Dispensing a Synthetic Green Leaf Volatile to Two Plant Species in a Common Garden Differentially Alters Physiological Responses and Herbivory

Abstract

Herbivore-induced plant volatile (HIPV)-mediated eavesdropping by plants is a well-documented, inducible phenomenon that has practical agronomic applications for enhancing plant defense and pest management. However, as with any inducible phenomenon, responding to volatile cues may incur physiological and ecological costs that limit plant productivity. In a common garden experiment, we tested the hypothesis that exposure to a single HIPV would decrease herbivore damage at the cost of reduced plant growth and reproduction. Lima bean (Phaseolus lunatus) and pepper (Capsicum annuum) plants were exposed to a persistent, low dose (~10 ng/h) of the green leaf volatile cis-3-hexenyl acetate (z3HAC), which is a HIPV and damage-associated volatile. z3HAC-treated pepper plants were shorter, had less aboveground and belowground biomass, and produced fewer flowers and fruits relative to controls, while z3HAC-treated lima bean plants were taller and produced more leaves and flowers than did controls. Natural herbivory was reduced in z3HAC-exposed lima bean plants, but not in pepper. Cyanogenic potential, a putative direct defense mechanism in lima bean, was lower in young z3HAC-exposed leaves, suggesting a growth–defense tradeoff from z3HAC exposure alone. Plant species-specific responses to an identical volatile cue have important implications for agronomic costs and benefits of volatile-mediated interplant communication under field conditions.

Volatile Dimethyl Disulfide from Guava Plants Regulate Developmental Performance of Asian Citrus Psyllid through Activation of Defense Responses in Neighboring Orange Plants

“…Meanwhile, plant defense is costly, as the activation of defense responses requires a significant investment of resources toward defense production [ 57 , 58 ]. These costs are typically measured as a reduction in plant fitness (e.g., survivorship, growth, and reproduction) in the absence of herbivores, and thus tradeoffs exist between investment in defenses and investment in growth and reproduction [ 59 , 60 , 61 ]. Interestingly, the perception of early reliable cues may allow a plant to anticipate a probable attack and prime its defenses before herbivory occurs.…”

“…We hypothesize that DMDS at the current concentration primes defense responses in orange plants. In addition, there are tradeoffs between defenses against herbivores and pathogens, or even against different herbivore species, so that defense against one may increase susceptibility to another, which would be consistent with an SA–JA tradeoff [ 60 , 64 , 65 ]. Thus, the utility of DMDS in field applications will depend on the impact at the community level.…”

“…It will be important to further evaluate the field application of DMDS in citrus orchards, as well as the tradeoff between the ecological costs and the fitness benefits of DMDS-induced resistance. In addition, enhancing plant immunity will depend on the plant’s life history, physiology, and other ecological factors, to determine whether a plant would benefit from eavesdropping volatile cues and what impact volatile-mediated eavesdropping might have on plants and their insect pests [ 60 ]. An important goal for future research is to determine how citrus plants integrate volatile cues, including volatile sulfurs and terpenoids in their environment, to optimize defense investments.…”

Early damage enhances compensatory responses to herbivory in wild lima bean

“…Induction of enhanced growth by volatiles has been shown for some plant species, including Arabidopsis thaliana ( Shimola and Bidart, 2019 ), Brassica sp. ( Pashalidou et al., 2020 ), lima bean ( Freundlich et al., 2021 ) and Medicago trunculata ( Maurya et al., 2022 ). In Brassica , volatiles emitted by plants infested with eggs of Pieris brassicae induce a higher reproductive output in undamaged exposed plants than in plants not exposed to volatiles.…”

(Z)‐3‐hexenol primes callose deposition against whitefly‐mediated begomovirus infection in tomato

“…Green leaf volatiles (GLVs), for example, are very quickly produced and/or emitted upon herbivory or pathogen infection by almost every green plant (Scala et al., 2013). GLVs have been found to contribute to the defense of plants against pest insects and pathogens by direct defense activation and defense priming (Ameye et al., 2015; Engelberth et al., 2004; Freundlich et al., 2021; Frost, Mescher, Dervinis et al., 2008; Kishimoto et al., 2005; Yang et al., 2020). However, little is known about the effects of priming by GLVs on plant–virus interactions (Hammerbacher et al., 2019; Heil, 2014), and thus whether defense priming can be useful for the biological control of viral diseases warrants study.…”