Dispensing a synthetic green leaf volatile to two plant species in a common garden differentially alters physiological responses and herbivory

Abstract

Highlight: Long-term exposure to a ubiquitous herbivore-associated volatile cue results in 30 species-specific fitness effects. Differential cue-mediated growth/defense tradeoffs have 31 important implications for plant-herbivore interactions. 32 33 34 35 36 2 Abstract 37 Herbivore-induced plant volatile (HIPV)-mediated eavesdropping is a well-documented, 38 inducible phenomenon that should-like any inducible phenomenon-incur fitness costs. Yet, 39 ecological costs associated with volatile exposure alone are unclear. In a common garden 40 experiment, we tested the hypothesis that exposure to a single HIPV would decrease herbivore 41 damage at the cost of reduced plant growth and reproduction. Lima bean (Phaseolus lunatus) and 42 pepper (Capsicum annuum) plants were exposed to a persistent, low-dose (~10ng/hour) of the 43 green leaf volatile cis-3-hexenyl acetate (z3HAC), a ubiquitous HIPV. z3HAC-treated pepper 44 plants were shorter, had less aboveground and belowground biomass, and produced fewer 45 flowers and fruits relative to controls while z3HAC-treated lima bean plants were taller and 46produced more leaves and flowers than did controls. Natural herbivory was reduced in z3HAC-47 exposed lima bean plants, but not in pepper. Cyanogenic potential, a putative defense 48 mechanism in lima bean, was lower in z3HAC-exposed leaves, suggesting a growth-defense 49 tradeoffs from z3HAC exposure alone. Plant species-specific responses to an identical priming 50 cue have important implications for ecological costs and benefits of volatile-mediated inter-plant 51 communication under field conditions. 52 53 Key Words -cis-3-hexenyl acetate, eavesdropping, lima bean, pepper, plant fitness, plant 54 volatiles 55 56 Abbreviations used-cis-3-hexenyl acetate (z3HAC), Herbivore-induced plant volatile (HIPV), 57 Green-leaf volatile (GLV) 58 59 60 Production and utilization of airborne chemical cues is prevalent within the plant 61 kingdom. Plants depend on airborne chemical signaling for pollination (Muhlemann et al., 62 2014), indirect defense (Mumm and Dicke, 2010), protection from pathogens (Farag et al., 632013), and herbivore resistance (Frost et al., 2008c). Volatile communication is also pivotal for 64 plant-plant signaling, and selection for such signaling depends on honest cues that reliably confer 65 ecologically relevant information. For example, herbivory is a fundamental ecological 66 interaction that impacts plant fitness, and many plants increase the production and emission of 67 volatile compounds in response to herbivore damage (Turlings et al., 1995). Such herbivore-68 induced plant volatiles (HIPVs) are potentially reliable cues around which plant-plant 69 eavesdropping could be evolutionarily adaptive(Rodriguez-Saona and Frost, 2010). Undamaged70

Integration of two herbivore‐induced plant volatiles results in synergistic effects on plant defence and resistance

“…Green leaf volatiles (GLVs) such as ( Z )‐3‐hexenal, ( Z )‐3‐hexen‐1‐ol, and ( Z )‐3‐hexenyl acetate (HAC) can induce and prime the expression of jasmonate biosynthesis genes, the production of jasmonates, and the emission of volatile terpenes (Engelberth et al, ). HAC can also modulate defense and growth in other plants such as poplar, lima bean and pepper (Frost et al, , Freundlich & Frost, ).The volatile phytohormone ethylene has been shown to increase the release of maize volatiles that are induced by ( Z )‐3‐hexen‐1‐ol (Ruther & Kleier, ). The aromatic volatile indole primes jasmonates and volatile terpenes and is required for within‐plant priming of monoterpenes (Erb et al, ).…”

Plant seeds are primed by herbivore-induced plant volatiles

“…Exposure of M. truncatula seeds to two GLVs ( z 3HOL and z 3HAC) stimulated vegetative growth. Our group has recently seen similar vegetative and reproductive growth stimulation using a low-dose, persistent application of z 3HAC in lima bean plants (Freundlich & Frost, 2018). In lima bean and M. truncatula , plants with increased growth also were better defended ((Freundlich & Frost, 2018) and Figs 1&3).…”

“…Our group has recently seen similar vegetative and reproductive growth stimulation using a low-dose, persistent application of z 3HAC in lima bean plants (Freundlich & Frost, 2018). In lima bean and M. truncatula , plants with increased growth also were better defended ((Freundlich & Frost, 2018) and Figs 1&3). GLVs are well-established priming cues against biotic stress (Engelberth et al , 2004; Frost et al , 2008c), and volatile communication between plants can alter biomass allocation (Ninkovic, 2003).…”

“…Our results suggest that GLVs can also stimulate plant growth and ostensibly overcome the growth-defense dilemma (Herms & Mattson, 1992) in some plant species. One caveat, though, is that our group also has shown that persistent exposure to z 3HAC reduces growth in Capsicum annuum (Freundlich & Frost, 2018), therefore the stimulating effect of GLVs is not universal.…”

Plant–Plant Communication: Is There a Role for Volatile Damage-Associated Molecular Patterns?

“…As addressed by Heil and Walters (2009) (VOC-mediated) induced systemic resistance seems to come with ecological costs. This effect is again highly species-specific and strongly dependent on the applied volatile, which was shown in a field study where lima bean and pepper (Capsicum annuum) were exposed to low doses of (Z)-3-hexenyl acetate for 7 days (Freundlich and Frost, 2019). Volatile treatment resulted in increased leaf Push-pull-intercropping systems DIV/cVOC For a full review see Pickett et al, 2014 Plant extracts DAMP For a full review see Quintana-Rodriguez et al, 2018 DIV, damage-induced volatiles; HIPV, herbivore-induced volatiles; cVOC, constitutive volatiles; GLV, green leaf volatiles; GMO, genetically modified organism; n.a., not applicable.…”