Plant Defense Responses to Insect Herbivores Through Molecular Signaling, Secondary Metabolites, and Associated Epigenetic Regulation

Abstract

Over millions of years of interactions, plants have developed complex defense mechanisms to counteract diverse insect herbivory strategies. These defenses encompass morphological, biochemical, and molecular adaptations that mitigate the impacts of herbivore attacks. Physical barriers, such as spines, trichomes, and cuticle layers, deter herbivores, while biochemical defenses include the production of secondary metabolites and volatile organic compounds (VOCs). The initial step in the plant's defense involves sensing mechanical damage and chemical cues, including herbivore oral secretions and herbivore-induced VOCs. This triggers changes in plasma membrane potential driven by ion fluxes across plant cell membranes, activating complex signal transduction pathways. Key hormonal mediators, such as jasmonic acid, salicylic acid, and ethylene, orchestrate downstream defense responses, including VOC release and secondary metabolites biosynthesis. This review provides a comprehensive analysis of plant responses to herbivory, emphasizing early and late defense mechanisms, encompassing physical barriers, signal transduction cascades, secondary metabolites synthesis, phytohormone signaling, and epigenetic regulation.

Keywords: epigenetic regulations; herbivore attack; molecular signaling; plant–herbivore interaction; secondary metabolites.

FIGURE 1

Overview of pathogen/herbivore induced hormonal regulation of genes (adapted from Bigeard et al. 2015).

FIGURE 2

The interaction between elicitors and receptors activates several signaling transduction pathways. In the ion flux transduction pathway, the ligand's interaction to the receptor results in the activation of the G‐protein leads to signal transduction via the activation of phosphatases, resulting in the stimulation of H‐ATPase located in the plasma membrane. This hyperpolarization additionally activates the calcium channels. This G‐protein activates protein kinases that block Ca²⁺ ATPase, resulting in a rise in calcium concentration. Conversely, the inhibition of H⁺ ATPase induces depolarization, subsequently leading to the opening of calcium channels, which ultimately elevates calcium concentration. Dashed lines indicate the alpha component of the active G protein.

FIGURE 3

PAMP + PRR (PTI) and Effector +R proteins produce ROS in several organelles like chloroplasts, mitochondria, and peroxisomes. In host‐insect interactions, one of the early signaling events detected in resistant host cells or cells treated with fungal elicitors artificially is the rapid and short‐lived generation of ROS radicals, including superoxide (${\mathrm{O}}_2^{-}$), hydrogen peroxide (H₂O₂), and hydroxyl radical (OH). The NADPH‐dependent oxidase enzyme, which is found in plant cell membranes, catalyzes the conversion of O₂ to ${\mathrm{O}}_2^{-}$. Superoxide dismutase enzyme converts oxygen to H₂O₂. Eventually, OH radicals are formed through the Fenton reaction.

FIGURE 4

PAMPs recognition by PRR (PTI) and Effectors recognition by R proteins lead to Phosphorylation of MAPK proteins. This PTI and ETI activates MAPKKKs or MEKs through phosphorylation followed by activation of MAPKKs or MEKs through phosphorylation of serine and threonine residues at S/T XXX S/T which further activates MAPKs through phosphorylation at threonine and tyrosine residues at TXY motif between 7th and 8th kinase subdomains. This complete MAPK cascade led to activation of plant defense response.

FIGURE 5

Under insect attack JA is synthesized and converted to JA‐Ile. This JA‐Ile binds with JAZand allow binding of JAZ to COI1. Binding of JA‐Ile to COI1 leads to ubiquitinylation and subsequent degradation of JAZ repressor proteins via the proteasome. In JA stimulated cells, COI1 dependent degradation of JAZ proteins cause disrupts of physical interaction between JAZ proteins and transcriptional activators. This enhances the transcriptional activity of different JA responsive TF and activation of a large number of JA responsive genes.