Stress-Induced Volatile Emissions and Signalling in Inter-Plant Communication

Abstract

The sessile plant has developed mechanisms to survive the "rough and tumble" of its natural surroundings, aided by its evolved innate immune system. Precise perception and rapid response to stress stimuli confer a fitness edge to the plant against its competitors, guaranteeing greater chances of survival and productivity. Plants can "eavesdrop" on volatile chemical cues from their stressed neighbours and have adapted to use these airborne signals to prepare for impending danger without having to experience the actual stress themselves. The role of volatile organic compounds (VOCs) in plant-plant communication has gained significant attention over the past decade, particularly with regard to the potential of VOCs to prime non-stressed plants for more robust defence responses to future stress challenges. The ecological relevance of such interactions under various environmental stresses has been much debated, and there is a nascent understanding of the mechanisms involved. This review discusses the significance of VOC-mediated inter-plant interactions under both biotic and abiotic stresses and highlights the potential to manipulate outcomes in agricultural systems for sustainable crop protection via enhanced defence. The need to integrate physiological, biochemical, and molecular approaches in understanding the underlying mechanisms and signalling pathways involved in volatile signalling is emphasised.

Keywords: VOCs; abiotic stress; biotic stress; plant–plant interactions; priming; stress signalling; volatile-mediated signalling.

Figure 2

A simplified schematic of the interactions among major VOC biosynthesis pathways in response to stress. (a) VOC emissions respond to biotic and abiotic stresses from both below and aboveground sources of a plant. (b) A generalised VOC emission response to stress is given, which depicts a hormetic-like biphasic pattern. (c) Increased stress results in decreased intercellular CO₂ concentration favouring photorespiration over photosynthesis, which is the source of VOC precursors. (d) Various root-to-shoot signalling molecules that are involved in stress signalling. (e) Membrane depolarisation activities involving ROS accumulation and Ca²⁺ influx as well as stress-induced phytohormones, e.g., ABA, JA, SA, and ET, activate defence signal transduction pathways that trigger gene expression of flux-controlling enzymes, e.g., TPS genes. Stressors affecting leaf temperature (T_leaf) influence the activity of the enzymes. (f) De novo VOC synthesis in the chloroplast and cytosol involves VOC precursors such as G3P (for the MEP pathway) and Ery4P (for the shikimic pathway), PEP from glycolysis, as well as its downstream metabolites pyruvate and acetyl-CoA that are involved in the Shikimic, MVA, and LOX biosynthesis pathways. Note that the sizes of organelles are not drawn to scale. Abbreviations: ABA, abscisic acid; JA, jasmonic acid; SA—salicylic acid; ET, ethylene; TPS, terpene synthase; G3P, glyceraldehyde 3-phosphate; MEP, 2-C-methyl-d-erythritol 4-phosphate; Ery4P, erythrose 4-phosphate; PEP, phosphoenol pyruvate; MVA, mevalonic acid; LOX, lipoxygenase; CLE25, CLAVATA3/EMBRYO-SURROUNDING REGION-RELATED 25; smRNA, small RNAs [114].

Figure 1

Biosynthetic sites, storage, and transport of major plant volatile organic compounds. The four major biosynthetic classes, (a) fatty acids, (b) terpenoids, (c) benzenoids, and (d) amino acids, are represented in the figure. Modification reactions including redox reactions, hydroxylation, acylation, and degradative reactions occur mainly in the cell cytosol. Some reactions may also occur in the membrane-bound sub-cellular compartments such as plastids, mitochondria, and endoplasmic reticulum. Inactive forms of the VOCs such as glycosides are stored in the vacuole, ducts, and other extracellular compartments such as trichomes. Transport of the volatiles is by passive diffusion and possibly via vesicular trafficking by the endoplasmic reticulum, golgi apparatus, and the trans-golgi network. (Modified from Pichersky et al. [51]).

Figure 3

Overview of long distance signals in plants. Long-distance signals include electrical, hydraulic, and chemical signals. Electrical signals found in plants include: slow wave potentials (SWPs) propagated in the functional xylem; action potentials (APs) initiated in the phloem; system potentials (SPs) propagated in the apoplast following mechanical perturbations or wounding; and wound potentials (WPs) through changes in cell turgor leading to plasma membrane depolarisation. Hydraulic signals involve changes in turgor pressure, mass flow, and pressure waves. SWPs are closely linked to hydraulic signals as a result of cavitation events or changes in turgor [154,155,156]. Chemical signals can be classified as: (i) secondary messengers including reactive oxygen species (ROS), inositol triphosphate (IP), Ca²⁺, K⁺, and anion fluxes; (ii) signalling cascade chemicals including mitogen-activated protein kinases (MAPKs); and (iii) chemical response signals including phytohormones and volatile organic compounds (VOCs). Herbivore-induced plant volatiles (HIPVs) have been well-documented involving both above- and below-ground biocontrol of herbivores by insect predators and parasitoids, such as the yellow jacket wasp and the parasitic wasp, respectively [157,158]. Recent advanced analyses have elucidated the role of various mobile molecules including small peptides [155,159,160] and small RNAs (small interfering RNA and micro RNAs) in long-distance systemic signalling [159,161,162,163]. Stomatal closure is one of the initial responses to osmotic stress to prevent hydraulic failure [164] and is regulated by abscisic acid (ABA) [165,166]. During water stress, the root-to-shoot communication is mediated by a small mobile root-derived peptide, CLAVATA3/EMBRYO-SURROUNDING REGION-RELATED 25 (CLE25), which then triggers ABA accumulation in the leaves via BARELY ANY MERISTEM1 (BAM1) and BAM2 receptors in the leaf vascular bundles [159]. Sound vibrations (SVs) or acoustic signals produced by both biotic and abiotic stresses act as stimuli capable of priming plants for future stress challenges and as long-range signals that activate plant-signalling pathways [148]. Leaf vibrations caused by herbivore chewing [148,149] and the “clicking” sound produced by the collapsing water column (cavitation) in the xylem [167] have been demonstrated to trigger systemic responses in distal regions of the plant. The perturbation of the plasma membrane by SVs is characterised by a sequence of molecular episodes including cell wall modification and microfilament rearrangement in plant cells [147,149,168].

Figure 4

Role and mechanism of action of stress-induced volatile organic compounds (VOCs). In response to both biotic and abiotic stresses, VOCs induce various defence-signalling pathways and are involved in intra- and inter-plant priming against future stress challenges. The antixenotic and antibiotic effects of VOCs facilitate direct and indirect defence responses against biotic stressors. Both abiotic and biotic stress induce the production of reactive oxygen species (ROS) whose negative oxidative effects are curbed by VOCs through ROS quenching and cell membrane stabilisation. Thermo-tolerance of photosynthetic tissue is also facilitated by some VOCs under high temperature conditions. (Modified from Vickers et al. [208]).

Figure 5

Integrating physiological, metabolome, proteome, and transcriptome analyses in understanding plant volatile signalling.