The Multifunctional Roles of Polyphenols in Plant-Herbivore Interactions

Abstract

There is no argument to the fact that insect herbivores cause significant losses to plant productivity in both natural and agricultural ecosystems. To counter this continuous onslaught, plants have evolved a suite of direct and indirect, constitutive and induced, chemical and physical defenses, and secondary metabolites are a key group that facilitates these defenses. Polyphenols-widely distributed in flowering plants-are the major group of such biologically active secondary metabolites. Recent advances in analytical chemistry and metabolomics have provided an opportunity to dig deep into extraction and quantification of plant-based natural products with insecticidal/insect deterrent activity, a potential sustainable pest management strategy. However, we currently lack an updated review of their multifunctional roles in insect-plant interactions, especially focusing on their insect deterrent or antifeedant properties. This review focuses on the role of polyphenols in plant-insect interactions and plant defenses including their structure, induction, regulation, and their anti-feeding and toxicity effects. Details on mechanisms underlying these interactions and localization of these compounds are discussed in the context of insect-plant interactions, current findings, and potential avenues for future research in this area.

Keywords: chemical defenses; flavonoids; insect herbivores; lignans; phenolic acid; phenylpropanoid pathway; polyphenols; secondary metabolites.

Figure 1

Basic classification and synthesis outline of major polyphenol classes in plants.

Figure 2

Schematic of phenylpropanoid pathway leading to synthesis of different polyphenols i.e., phenolic acids, flavonoids, stilbenes and lignans by the action of various enzymes.

Figure 3

Schematic representation of signaling cascade after insect herbivory at the cellular level inside a plant cell. The regurgitant of caterpillar that includes contents from salivary gland and gut consists of fatty acid conjugates, β-glucose oxidase, peroxidase that acts as elicitors. Elicitors binds with the receptors on cell membrane and cause biochemical changes in the cell culminating in gene expression and the activation of octa-decanoid pathway [117] which upregulates defense- related genes followed by down-regulation of photosynthesis genes. The upregulation of defense genes that encodes proteins can be broadly classified into three categories- defense genes which produce anti-nutritional proteins and the enzymes involved in shikimate-phenylpropanoid pathway producing secondary metabolites, proteinase inhibitors which are involved in cross-linking and polymerization of cell walls and the third includes phytohormone signaling pathway genes for i.e., jasmonic acid, salicylic acid and ethylene. Jasmonic acid moves to plastid/chloroplast to activate the chief enzyme of shikimate pathway i.e., phenylalanine ammonia lyase (PAL). Most of the polyphenol biosynthesis takes place in plastids, however flavonoid production occurs either in the cytoplasm or the cytoplasmic surface of endoplasmic reticulum [127]. PAL in the stomata diverts amino acids from primary metabolism toward the formation of secondary metabolites including a diverse set of polyphenols via activation of a suite of defense genes [128]. Some polyphenols are shuttled outside the cell to act as anti-feedant or anti-deterrent to ward-off the herbivory, while others are stored inside the tonoplast of cells for quick-future action. These polyphenols are compartmentalized by converting them into inert and reduced state called phenyloplast, protected inside the tonoplast. During the successive herbivore attack, the regurgitant of herbivores that activates reactive oxygen species generates oxidative stress in the cell, leading to dissolution of compartments and release of polyphenol oxidase. Polyphenol oxidase can form quinones which act as anti-nutritional proteins interfering with digestibility and nutrient uptake of insects or produce proteinase-inhibitors leading to cross-linking and polymerization of cells leading to herbivore defense. Illustration by Annette Diaz, conceptualized by Ishveen Kaur and Japneet Kaur.

Figure 4

Schematic illustrating the wide gamut of herbivory related functions performed by polyphenols in plants. Plants produce polyphenols at the advent of adverse conditions such as biotic and abiotic stresses. Herbivory causes abrasions, wounds, and tissue loss which act as signal for the production of polyphenols. Moreover, the saliva or regurgitant from herbivores contain peroxidases which act as elicitors for the activation of different signaling pathways [112]. These secretions activate different plant hormones and signaling pathways such as jasmonic acid, salicylic acid and octadecanoid pathway [128] which generate and transmit signals to all the parts of plants which is depicted by bi-directional arrows running throughout the plant leading to generation of Systemic Induced Resistance (SIR) in the plants [148]. The production of polyphenols also leads to synthesis of sesquiterpenes for defense priming of the neighboring plants. Both positive and negative impacts are being illustrated on the plant with left and right sides of the schematic respectively. Polyphenols generally have anti-feedent and anti-deterrent effect on most of the insects. Flavonoids (class of polyphenols) and tannins have cascading effects on the feeding and oviposition activity of tobacco hornworm caterpillar [Manduca sexta L.; [8,22], also protects plants against the damaging herbivores by releasing herbivore-induced plant volatiles (HIPV) attracting their predators and parasitoids [149]. Activation of defense mechanisms also leads to the production of reactive oxygen species (ROS) which ultimately lead to the formation of polyphenol oxidase and subsequent synthesis of compounds such as proteinase inhibitors preventing the digestibility of tissues by cross-linking and polymerizing the cells walls with alkylated amino acids. Polymerization of cinnamyl alcohol into lignin by polyphenol oxidase (formed due to activation and synthesis of polyphenols) deposits lignin in leaves and fruits which also confers resistance to the plants [150]. These chemical toxins are also observed to have negative impacts on activity and functionality of microbes, thus indirectly affecting their symbiotic insects as well [151]. Polyphenols are also observed to affect the herbivores positively; thus, playing dual role in plant-insect relationship dynamics. Flavanone glycosides present in carrot (Daucus carota L.; Apiaceae) acts as oviposition stimulant for black swallowtail butterfly (Papilio polyxenes Fabricius) by releasing volatiles which attract the insects to lay eggs [145], and sequestration of flavone glucosides in the wings of lycaenid butterfly (Polyommatus bellargus Rottemburg) aiding them in visual communication and mate recognition. Illustration by Annette Diaz, conceptualized by Ishveen Kaur and Japneet Kaur.