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The Multifunctional Roles of Polyphenols in Plant-Herbivore Interactions

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The Multifunctional Roles of Polyphenols in Plant-Herbivore Interactions International Journal of Molecular Sciences Review The Multifunctional Roles of Polyphenols in Plant-Herbivore Interactions Sukhman Singh 1,†, Ishveen Kaur 2,† and Rupesh Kariyat 1,2,* 1 Department of Biology, University of Texas Rio Grande Valley, Edinburg, TX 78539, USA; [email protected] 2 School of Earth, Environmental and Marine Sciences, University of Texas Rio Grande Valley, Edinburg, TX 78539, USA; [email protected] * Correspondence: [email protected] † There authors contributed equally to this manuscript. 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 Citation: Singh, S.; Kaur, I.; Kariyat, avenues for future research in this area. R. The Multifunctional Roles of Polyphenols in Plant-Herbivore Keywords: secondary metabolites; polyphenols; phenylpropanoid pathway; phenolic acid; flavonoids; Interactions. Int. J. Mol. Sci. 2021, 22, lignans; insect herbivores; chemical defenses 1442. https://doi.org/10.3390/ ijms22031442 Academic Editor: Federico Brilli 1. Introduction Received: 8 December 2020 The millions of years of dynamic co-existence and relentless competition for sur- Accepted: 26 January 2021 vival has led plants to evolve complex strategies to survive against the onslaught of Published: 1 February 2021 damaging insect herbivores [1–3], primarily mediated through tolerance and resistance mechanisms [4,5]. While resistance traits assist plants to prevent the attack of insects, Publisher’s Note: MDPI stays neutral tolerance allows them to combat herbivory or offset fitness consequences by increasing with regard to jurisdictional claims in the photosynthetic activity at the damaged site, and utilization of stored resources for published maps and institutional affil- iations. compensatory growth [4]. Resistance mechanisms also include mechanical defenses to deter the insects from feeding- using morphological adaptations including, but not limited to waxy cuticle, trichomes, thorns, and spines [6,7]. Being the first line of defense, herbi- vores have to face these challenges pronto as they come in contact with plants, although these defenses can also act in tandem to successfully ward off herbivory [4]. However, Copyright: © 2021 by the authors. selection pressure for survival in this never ending co-evolutionary arms race has also led Licensee MDPI, Basel, Switzerland. to the development of complex, biochemically based, and tightly regulated second line This article is an open access article of defenses. These include the production of toxins that deter herbivores from feeding, distributed under the terms and conditions of the Creative Commons reduce the palatability/digestibility of plant tissue, and compounds that can negatively Attribution (CC BY) license (https:// affect herbivore growth and development [8,9]. These defenses also include the release of creativecommons.org/licenses/by/ constitutive and herbivore induced plant volatiles that attract predators and parasitoids, 4.0/). Int. J. Mol. Sci. 2021, 22, 1442. https://doi.org/10.3390/ijms22031442 https://www.mdpi.com/journal/ijms Int. J. Mol. Sci. 2021, 22, 1442 2 of 19 Int. J. Mol. Sci. 2021, 22, 1442 2 of 20 cases, selectively repel herbivores [10,11]. Collectively, these compounds are defined as plant secondary metabolites. and inPlant many cells cases, produce selectively two types repel of herbivores compound [10s; primary,11]. Collectively, metabolites these and compounds secondary me- are definedtabolites as (plant plant secondary metabolites.metabolites; PSM) [12,13]. Primary metabolites include com- poundsPlant vital cells for produce plant growth, two types development, of compounds; and fitness. primary These metabolites include andcarbohydrates, secondary metaboliteslipids, nucleic (plant acids, secondary and proteins metabolites; inevitable PSM) for [cell12,13 structure,]. Primary and metabolites physiological include and com- bio- poundschemical vital functioning for plant in growth, plants; development,whereas PSM, and although fitness. not These directly include involved carbohydrates, in growth lipids,and metabolism, nucleic acids, are andessential proteins for interactions inevitable for with cell the structure, environment. and physiological They are synthesized and bio- chemicaland can also functioning be induced in plants; during whereas biotic and PSM, abiotic although stresses- not protecting directly involved the plant in from growth in- andsects, metabolism, mammalian are herbivores, essential for micro-organisms, interactions with UV the radiation, environment. high temperature, They are synthesized shading, andmechanical can also injury, be induced wounding, during and biotic heavy and metal abiotic toxicity stresses- to name protecting a few [14–17]. the plant As from an anti- in- sects,herbivore mammalian defense, herbivores, they also improve micro-organisms, host plant UV survival radiation, and high fitness temperature, [12,18,19] shading,by nega- mechanicaltively affecting injury, the wounding, survivability, and vigor, heavy host metal location toxicity and to namefitness a fewof the [14 herbivores–17]. As an [8,20– anti- herbivore23]. Furthermore, defense, theythe production also improve of hostthese plant compounds survival andis tightly fitness regulated [12,18,19] and by negatively decreases affectingonce they the regain survivability, normal state vigor, post host induction, location and since fitness they ofrequire the herbivores huge investment [8,20–23]. of Fur- re- thermore,sources; making the production it expensive of these to compoundscontinuously is produce tightly regulated them, leading and decreases to growth-fitness once they regaintrade-offs normal [4,24,25]. state post induction, since they require huge investment of resources; making it expensive to continuously produce them, leading to growth-fitness trade-offs [4,24,25]. 2. Classification 2. ClassificationPlant secondary metabolites are generally divided into three broad classes: terpe- noids,Plant phenolics secondary and alkaloids, metabolites with are phenolics generally (polyphenols) divided into being three broadthe largest, classes: diverse ter- penoids,and most phenolics widely distributed and alkaloids, class with among phenolics them. (polyphenols) Several thousand being thepolyphenolic largest, diverse com- andpounds most are widely found distributedin plants, synthesized class among via them. the shikimic Several acid-derived thousand polyphenolic phenylpropanoid com- poundsand/or polyketide are found inpathways plants, synthesized [26]. They have via the a basic shikimic structure acid-derived consisting phenylpropanoid of benzene ring and/orwith a hydroxyl polyketide group pathways attached, [26]. without They have any anitrogen-based basic structure functional consisting group of benzene [27–29]. ring L- withphenylalanine a hydroxyl is groupthe primary attached, compound without in any this nitrogen-based pathway to be functionalsynthesized group and form [27–29 the]. L-phenylalaninebasis for downstream is the synthesis primary of compound other poly inphenols this pathway (Figure to1). beMajor synthesized groups of and polyphe- form the basis for downstream synthesis of other polyphenols (Figure1). Major groups of nols include flavonoids (C6-C3-C6), phenolic acids (C6-C1), stilbenes (C6-C2-C6) and lignans polyphenols include flavonoids (C -C -C ), phenolic acids (C -C ), stilbenes (C -C -C ) (C6-C3). Polyphenols not only contribute6 3 to6 the flavor, color, odor,6 1 astringency, oxidative6 2 6 andstability lignans and (C bitterness6-C3). Polyphenols [30,31] of different not only contributeplant parts, to but the also flavor, play color, a critical odor, role astringency, as plant oxidativechemical stabilitydefenses and [30]. bitterness [30,31] of different plant parts, but also play a critical role as plant chemical defenses [30]. Figure 1. Basic classification and synthesis outline of major polyphenol classes in plants. Figure 1. Basic classification and synthesis outline of major polyphenol classes in plants. The idea of plant-insect interactions either positively or negatively affected by polyphe- nols was first proposed by Fraenkel in 1959 [32]. Following that, numerous studies Int. J. Mol. Sci. 2021, 22, 1442 3 of 20 investigated the defensive as well as stimulatory roles of such
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