Dynamic distress calls: volatile info chemicals induce and regulate defense responses during herbivory

Abstract

Plants are continuously threatened by a plethora of biotic stresses caused by microbes, pathogens, and pests, which often act as the major constraint in crop productivity. To overcome such attacks, plants have evolved with an array of constitutive and induced defense mechanisms- morphological, biochemical, and molecular. Volatile organic compounds (VOCs) are a class of specialized metabolites that are naturally emitted by plants and play an important role in plant communication and signaling. During herbivory and mechanical damage, plants also emit an exclusive blend of volatiles often referred to as herbivore-induced plant volatiles (HIPVs). The composition of this unique aroma bouquet is dependent upon the plant species, developmental stage, environment, and herbivore species. HIPVs emitted from infested and non-infested plant parts can prime plant defense responses by various mechanisms such as redox, systemic and jasmonate signaling, activation of mitogen-activated protein (MAP) kinases, and transcription factors; mediate histone modifications; and can also modulate the interactions with natural enemies via direct and indirect mechanisms. These specific volatile cues mediate allelopathic interactions leading to altered transcription of defense-related genes, viz., proteinase inhibitors, amylase inhibitors in neighboring plants, and enhanced levels of defense-related secondary metabolites like terpenoids and phenolic compounds. These factors act as deterrents to feeding insects, attract parasitoids, and provoke behavioral changes in plants and their neighboring species. This review presents an overview of the plasticity identified in HIPVs and their role as regulators of plant defense in Solanaceous plants. The selective emission of green leaf volatiles (GLVs) including hexanal and its derivatives, terpenes, methyl salicylate, and methyl jasmonate (MeJa) inducing direct and indirect defense responses during an attack from phloem-sucking and leaf-chewing pests is discussed. Furthermore, we also focus on the recent developments in the field of metabolic engineering focused on modulation of the volatile bouquet to improve plant defenses.

Keywords: HIPVs; VOCs (volatile organic compounds); biotic stress; defense responses; herbivory; metabolomics; terpenoids.

Figure 1

Overview of different classes of herbivore induced plant volatiles (HIPVs), including green leaf volatiles, terpenoids, and aromatic compounds along with their biosynthesis pathways. In the figure, block arrows represent multiple biosynthetic steps involved. Abbreviations: acetyl-CoA, acetyl-coenyzme A; DMAPP, dimethylallyl pyrophosphate; DMNT, 4,8-dimethylnona-1,3,7-triene; E4P, erythrose 4-phosphate; IPP, isopentenyl pyrophosphate; PEP, phosphoenolpyruvate; TMTT, 4,8,12-trimethyltrideca-1,3,7,11-tetraene.

Figure 2

Diversity of HIPVs emitted in Solanaceae crops under herbivory. Emission of higher amounts of VOCs including terpenoids, GLVs, and few aromatics under the attack of chewing herbivores and mesophyll-feeding stylet feeders along with selective emission of aromatics, terpenoids, and few GLVs under the attack of phloem feeding stylet feeders is shown. In set in the figures shows a representative cross-section of leaf tissue damage under respective herbivory.

Figure 3

Schematic model of herbivore-induced defense signaling in plants. Role of specific early defense regulators and components comprising of Ca²⁺, LRR-RLKs, MAPKs, WRKY transcription factors, and jasmonate biosynthesis genes leading to downstream defense gene expression to activate plant defenses is illustrated. The role of GLVs and terpenoids in mediating the direct and indirect responses via tritrophic interactions is also exemplified.