Volatile-mediated plant-plant interactions: volatile organic compounds as modulators of receiver plant defence, growth, and reproduction

Abstract

It is firmly established that plants respond to biotic and abiotic stimuli by emitting volatile organic compounds (VOCs). These VOCs provide information on the physiological status of the emitter plant and are available for detection by the whole community. In the context of plant-plant interactions, research has focused mostly on the defence-related responses of receiver plants. However, responses may span hormone signalling and both primary and secondary metabolism, and ultimately affect plant fitness. Here we present a synthesis of plant-plant interactions, focusing on the effects of VOC exposure on receiver plants. An overview of the important chemical cues, the uptake and conversion of VOCs, and the adsorption of VOCs to plant surfaces is presented. This is followed by a review of the substantial VOC-induced changes to receiver plants affecting both primary and secondary metabolism and influencing plant growth and reproduction. Further research should consider whole-plant responses for the effective evaluation of the mechanisms and fitness consequences of exposure of the receiver plant to VOCs.

Keywords: Defence; green leaf volatiles; growth; photosynthesis; plant–plant communication; primary metabolism; priming; reproduction; secondary metabolism; terpenes; volatile organic compounds.

Fig. 1.

Summary of known changes occurring in receiver plants induced by volatile cues. By influencing the rate of photosynthesis, nutrient assimilation, and hormone signalling, VOCs might reconfigure the primary and secondary metabolism to support physiological adjustments in receiver plants. Physiological adjustments to VOCs are characterized by an increase in defences before and upon stress in receivers, such as a greater production of extrafloral nectar (Kost and Heil, 2006; Choh et al., 2006), volatile emissions (Engelberth et al., 2004; Li and Blande, 2017), and proteinase inhibitors (Farmer and Ryan, 1990; Kessler et al., 2006). VOCs can also influence receiver plant performance by affecting root and shoot growth (Ninkovic, 2003; Engelberth and Engelberth, 2019) and their reproduction (Kost and Heil, 2006; Pashalidou et al., 2020).

Fig. 2.

Ecological consequences of emitting and receiving volatile cues. The arrows indicate the direction of VOC transport. The boxes indicate the potential outcomes of the response and whether the emitter or receiver gains a beneficial (+) or a detrimental (-) effect on fitness. SAR indicates that the emitting plant may gain systemic acquired resistance. We refer to allelopathy as a phenomenon whereby the emitter releases chemicals that have detrimental effects on the performance of the receiver plant (Inderjit and Duke, 2003). Eavesdropping is the process whereby a receiver intercepts and uses information encoded in chemical cues that evolved to provide information to a different recipient (Karban, 2015). MBH indicates the mutual-benefits hypothesis, whereby the emitter and receiver benefit from the transport of VOC cues, irrespective of their relatedness, through the responses of receivers reducing the risk of herbivory (Kalske et al., 2019).