Sequestration of Exogenous Volatiles by Plant Cuticular Waxes as a Mechanism of Passive Associational Resistance: A Proof of Concept

Abstract

Numerous plant-derived volatile organic compounds (VOCs) induce the expression of resistance-related genes and thereby cause an "associational resistance" in neighbouring plants. However, VOCs can also be sequestered by plant cuticular waxes. In case that they maintain their biological activity, such sequestered VOCs could generate a "passive" associational resistance that is independent of any gene expression in the receiver. As a proof of concept, we used major components of the cuticular wax layers of the tree, Parkinsonia praecox, and conidia of Colletotrichum lindemuthianum, a fungal pathogen that has not been reported to infect P. praecox. Wax layers were re-constituted on glass slides and exposed to each of 20 pure VOCs for 1 d and then to ambient air for 1 d or 15 d. Gas chromatography-mass spectrometry (GC-MS) analyses showed that all 20 VOCs were sequestered by the re-constituted wax layers. Exposure to 18 of the VOCs significantly inhibited the germination of C. lindemuthianum conidia on these wax layers after 1 day of exposure to ambient air. Four of the VOCs: 4Z-heptenol, farnesene, limonene, and 2E-decenal, inhibited germination rates to less than 25% of the controls. After 15 d, all VOCs were still detectable, although at strongly reduced concentrations, and no significant inhibition of conidial germination could be detected anymore. Exogenous VOCs can be sequestered by the components of plant cuticular waxes and maintain their biological activity, at least over a certain time span: an effect that could generate a transient "passive associational resistance" to pathogens.

Antagonist effects of the leek Allium porrum as a companion plant on aphid host plant colonization

“…Not only the time to first probe (t > 1Pr), but also the parameters of the pathway phase were unchanged, suggesting that the modifications of M. persicae feeding behavior in the presence of leek were probably not due to physical or chemical changes in epiderm and/or mesophyll tissues. Indeed the hypothesis that leek VOCs could be adsorbed in the sweet pepper leaf cuticle can be ruled out here, although such phenomena have already been shown in other studies 37 , 38 and particularly in a study involving Allium spp . VOCs 39 .…”

Seasonal and environmental variation in volatile emissions of the New Zealand native plant Leptospermum scoparium in weed-invaded and non-invaded sites

“…The composition of volatile blends depends on plant species, organ, developmental stage and physiological status of the emitting plant 6 – 9 . Some plants also adsorb their neighbour’s volatiles and passively re-release them 10 , 11 . However, volatile emission is also extremely plastic, with emissions varying in response to biotic and abiotic factors such as temperature, soil nutrients, herbivory or disease 12 .…”

Social networking in crop plants: Wired and wireless cross‐plant communications

“…Recent studies identified different mechanisms whereby receiver plants perceive VOCs from neighbour plants. VOCs can be absorbed by a wax layer on the epidermal cell, which traps VOCs and slowly releases them to attract or repel herbivores and their parasitoids and entomopathogens (Camacho‐Coronel, Molina‐Torres, & Heil, 2020; Lin et al, 2016).…”

“…In inter‐plant communication, VOCs modulate receiver plant physiology and directly or indirectly affect other plant holobiome members. VOCs captured by receiver plant wax display fungicidal and bactericidal activity for several days (Camacho‐Coronel et al, 2020). GLVs and terpenoid volatiles have strong fungicidal and bactericidal activity in vitro and in planta (Huang et al, 2012; Pontin, Bottini, Burba, & Piccoli, 2015; Quintana‐Rodriguez et al, 2015).…”