Plants respond to herbivory through various morphological, biochemicals, and molecular mechanisms to counter/offset the effects of herbivore attack. The biochemical mechanisms of defense against the herbivores are wide-ranging, highly dynamic, and are mediated both by direct and indirect defenses. The defensive compounds are either produced constitutively or in response to plant damage, and affect feeding, growth, and survival of herbivores. In addition, plants also release volatile organic compounds that attract the natural enemies of the herbivores. These strategies either act independently or in conjunction with each other. However, our understanding of these defensive mechanisms is still limited. Induced resistance could be exploited as an important tool for the pest management to minimize the amounts of insecticides used for pest control. Host plant resistance to insects, particularly, induced resistance, can also be manipulated with the use of chemical elicitors of secondary metabolites, which confer resistance to insects. By understanding the mechanisms of induced resistance, we can predict the herbivores that are likely to be affected by induced responses. The elicitors of induced responses can be sprayed on crop plants to build up the natural defense system against damage caused by herbivores. The induced responses can also be engineered genetically, so that the defensive compounds are constitutively produced in plants against are challenged by the herbivory. Induced resistance can be exploited for developing crop cultivars, which readily produce the inducible response upon mild infestation, and can act as one of components of integrated pest management for sustainable crop production. Keywords: Plant defense, herbivory, direct defense, indirect defense, biotic stress, abiotic stress Plants and insects have been living together for more than 350 million years. In co- evolution, both have evolved strategies to avoid each other’s defense systems. This evolutionary arms race between plants and insects has resulted in the development of an elegant defense system in plants that has the ability to recognize the nonself molecules or signals from damaged cells, much like the animals, and activates the plant immune response against the herbivores.1-3 To counter the herbivore attack, plants produce specialized morphological structures or secondary metabolites and proteins that have toxic, repellent, and/or antinutitional effects on the herbivores.4-6 Plants confront the herbivores both directly by affecting host plant preference or survival and reproductive success (direct defense), and indirectly through other species such as natural enemies of the insect pests (indirect defense).1,7,8 Direct defenses are mediated by plant characteristics that affect the herbivore’s biology such as mechanical protection on the surface of the plants (e.g., hairs, trichomes, thorns, spines, and thicker leaves) or production of toxic chemicals such as terpenoids, alkaloids, anthocyanins, phenols, and quinones) that either kill or retard the development of the herbivores.9 Indirect defenses against insects are mediated by the release of a blend of volatiles that specifically attract natural enemies of the herbivores and/or by providing food (e.g., extra floral nectar) and housing to enhance the effectiveness of the natural enemies.8 Research on plant-herbivore interactions is one of the most important and multidisciplinary undertakings in plant biology involving various disciplines to describe chemical and ecological processes influencing the outcome of plant - herbivore interactions. Our understanding of how plants communicate with their neighbors, symbionts, pathogens, herbivores, and with their personal “bodyguards”- the natural enemies, both above and below ground, via chemical signals, is still in its infancy. This is an enthralling area from an ecological point of view, and has a great potential for utilization in crop protection. Understanding the nature of gene expression of the plant defensive traits will have a tremendous application in designing crop plants with better protection against the herbivores. This in turn will reduce the need for use of harmful pesticides for insect control. However, the arms race between plants and herbivores will continue, and herbivores could co-evolve in response to the resistant plant genotypes. Knowledge of the complex chemical plant-herbivore interactions is required to optimize the production of new crops. Host plant defenses against insectsPlants respond to herbivore attack through an intricate and dynamic defense system that includes structural barriers, toxic chemicals, and attraction of natural enemies of the target pests (Fig. 1).1,9,10 Both defense mechanisms (direct and indirect) may be present constitutively or induced after damage by the herbivores. Induced response in plants is one of the important components of pest control in agriculture, and has been exploited for regulation of insect herbivore population.1,11,12 Over the past few decades, considerable progress has been made in studying induced responses in plants against different stresses, and has become an important topic in evolutionary biology and ecology. Although induced responses have some metabolic costs,13 they are very important when aimed at alleviating the stress of immediate concern, as most of these chemicals are produced in response to herbivore attack.14,15 Induced defenses make the plants phenotypically plastic, and thereby, decrease the chances of the attacking insects to adapt to the induced chemicals.1,12 Changes in defensive constituents of a plant on account of insect attack develop unpredictability in the plant environment for insect herbivores, which in turn, affects the fitness and behavior of the herbivores.5,6,14 If induced response occurs very early, it is of great benefit to the plant, and reduces the subsequent herbivore and pathogen attack, besides improving overall fitness of the plant.12 Plants with high variability in defensive chemicals exhibit a better defense compared with those with moderate variability.5,6 Progress in insect-plant interactions has improved our understanding of the evolution of defensive approaches exploited deployed by the plants against herbivory;10 however, the underlying mechanisms of defense are less clearly understood Direct defensesPlant structural traits such as leaf surface wax, thorns or trichomes, and cell wall thickness/ and lignification form the first physical barrier to feeding by the herbivores, and the secondary metabolites such act as toxins and also affect growth, development, and digestibility reducers form the next barriers that defend the plant from subsequent attack.9,16 Moreover, synergistic effect among different defensive components enhances the defensive system of plants against the herbivores invaders. In tomato, alkaloids, phenolics, proteinase inhibitors (PIs), and the oxidative enzymes when ingested separately result in a reduced affect, but act together in a synergistic manner, affecting the insect during ingestion, digestion and metabolism.17 InNicotiana attenuata (Torr. ex Watson), trypsin proteinase inhibitors and nicotine expression, contributed synergistically to the defensive response against Spodoptera exigua (Hub.).15 The role of morphological and biochemical constituents in host plant resistance (HPR), and induced responses to insect damage will be discussed below. Morphological structuresPlant structures are the first line of defense against herbivory, and play an important role in host plant resistance (HPR) to insects. The first line of plant defense against insect pests is the erection of a physical barrier either through the formation of a waxy cuticle,9,16 and/or the development of spines, setae, and trichomes.18,19 Structural defenses includes morphological and anatomical traits that confer a fitness advantage to the plant by directly deterring the herbivores from feeding,16 and range from prominent protrubances on a plant to microscopic changes in cell wall thickness as a result of lignification and suberization.9,19 Structural traits such as spines and thorns (spinescence), trichomes (pubescence), toughened or hardened leaves (sclerophylly), incorporation of granular minerals into plant tissues, and divaricated branching (shoots with wiry stems produced at wide axillary angles) play a leading role in plant protection against herbivory.9,19,20 Sclerophylly refers to the hardened leaves, and plays an active role in plant defense against herbivores by reducing the palatability and digestibility of the tissues, thereby, reducing the herbivore damage.9,21 Spinescence includes plant structures such as spines, thorns and prickles. It has been reported to defend the plants against many insects.9 Pubescence consists of the layer of hairs (trichomes) extending from the epidermis of the above ground plant parts including stem, leaves, and even fruits, and occur in several forms such as straight, spiral, stellate, hooked, and glandular.9 Chamarthi et al.20 reported that leaf glossiness, plumule and leaf sheath pigmentation were responsible for shoot fly Atherigona soccata (Rondani) resistance in sorghum Sorghum bicolor (L.) (Moench). TrichomesTrichomes play an imperative role in plant defense against many insect pests and involve both toxic and deterrent effects.20,21 Trichome density negatively affects the ovipositional behavior, feeding and larval nutrition of insect pests.21 In addition, dense trichomes affect the herbivory mechanically, and interfere with the movement of insects and other arthropods on the plant surface, thereby, reducing their access to leaf epidermis.16 These can be, straight, spiral, hooked, branched, or un-branched and can be glandular or nonglandular.9 Glandular trichomes secrete secondary metabolites including flavonoids, terpenoids, and alkaloids that can be poisonous, repellent, or trap insects and other organisms, thus forming a combination of structural and chemical defense.9,18 Induction of trichomes in response to insect damage has been reported in many plants.22 This increase in trichome density in response to damage can only be observed in leaves developing during or subsequent to insect attack, since the density of trichomes of existing leaves does not change.16 Dalin and Bjorkman23reported that damage by adult leaf beetles, Phratora vulgatissima L. in Salix cinerea L. induced higher trichome density in the new leaves developing thereafter. Likewise, increase in trichome density in S. cinerain response to coleopteran damage has also been reported.24 Increase in trichome density after insect damage has also been reported in Lepidium virginicum L. and Raphanus raphanistrum L.22 In black mustard, trichomes density and glucosinolate levels were elevated after feeding by Pieris rapae (L.).25 Trichome density increased in Alnus incana Moench as a result of damage by beetles.26 The increase in trichome density in response to herbivory is typically between 25 to 100%, however, there are cases where 500 – 1000% increase in trichome density has also been reported. Changes in trichome density occur within days or weeks after insect damage.22-24 Furthermore, change in relative proportion of glandular and non-glandular trichomes is also induced by herbivory.22 A positive correlation has been observed between natural enemies’ abundance and trichome density. Trichome exudates also serve as extra floral nectar (EFN) for scelonid egg parasitoid, of squash bugs, Gryon pennsylvanicum.27 Secondary metabolites and plant defenseSecondary metabolites are the compounds that do not affect the normal growth and development of a plant, but reduce the palatability of the plant tissues in which they are produced.1 The defensive (secondary) metabolites can be either constitutive stored as inactive forms or induced in response to the insect or microbe attack. The former are known as phytoanticipins and the latter as phytoalexins. The phytoanticipins are mainly activated by β-glucosidase during herbivory, which in turn mediate the release of various biocidal aglycone metabolites.28 The classic examples of phytoanticipins are glucosinolates that are hydrolyzed by myrosinases (endogenous β-thioglucoside glucohydrolases) during tissue disruption. Other phytoanticipins include Benzoxazinoids (BXs), which are widely distributed among Poaceae. Hydrolyzation of BX-glucosides by plastid-targeted β-glucosidases during tissue damage leads to the production of biocidal aglycone BXs, which play an important role in plant defense against insects.28 Phytoalexins include isoflavonoids, terpenoids, alkaloids, etc., that influence the performance and survival of the herbivores.29 The secondary metabolites not only defend the plants from different stresses, but also increase the fitness of the plants. It has been reported that maize HPR to corn earworm, Helicoverpa zea (Boddie) is mainly due to the presence of the secondary metabolites C-glycosyl flavone maysin [2”- O - a –L-rhamnosyl- 6- C - (6-deoxy-xylo -hexos-4-ulosyl) luteolin] and the phenylpropanoid product, chlorogenic acid.30 Compound, 4, 4- dimethyl cyclooctene has been found to be responsible for shoot fly A. soccata resistance in sorghum S. bicolor.31 Secondary metabolites have been primarily studied as the mediators of direct defense, however much is to be done to reveal the unidentified or emerging signaling pathways. Mass spectrometry used for the secondary metabolite profiling and gene expression analysis by high-throughput sequencing has made this field more exciting and cost-effective. Study on secondary metabolites could lead to the identification of new signaling molecules involved in plant resistance against herbivores and other stresses. Ultimately genes and enzymes involved in the biosynthesis of these metabolites could be identified. Role of some of the secondary metabolites in plant defense will be discussed below. Plant phenolicsAmong the secondary metabolites, plant phenols constitute one of the most common and widespread group of defensive compounds, which play a major role in HPR against herbivores, including insects.4-6,18 Phenols act as a defensive mechanism not only against herbivores, but also against microorganisms and competing plants. Qualitative and quantitative alterations in phenols and elevation in activities of oxidative enzyme in response to insect attack is a general phenomenon.5,6,32 Lignin, a phenolic heteropolymer plays a central role in plant defense against insects and pathogens.32 It limits the entry of pathogens by blocking physically or increasing the leaf toughness that reduces the feeding by herbivores, and also decreases the nutritional content of the leaf.33 Lignin synthesis has been found to be induced by herbivory or pathogen attack and its rapid deposition reduce further growth of the pathogen or herbivore fecundity.33 Increase in expression of lignin associated genes (CAD/CAD-like genes) in plants infected with pests and pathogens have been documented.32 Oxidation of phenols catalyzed by polyphenol oxidase (PPO) and peroxidase (POD) is a potential defense mechanism in plants against herbivorous insects. Quinones formed by oxidation of phenols bind covalently to leaf proteins, and inhibit the protein digestion in herbivores.34 In addition, quinones also exhibit direct toxicity to insects.17,34 Alkylation of amino acids reduces the nutritional value of plant proteins for insects, which in turn negatively affects the insect growth and development.34 Phenols also play an important role in cyclic reduction of reactive oxygen species (ROS) such as superoxide anion and hydroxide radicals, H2O2, and singlet oxygen, which in turn activate a cascade of reactions leading to the activation of defensive enzymes.35 Simple phenolics (salicylates) act as antifeedant to insect herbivores such as Operophtera brumata (L.) in Salix leaves, and there is a negative correlation between the salicylate levels and the larval growth, however, salicylic acid (SA) is much more important as phytohormone than as deterrent.36 FlavonoidsFlavonoids play a central role in various facets of plant life especially in plant-environment interactions.37These defend plants against various biotic and abiotic stresses including UV radiations, pathogens and insect pests.37 Flavonoids are cytotoxic and interact with different enzymes through complexation. Both flavonoids and isoflavonoids protect the plant against insect pests by influencing the behavior, and growth and development of insects.36 In addition, flavonoids scavenge the free radicals including ROS, and reduce their formation by chelating the metals.37 Flavonoids are divided into various classes that include anthocyanins, flavones, flavonols, flavanones, dihydroflavonols, chalcones, aurones, flavan, and proanthocyanidins.37More than 5,000 flavonids have been reported in plants. A number of flavones such as flavonols, flavones, proanthocyanidins, flavan 3-ols, flavonones, flavans, and isoflavonoids have been investigated as feeding deterrents against many insect pests. Flavonoids such as flavones 5 -hydroxyisoderricin,7- methoxy-8- (3- methylbutadienyl) –flavanone and 5-methoxyisoronchocarpin isolated from Tephrosia villosa (L.), T. purpurea (L.), and T. vogelii Hook, respectively have been found as feeding deterrents against Spodoptera exempta (Walk.), and Spodoptera littoralis Bios.38 Overexpressing a transcription factor controlling flavonoid production in Arabidopsis has been reported to confer resistance against Spodoptera frugiperda(J.E. Smith).39 Angustone A, licoisoflavone B, angustone B, and angustone C. Isoflavones, licoisoflavone A, luteone, licoisoflavone B, and wighteone have been found to be not only feeding deterrents to insects, but also have antifungal activity against the fungi, Colletotrichum gloeosporiode (Penz.) and Cladosporium cladosporioides (Fres.).40 Isoflavonoids (judaicin, judaicin-7-O-glucoside, 2-methoxyjudaicin, and maackiain) isolated from the wild relatives of chickpea act as antifeedant against Helicoverpa armigera(Hubner) at 100 ppm. Judaicin and maackiain were also found to be deterrent to S. littoralis and S. frugiperda, respectively.41 Cyanopropenyl glycoside and alliarinoside strongly inhibit feeding by the native American butterfly, Pieris napi oleracea L., while a flavone glycoside, isovitexin-6”-D-β-glucopyranoside acts as a direct feeding deterrent to the late instars.42 TanninsTannins have a strong deleterious effect on phytophagous insects and affect the insect growth and development by binding to the proteins, reduce nutrient absorption efficiency, and cause midgut lesions.18,43,44 Tannins are astringent (mouth puckering) bitter polyphenols and act as feeding deterrents to many insect pests. They precipitate proteins nonspecifically (including the digestive enzymes of herbivores), by hydrogen bonding or covalent bonding of protein –NH2 groups. In addition, tannins also chelate the metal ions, thereby reducing their bioavailability to herbivores. When ingested, tannins reduce the digestibility of the proteins thereby decrease the nutritive value of plants and plant parts to herbivores. Role of tannins in plant defense against various stresses and their induction in response to insect damage has been studied in many plants.44 For example, e.g., in Populus species,45 and in Pinus sylvestris L.46 However, no effect of herbivore damage on tannin content was observed in Quercus serrata (Thunb.)47 and Betula pendulaRoth.48 Like proteinase inhibitors and oxidative enzymes, tannins have been reported to be systemically induced in neighboring leaves of the damaged plant.45 Condensed tannins are oligomeric or polymeric flavonoids, also known as proanthocyanidins. They have diverse structures and functions. They act as feeding deterrents against some insects such as, Lymantria dispar (L.), Euproctis chrysorrhoea (L.) and O. brumata.49,50 Condensed tannins such as (+) -catechin, (+) - gallocatechin, and vanillin in leaves of Quercus robur L. inhibited winter moth larvae, O. brumata.49Procyanindin polymers have been found as feeding deterrent to Aphis Craccivora (Koch) in groundnut.51Condensed tannins from Alaska paper birch (coated on birch leaves at 3% dry wt.) reduced the pupal mass and survival of Rheumaptera hastata (L.) larvae.52 It has been reported that induction of tannins in Populus tremuloides Michx. leaves in response to wound- and herbivore occur by transcriptional activation of the flavonoid pathway.45 Genes responsible for the production of tannins in response to wounding have been identified and are activated by the expression of a condensed tannins regulatory gene, PtMYB134, which is itself induced by damage.53 Furthermore, induction of tannin is also stimulated by light stress,14,53 and exposure to UV light in hybrid poplar.53 However, some polyphagous insect species have the ability to tolerate gallotannins, e.g., Shistocerca gregaria (Forsk.) tolerates tannins by hydrolyzing them rapidly to avoid any damaging effects by restricting the passage of tannins by adsorbing them on the thick peritrophic membrane, and by inhibiting the tannin protein complex formation by surfactants in the midgut.54 Plant defensive proteinsEcologically, in insect-plant interaction, interrelationship between two is important for the survival of the both. Insects always look for a true and healthy host plant that can provide them proper food and could be suitable for mating, oviposition and also provides food for the offsprings. The nutritional requirements of insects are similar to other animals, and any imbalance in digestion and utilization of plant proteins by the insects’ results in drastic effects on insect physiology. Alteration of gene expression under stress including insect attack leads to qualitative and quantitative changes in proteins, which in turn play an important role in signal transduction, and oxidative defense (Table 1).4,55 Many plant proteins ingested by insects are stable, and remain intact in the midgut, and also move across the gut wall into the hemolymph. An alteration in the protein’s amino acid content or sequence influences the function of that protein. Likewise, anti-insect activity of a proteolysis-susceptible toxic protein can be improved by administration of protease inhibitors (PIs), which prevent degradation of the toxic proteins, and allows them to exert their defensive function. Better understanding of protein structure and post-translational modifications contributing to stability in the herbivore gut would assist in predicting toxicity and mechanism of plant resistance proteins (PRPs). Recent advances in microarray and proteomic approaches have revealed that a wide spectrum of PRPs is involved in plant defense against herbivores.56,57 Due to diverse feeding habits of arthropods, multiple signaling pathways including jasmonic acid (JA), SA and/or ethylene (ET) regulate arthropod-inducible proteins.8 Table 1. Plant defensive proteins against insect pests
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