) and as a gender-specific terpene produced by predators (Brown et al. 2006). b-caryophyllene has already been implicated in direct and indirect defense, in herbivore attraction or repellence depending on context, and in broader volatile signaling networks. Because of these multiple effects, one must be careful not to overstate the specificity of b-caryophyllene. Secondly, whether neighboring plants perceive b-caryophyllene itself as a uniquely informative cue of virus risk, rather than a proxy embedded in a broader blend or exposure history, remains an open mechanistic question. After careful consideration of the organisms involved, b-caryophyllene may be incorporated to manage vector-borne viral diseases, for example, by using cultivars that show strong antipathogen defenses upon exposure to this sesquiterpene.