Deciphering the Role of Ion Channels in Early Defense Signaling against Herbivorous Insects

Abstract

Plants and insect herbivores are in a relentless battle to outwit each other. Plants have evolved various strategies to detect herbivores and mount an effective defense system against them. These defenses include physical and structural barriers such as spines, trichomes, cuticle, or chemical compounds, including secondary metabolites such as phenolics and terpenes. Plants perceive herbivory by both mechanical and chemical means. Mechanical sensing can occur through the perception of insect biting, piercing, or chewing, while chemical signaling occurs through the perception of various herbivore-derived compounds such as oral secretions (OS) or regurgitant, insect excreta (frass), or oviposition fluids. Interestingly, ion channels or transporters are the first responders for the perception of these mechanical and chemical cues. These transmembrane pore proteins can play an important role in plant defense through the induction of early signaling components such as plasma transmembrane potential (Vm) fluctuation, intracellular calcium (Ca2+), and reactive oxygen species (ROS) generation, followed by defense gene expression, and, ultimately, plant defense responses. In recent years, studies on early plant defense signaling in response to herbivory have been gaining momentum with the application of genetically encoded GFP-based sensors for real-time monitoring of early signaling events and genetic tools to manipulate ion channels involved in plant-herbivore interactions. In this review, we provide an update on recent developments and advances on early signaling events in plant-herbivore interactions, with an emphasis on the role of ion channels in early plant defense signaling.

Plant Responses to Herbivory, Wounding, and Infection

“…Leaf damage caused by insect attacks suggests the delivery of resistance elicitors through attachments to different receptors on the plasma membrane [5]. The interaction between resistance elicitors and receptors causes a fluctuation in Vm, i.e., cell membrane electrical potential maintained by ion flux balance across the plasma membrane [27]. These electrical signals move from cell to cell in plants, carrying different messages.…”

“…These electrical signals move from cell to cell in plants, carrying different messages. Unbalanced ion fluxes give rise to positive or negative changes in Vm, defined as depolarization and hyperpolarization, respectively [27], which induce plant defense responses. For example, the herbivore Spodoptera littoralis induces Vm depolarization in infected Lima bean plants (Phaseolus lunatus) [28].…”

“…The elevation of intracellular Ca 2+ ions and ROS act as signal transducers under biotic stress. Several forms of ROS are present in plants, including hydrogen peroxide (H 2 O 2 •), superoxide anion (O 2 −•−), hydroxyl radical (HO•), peroxynitrite (ONOO), and singlet oxygen (1O 2 ) [27]. ROS are mainly generated through the action of NADPH oxidase, which is activated by Ca 2+ ions, producing O 2− for further conversion to H 2 O 2 in the plasma membrane [52].…”

“…However, the role of Ca 2+ -binding proteins in phytohormone regulation remains poorly understood. trite (ONOO), and singlet oxygen (1O2) [27]. ROS are mainly generated through the action of NADPH oxidase, which is activated by Ca 2+ ions, producing O2− for further conversion to H2O2 in the plasma membrane [52].…”

“…The release of long-distance signals from the site of damage to different plant parts is an important defensive strategy necessary for plant survival. Systemic signaling is involved in the communication between wounded and unwounded plant tissues [27]. Once cell membrane and signal transduction are interrupted, ion channels move ions across plasma membranes, facilitating long-distance communication between cells.…”