PSB 7 1306

Plant Signaling & Behavior 7:10, 1306-1320; October 2012; © 2012 Landes Bioscience
Mechanisms of Plant Defense against Insect

Herbivores
Abdul Rashid War,1,2 Michael Gabriel Paulraj,2 Tariq Ahmad,3 Abdul Ahad Buhroo,3 Barkat Hussain,4 Savarimuthu Ignacimuthu2
and Hari Chand Sharma1,*
1
International Crops Research Institute for the Semi-Arid Tropics (ICRISAT); Patancheru, Andhra Pradesh, India; 2Entomology Research Institute; Loyola College; Chennai, Tamil
Nadu, India; 3Division of Entomology; Department of Zoology; University of Kashmir; Srinagar, J&K, India; 4Division of Entomology; SKUAST-K; Shalimar, Srinagar, J&K, India
Keywords: plant defense, herbivory, direct defense, indirect defense, biotic stress, abiotic stress
©2012 Landes Bioscience. Do not distribute.

specialized morphological structures or secondary metabolites
Plants respond to herbivory through various morphological, and proteins that have toxic, repellent, and/or antinutitional
biochemicals, and molecular mechanisms to counter/offset
effects on the herbivores.4-6 Plants confront the herbivores both
the effects of herbivore attack. The biochemical mechanisms
of defense against the herbivores are wide-ranging, highly
directly by affecting host plant preference or survival and repro-
dynamic, and are mediated both by direct and indirect ductive success (direct defense), and indirectly through other
defenses. The defensive compounds are either produced species such as natural enemies of the insect pests (indirect
constitutively or in response to plant damage, and affect defense).1,7,8 Direct defenses are mediated by plant characteristics
feeding, growth, and survival of herbivores. In addition, plants that affect the herbivore’s biology such as mechanical protection
also release volatile organic compounds that attract the on the surface of the plants (e.g., hairs, trichomes, thorns, spines,
natural enemies of the herbivores. These strategies either act and thicker leaves) or production of toxic chemicals such as ter-
independently or in conjunction with each other. However, our penoids, alkaloids, anthocyanins, phenols, and quinones) that
understanding of these defensive mechanisms is still limited. either kill or retard the development of the herbivores.9 Indirect
Induced resistance could be exploited as an important tool for defenses against insects are mediated by the release of a blend of
the pest management to minimize the amounts of insecticides
volatiles that specifically attract natural enemies of the herbivores
used for pest control. Host plant resistance to insects,
particularly, induced resistance, can also be manipulated with
and/or by providing food (e.g., extra floral nectar) and housing
the use of chemical elicitors of secondary metabolites, which to enhance the effectiveness of the natural enemies.8 Research
confer resistance to insects. By understanding the mechanisms on plant-herbivore interactions is one of the most important
of induced resistance, we can predict the herbivores that are and multidisciplinary undertakings in plant biology involving
likely to be affected by induced responses. The elicitors of various disciplines to describe chemical and ecological processes
induced responses can be sprayed on crop plants to build up the influencing the outcome of plant-herbivore interactions. Our
natural defense system against damage caused by herbivores. understanding of how plants communicate with their neighbors,
The induced responses can also be engineered genetically, so symbionts, pathogens, herbivores, and with their personal “body-
that the defensive compounds are constitutively produced in guards”—the natural enemies, both above and below ground, is
plants challenged by the herbivory. Induced resistance can be still in its infancy. This is an enthralling area from an ecological
exploited for developing crop cultivars, which readily produce
point of view, and has a great potential for utilization in crop pro-
the inducible response upon mild infestation, and can act
as one of components of integrated pest management for
tection. Understanding the nature of gene expression of the plant
sustainable crop production. 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
Introduction will continue, and herbivores could co-evolve in response to the
resistant plant genotypes. Knowledge of the complex chemical
Plants and insects have been living together for more than 350 plant-herbivore interactions is required to optimize the produc-
million years. In co- evolution, both have evolved strategies to tion of new crops.
avoid each other’s defense systems. This evolutionary arms race Host plant defenses against insects. Plants respond to her-
between plants and insects has resulted in the development of an bivore attack through an intricate and dynamic defense system
elegant defense system in plants that has the ability to recognize that includes structural barriers, toxic chemicals, and attraction
the nonself molecules or signals from damaged cells, much like of natural enemies of the target pests (Fig. 1).1,9,10 Both defense
the animals, and activates the plant immune response against mechanisms (direct and indirect) may be present constitutively
the herbivores.1-3 To counter the herbivore attack, plants produce or induced after damage by the herbivores. Induced response
in plants is one of the important components of pest control in
*Correspondence to: Hari Chand Sharma; Email: [email protected] agriculture, and has been exploited for regulation of insect her-
Submitted: 07/14/12; Revised: 07/28/12; Accepted: 07/29/12 bivore population.1,11,12 Over the past few decades, considerable
http://dx.doi.org/10.4161/psb.21663
1306 Plant Signaling & Behavior Volume 7 Issue 10

REVIEW

Figure 1. Mechanism of induced resistance in plants. POD, peroxidase; PPO, polyphenol oxidase; PAL, phenylalanine ammonia lyase; TAL, tyrosine
alanine ammonia lyase; LOX, lipoxygenase; SOD, superoxide dismutase; APX, ascorbate peroxidase; HIPVs, herbivore induced plant volatiles.
progress has been made in studying induced responses in plants enzymes, when ingested separately result in a reduced affect, but
against different stresses, and has become an important topic in act together in a synergistic manner, affecting the insect dur-
evolutionary biology and ecology. Although induced responses ing ingestion, digestion and metabolism.17 In Nicotiana attenu-
have some metabolic costs,13 they are very important when ata (Torr. ex Watson), trypsin proteinase inhibitors and nicotine
aimed at alleviating the stress of immediate concern, as most of expression, contributed synergistically to the defensive response
these chemicals are produced in response to herbivore attack.14,15 against Spodoptera exigua (Hub.).15 The role of morphological
Induced defenses make the plants phenotypically plastic, and and biochemical constituents in host plant resistance (HPR), and
thereby, decrease the chances of the attacking insects to adapt to induced responses to insect damage will be discussed below.
the induced chemicals.1,12 Morphological structures. Plant structures are the first line
Changes in defensive constituents of a plant on account of of defense against herbivory, and play an important role in HPR
insect attack develop unpredictability in the plant environment to insects. The first line of plant defense against insect pests is
for insect herbivores, which in turn, affects the fitness and behav- the erection of a physical barrier either through the formation
ior of the herbivores.5,6,14 If induced response occurs very early, it of a waxy cuticle,9,16 and/or the development of spines, setae,
is of great benefit to the plant, and reduces the subsequent herbi- and trichomes.18,19 Structural defenses includes morphological
vore and pathogen attack, besides improving overall fitness of the and anatomical traits that confer a fitness advantage to the plant
plant.12 Plants with high variability in defensive chemicals exhibit by directly deterring the herbivores from feeding,16 and range
a better defense compared with those with moderate variability.5,6 from prominent protrubances on a plant to microscopic changes
Progress in insect-plant interactions has improved our under- in cell wall thickness as a result of lignification and suberiza-
standing of the evolution of defensive approaches deployed by tion.9,19 Structural traits such as spines and thorns (spinescence),
plants against herbivory;10 however, the underlying mechanisms trichomes (pubescence), toughened or hardened leaves (sclero-
of defense are less clearly understood. phylly), incorporation of granular minerals into plant tissues, and
Direct defenses. Plant structural traits such as leaf surface divaricated branching (shoots with wiry stems produced at wide
wax, thorns or trichomes, and cell wall thickness and lignification axillary angles) play a leading role in plant protection against her-
form the first physical barrier to feeding by the herbivores, and the bivory.9,19,20 Sclerophylly refers to the hardened leaves, and plays
secondary metabolites such act as toxins and also affect growth, an active role in plant defense against herbivores by reducing the
development, and digestibility reducers form the next barriers that palatability and digestibility of the tissues, thereby, reducing the
defend the plant from subsequent attack.9,16 Moreover, synergistic herbivore damage.9,21
effect among different defensive components enhances the defen- Spinescence includes plant structures such as spines,
sive system of plants against the herbivores invaders. In tomato, thorns and prickles. It has been reported to defend the plants
alkaloids, phenolics, proteinase inhibitors (PIs), and the oxidative against many insects.9 Pubescence consists of the layer of hairs
www.landesbioscience.com Plant Signaling & Behavior 1307

(trichomes) extending from the epidermis of the above ground (endogenous β-thioglucoside glucohydrolases) during tissue dis-
plant parts including stem, leaves, and even fruits, and occur ruption. Other phytoanticipins include Benzoxazinoids (BXs),
in several forms such as straight, spiral, stellate, hooked, and which are widely distributed among Poaceae. Hydrolyzation
glandular.9 Chamarthi et al.20 reported that leaf glossiness, plu- of BX-glucosides by plastid-targeted β-glucosidases during tis-
mule and leaf sheath pigmentation were responsible for shoot sue damage leads to the production of biocidal aglycone BXs,
fly Atherigona soccata (Rondani) resistance in sorghum Sorghum which play an important role in plant defense against insects.28
bicolor (L.) (Moench). Phytoalexins include isoflavonoids, terpenoids, alkaloids, etc.,
Trichomes. Trichomes play an imperative role in plant defense that influence the performance and survival of the herbivores.29
against many insect pests and involve both toxic and deterrent The secondary metabolites not only defend the plants from dif-
effects.20,21 Trichome density negatively affects the ovipositional ferent stresses, but also increase the fitness of the plants. It has
behavior, feeding and larval nutrition of insect pests.21 In addi- been reported that maize HPR to corn earworm, Helicoverpa zea
tion, dense trichomes affect the herbivory mechanically, and (Boddie) is mainly due to the presence of the secondary metabo-

interfere with the movement of insects and other arthropods on lites C-glycosyl flavone maysin [2"-O-a-L-rhamnosyl-6-C-(6-
the plant surface, thereby, reducing their access to leaf epider- deoxy-xylo-hexos-4-ulosyl) luteolin] and the phenylpropanoid
mis.16 These can be, straight, spiral, hooked, branched, or un- product, chlorogenic acid.30 Compound, 4, 4-dimethyl cyclooc-
branched and can be glandular or nonglandular.9 Glandular tene has been found to be responsible for shoot fly A. soccata resis-
trichomes secrete secondary metabolites including flavonoids, tance in sorghum S. bicolor.31
terpenoids, and alkaloids that can be poisonous, repellent, or Secondary metabolites have been primarily studied as the medi-
trap insects and other organisms, thus forming a combination of ators of direct defense, however much is to be done to reveal the
structural and chemical defense.9,18 unidentified or emerging signaling pathways. Mass spectrometry
Induction of trichomes in response to insect damage has used for the secondary metabolite profiling and gene expression
been reported in many plants.22 This increase in trichome den- analysis by high-throughput sequencing has made this field more
sity in response to damage can only be observed in leaves devel- exciting and cost-effective. Study on secondary metabolites could
oping during or subsequent to insect attack, since the density lead to the identification of new signaling molecules involved in
of trichomes of existing leaves does not change.16 Dalin and plant resistance against herbivores and other stresses. Ultimately
Bjorkman 23 reported that damage by adult leaf beetles, Phratora genes and enzymes involved in the biosynthesis of these metabo-
vulgatissima L. in Salix cinerea L. induced higher trichome den- lites could be identified. Role of some of the secondary metabolites
sity in the new leaves developing thereafter. Likewise, increase in plant defense will be discussed below.
in trichome density in S. cinera in response to coleopteran dam- Plant phenolics. Among the secondary metabolites, plant phe-
age has also been reported.24 Increase in trichome density after nols constitute one of the most common and widespread group
insect damage has also been reported in Lepidium virginicum of defensive compounds, which play a major role in HPR against
L. and Raphanus raphanistrum L.22 In black mustard, trichome herbivores, including insects.4-6,18 Phenols act as a defensive mecha-
density and glucosinolate levels were elevated after feeding by nism not only against herbivores, but also against microorganisms
Pieris rapae (L.).25 Trichome density increased in Alnus incana and competing plants. Qualitative and quantitative alterations in
Moench as a result of damage by beetles.26 The increase in tri- phenols and elevation in activities of oxidative enzyme in response
chome density in response to herbivory is typically between to insect attack is a general phenomenon.5,6,32
25–100%, however, there are cases where 500–1000% increase Lignin, a phenolic heteropolymer plays a central role in plant
in trichome density has been reported. Changes in trichome defense against insects and pathogens.32 It limits the entry of
density occur within days or weeks after insect damage.22-24 pathogens by blocking physically or increasing the leaf tough-
Furthermore, change in relative proportion of glandular and ness that reduces the feeding by herbivores, and also decreases the
non-glandular trichomes is also induced by herbivory.22 A posi- nutritional content of the leaf.33 Lignin synthesis has been found
tive correlation has been observed between natural enemies’ to be induced by herbivory or pathogen attack and its rapid depo-
abundance and trichome density. Trichome exudates also serve sition reduce further growth of the pathogen or herbivore fecun-
as extra floral nectar (EFN) for scelonid egg parasitoid, of squash dity.33 Increase in expression of lignin associated genes (CAD/
bugs, Gryon pennsylvanicum Ashmead.27 CAD-like genes) in plants infected with pests and pathogens have
Secondary metabolites and plant defense. Secondary metab- been documented.32
olites are the compounds that do not affect the normal growth Oxidation of phenols catalyzed by polyphenol oxidase (PPO)
and development of a plant, but reduce the palatability of the and peroxidase (POD) is a potential defense mechanism in plants
plant tissues in which they are produced.1 The defensive (sec- against herbivorous insects. Quinones formed by oxidation of
ondary) metabolites can be either constitutive stored as inactive phenols bind covalently to leaf proteins, and inhibit the protein
forms or induced in response to the insect or microbe attack. The digestion in herbivores.34 In addition, quinones also exhibit direct
former are known as phytoanticipins and the latter as phytoalex- toxicity to insects.17,34 Alkylation of amino acids reduces the nutri-
ins. The phytoanticipins are mainly activated by β-glucosidase tional value of plant proteins for insects, which in turn negatively
during herbivory, which in turn mediate the release of various affects the insect growth and development.34 Phenols also play
biocidal aglycone metabolites.28 The classic examples of phyto- an important role in cyclic reduction of reactive oxygen species
anticipins are glucosinolates that are hydrolyzed by myrosinases (ROS) such as superoxide anion and hydroxide radicals, H2O2,

and singlet oxygen, which in turn activate a cascade of reactions defense against various stresses and their induction in response to
leading to the activation of defensive enzymes.35 Simple pheno- insect damage has been studied in many plants.44 For example,
lics (salicylates) act as antifeedant to insect herbivores such as e.g., in Populus species,45 and in Pinus sylvestris L.46 However,
Operophtera brumata (L.) in Salix leaves, and there is a negative no effect of herbivore damage on tannin content was observed
correlation between the salicylate levels and the larval growth, in Quercus serrata (Thunb.)47 and Betula pendula Roth.48 Like
however, salicylic acid (SA) is much more important as phytohor- proteinase inhibitors and oxidative enzymes, tannins have been
mone than as deterrent.36 reported to be systemically induced in neighboring leaves of the
Flavonoids. Flavonoids play a central role in various facets of damaged plant.45
plant life especially in plant-environment interactions.37 These Condensed tannins are oligomeric or polymeric flavonoids,
defend plants against various biotic and abiotic stresses including also known as proanthocyanidins. They have diverse struc-
UV radiations, pathogens and insect pests.37 Flavonoids are cyto- tures and functions. They act as feeding deterrents against some
toxic and interact with different enzymes through complexation. insects such as, Lymantria dispar (L.), Euproctis chrysorrhoea (L.)

Both flavonoids and isoflavonoids protect the plant against insect and O. brumata.49,50 Condensed tannins such as (+) -catechin, (+)
pests by influencing the behavior, and growth and development of - gallocatechin, and vanillin in leaves of Quercus robur L. inhib-
insects.36 In addition, flavonoids scavenge the free radicals includ- ited winter moth larvae, O. brumata.49 Procyanindin polymers
ing ROS, and reduce their formation by chelating the metals.37 have been found as feeding deterrent to Aphis craccivora (Koch)
Flavonoids are divided into various classes that include anthocya- in groundnut.51 Condensed tannins from Alaska paper birch
nins, flavones, flavonols, flavanones, dihydroflavonols, chalcones, (coated on birch leaves at 3% dry wt.) reduced the pupal mass
aurones, flavan, and proanthocyanidins.37 More than 5,000 flavo- and survival of Rheumaptera hastata (L.) larvae.52 It has been
nids have been reported in plants. A number of flavones such as reported that induction of tannins in Populus tremuloides Michx.
flavonols, flavones, proanthocyanidins, flavan 3-ols, flavonones, leaves in response to wound- and herbivore occurs by transcrip-
flavans, and isoflavonoids have been investigated as feeding tional activation of the flavonoid pathway.45 Genes responsible
deterrents against many insect pests. Flavonoids such as flavones for the production of tannins in response to wounding have been
5-hydroxyisoderricin, 7-methoxy-8- (3-methylbutadienyl)-fla- identified and are activated by the expression of a condensed
vanone and 5-methoxyisoronchocarpin isolated from Tephrosia tannins regulatory gene, PtMYB134, which is itself induced by
villosa (L.), T. purpurea (L.), and T. vogelii Hook, respectively damage.53 Furthermore, induction of tannin is also stimulated
have been found as feeding deterrents against Spodoptera exempta by light stress,14,53 and exposure to UV light in hybrid poplar.53
(Walk.), and Spodoptera littoralis Bios.38 Overexpressing a tran- However, some polyphagous insect species have the ability to tol-
scription factor controlling flavonoid production in Arabidopsis erate gallotannins, e.g., Shistocerca gregaria (Forsk.) tolerates tan-
has been reported to confer resistance against Spodoptera frugi- nins by hydrolyzing them rapidly to avoid any damaging effects
perda (J.E. Smith).39 Angustone A, licoisoflavone B, angustone B, by restricting the passage of tannins by adsorbing them on the
and angustone C. Isoflavones, licoisoflavone A, luteone, licoiso- thick peritrophic membrane, and by inhibiting the tannin pro-
flavone B, and wighteone have been found to be not only feed- tein complex formation by surfactants in the midgut.54
ing deterrents to insects, but also have antifungal activity against Plant defensive proteins. Ecologically, in insect-plant interac-
the fungi, Colletotrichum gloeosporiode (Penz.) and Cladosporium tion, interrelationship between two is important for the survival
cladosporioides (Fres.).40 Isoflavonoids (judaicin, judaicin-7-O-glu- of the both. Insects always look for a true and healthy host plant
coside, 2-methoxyjudaicin, and maackiain) isolated from the wild that can provide them proper food and could be suitable for mat-
relatives of chickpea act as antifeedant against Helicoverpa armig- ing, oviposition and also provides food for the offsprings. The
era (Hubner) at 100 ppm. Judaicin and maackiain were also found nutritional requirements of insects are similar to other animals,
to be deterrent to S. littoralis and S. frugiperda, respectively.41 and any imbalance in digestion and utilization of plant proteins
Cyanopropenyl glycoside and alliarinoside strongly inhibit feed- by the insects’ results in drastic effects on insect physiology.
ing by the native American butterfly, Pieris napi oleracea L., while Alteration of gene expression under stress including insect attack
a flavone glycoside, isovitexin-6"-D-β-glucopyranoside acts as a leads to qualitative and quantitative changes in proteins, which in
direct feeding deterrent to the late instars.42 turn play an important role in signal transduction, and oxidative
Tannins. Tannins have a strong deleterious effect on phy- defense (Table 1).4,55 Many plant proteins ingested by insects are
tophagous insects and affect the insect growth and development stable, and remain intact in the midgut, and also move across the
by binding to the proteins, reduce nutrient absorption efficiency, gut wall into the hemolymph. An alteration in the protein’s amino
and cause midgut lesions.18,43,44 Tannins are astringent (mouth acid content or sequence influences the function of that protein.
puckering) bitter polyphenols and act as feeding deterrents to Likewise, anti-insect activity of a proteolysis-susceptible toxic
many insect pests. They precipitate proteins nonspecifically protein can be improved by administration of protease inhibitors
(including the digestive enzymes of herbivores), by hydrogen (PIs), which prevent degradation of the toxic proteins, and allows
bonding or covalent bonding of protein-NH2 groups. In addi- them to exert their defensive function. Better understanding of
tion, tannins also chelate the metal ions, thereby reducing their protein structure and post-translational modifications contribut-
bioavailability to herbivores. When ingested, tannins reduce the ing to stability in the herbivore gut would assist in predicting tox-
digestibility of the proteins thereby decrease the nutritive value icity and mechanism of plant resistance proteins (PRPs). Recent
of plants and plant parts to herbivores. Role of tannins in plant advances in microarray and proteomic approaches have revealed

Table 1. Plant defensive proteins against insect pests
Putative defense protein Plant species Insect species Reference
Schizaphis graminum
Manduca sexta
Sorghum bicolor 150
Helicoverpa armigera
Tomato 56
Manduca sexta
Gossypium hirsutum 75
Spodoptera littoralis
PIs Solanum nigrum 77
Spodoptera exigua
Nicotiana attenuata 15
Spodoptera exigua
Transgenic Arabidopsis/oil seed rape 156
Plutella xylostella
Transgenic Arabidopsis/ tobacco 156
Mamesrra brassicae
Spodoptera littoralis

Cucumis sativus Spodoptera littoralis 149
Nicotiana attenuata Bemisia tabaci 152
Alnus glutinosa Agelastica alni 85
LOXs
Wheat Sitobion avenae 80
Tomato Macrosiphium euphorbiae Myzus persicae 91
Nicotiana attenuata Myzus nicotianae 92
Alnus glutinosa Agelastica alni

85
Arabidopsis Bemisia tabaci (whitefly)
152
Buffalograss Blissus oxiduus
81, 55, 86
Peroxidases Poplar Lymantria dispar
157
Medicago sativa Aphis medicaginis
57
Corn Spodoptera littoralis
158
Rice Spodoptera frugiperda
Manduca sexta
Tomato 56
Blissus oxiduus
PPOs Buffalograss 81
Spodoptera frugiperda,
Tomato 34
Helicoverpa armigera
Chitinases Sorghum bicolor Schizaphis graminum 150
Hevein-like protein Arabidopsis Bemisia tabaci 152
Catalase Bufallograssses Blissus oxiduus 81
SOD Medicago sativa Aphis medicaginis 157
that a wide spectrum of PRPs is involved in plant defense against Efficacies of carbohydrate binding plant lectins such as GNA,
herbivores.56,57 Due to diverse feeding habits of arthropods, mul- Phaseolus haemagglutinin, and wheat germ agglutinin, have been
tiple signaling pathways including jasmonic acid (JA), SA and/or studied in detail against many insect pests.59 Mannose - binding
ethylene (ET) regulate arthropod-inducible proteins.8 lectins have been reported to be effective against sucking insects,
Plant lectins. Lectins are carbohydrate-binding (glyco) proteins, because of their interaction with a specific carbohydrate residue of
ubiquitous in nature, and have protective function against a range the cell membrane.60 Expression of lectin coding genes in trans-
of pests.58,59 The insecticidal activities of different plant lectins genic plants and their defense against insects has been worked
have been utilized as naturally occurring insecticides against insect out in many plants, e.g., GNA, PSA (Pisum sativum L.; pea),
pests (Table 2).60 One of the most important properties of lectins WGA (Triticum vulgare Kunth; wheatgerm), ConA (Canavalia
is their survival in the digestive system of herbivores that gives them ensiformis (L.); jack bean), AIA (Artocarpus integrifolia Forst.;
a strong insecticidal potential.59 They act as antinutritive and/or jack fruit), OSA (Oryza sativa L.; rice), ASAL (Allium sativum
toxic substances by binding to membrane glycosyl groups lining L.), and UDA (Urtica dioica L.; stinging nettle).58,60,63 The Arum
the digestive tract, leading to an array of harmful systemic reac- maculatum L. lectin has been found effective against the aphids
tions.58,59 Lectins are stable over a large range of pH and damage the Lipaphis erysimi (Kalt.) and A. craccivora when incorpoated in an
luminal epithelial membranes, thereby interfere with the nutrient artificial diet.64
digestion and absorption.58 Disruption of lipid, carbohydrate, and Studies on the mechanism of action of the mannose-specific
protein metabolism causes enlargement and/or atrophy of key tis- lectin, GNA against brown planthopper (Nilaparvata lugens
sues, which in turn alters the hormonal and immunological status, (Stal.) in rice has shown that GNA binds to the luminal surface
threatening the growth and development of insects.58-60 of the midgut epithelial cells within the planthopper by recogniz-
Lectins have been found to be promising against homop- ing the cell surface carbohydrate moieties of glycoproteins and/
teran,58,60 lepidopteran,61 and coleopteran insects.61 Insecticidal or other glycoconjugates in the gut.65 Immuno-labeling GNA
properties of Galanthus nivalis L. agglutinin (GNA) were the assay has shown its presence in the fat bodies, ovarioles, and
first plant lectin shown to be active against hemipteran insects.62 hemolymph, indicating the ability of GNA to cross the midgut

Table 2. Plant defensive lectins and lectin like proteins and target insect pests
Lectin Plant Insect Reference
Tobacco Aphids 63
Allium sativum leaf lectin
Chickpea Aphis craccivora 58
Mayetiola destructor
Jacalin-like lectins Wheat 70
Anagasta kuehniella
Bauhinia monandra leaf lectin Tobacco 61
Zabrotes subfasciatus Callosobruchus maculates
Aphids 67
Rice
Nilaparvata lugens 60
Snowdrop lectin Wheat
Aphids 62
Arabidopsis
Pieris rapae, Spodoptera littoralis 149

Spodoptera littoralis, Manduca sexta,
Nictaba-related lectins NICTABA, PP2 Tobacco 69
Acyrthosiphon pisum
Arum maculatum lectin Lipaphis erysimi, Aphis craccivora 64
epithelial barrier and pass into the insect’s circulatory system lepidopteran,75 and hemipteran insects.76 The success of trans-
leading to systemic toxic effect.65 Partial resistance to homop- genic crops in expressing PIs against insect pests has accentu-
teran insect pests has been reported in transgenic plants express- ated the need to understand the mechanisms, and interactions
ing snowdrop lectin in tobacco,66 rice,67 and wheat.62 of multiple PIs with other defenses, and the adaptive responses
Plant lectins are induced by elicitors as an induced response to of the herbivores.
various stresses.68 JA induced the expression of NICTABA lectin Many classes of PIs are induced in plants in response to
in tobacco leaves.68,69 Induction of NICTABA by herbivores infes- stresses. Kunitz proteinase inhibitors (KPIs) are the serine PIs
tation including S. littoralis, Manduca sexta L. and Tetranychus (SPIs), which are among the most strongly upregulated defense
urticae Koch has been reported in tobacco plants.69 Expression genes in response to wounding or herbivore feeding in plants.14
of a mannose-binding jacalin-like lectin called Hessian fly, The SPIs from Solanum nigrum L. have been found to adversely
Mayetiola destructor (Say) responsive protein 1 (HFR1), and two affect a number of insect pests.77 Progress in genome sequenc-
chimerolectin- like proteins called HFR2 and HFR3 have been ing has resulted in identification of a large number of protein-
reported to be induced by the larvae of Hessian fly, M. destructor ase inhibitors and other defense components induced in plants
in wheat.70,71 Differences in feeding behavior of insects results in on account of herbivore damage. Although most of the KPIs
expression of different lectins, e.g., larvae of the fall armyworm, in plants are upregulated in response to insect herbivory, their
S. frugiperda induced HFR2, but not HFR3 expression while the degree of induction varies as per the insect plant interaction.
phloem-feeding bird cherry-oat aphid, Rhopalosiphum padi Koch, Various KPIs allow plants to deal with multiple generations of
induced HFR3 and HFR2, but latter was expressed much later insects by providing a genetic storehouse of varied PIs. However,
(12 d) than the former (24 h).70,72 Several jasmonate-inducible some insects respond to PIs by constitutive or induced produc-
lectins are expressed in leaf tissues of monocots such as rice, bar- tion of PI-insensitive proteases or by inactivation of ingested PIs,
ley, wheat, rye, and maize.73 Advancement of our understanding thereby, preventing them from binding to sensitive proteases.78
in induction of plant lectins in response to various stresses, espe- Such a feeding response by insects negatively affects the PI activ-
cially herbivory, and their role in plant defense has the potential ity, and may result in even greater damage to the plants.15 This
for utilization of these entomotoxic lectins in crop protection counter defense by the insects is a major hindrance to manipula-
through genetic engineering. Although, transformation of lectin tion and utilization of PIs for a longer-lasting plant defense, and
genes into plants seems to be very attractive and effective, care is there is a need to understand the mechanisms by which insects
needed, because of possible toxicity of some lectins to non-target counteract the PI-based plant defense.
organisms, including mammals. Enzymes. One of the important aspects of HPR against
Proteinase inhibitors. Proteinase inhibitors (PIs) cover one of insects is the disruption of insect’s nutrition. The enzymes that
the most abundant defensive classes of proteins in plants. Higher impair the nutrient uptake by insects through the formation of
concentration of PIs occurs in storage organs such as seeds and electrophiles includes peroxidases (PODs), polyphenol oxidases
tubers, and 1 to 10% of their total proteins comprise of PIs, (PPOs), ascorbate peroxidases, and other peroxidases by oxidiz-
which inhibit different types of enzymes and play an important ing mono- or dihydroxyphenols, that lead to the formation of
role in plant defense against insect herbivory (Table 1).74,75 PIs reactive o-quinones, which in turn polymerize or form covalent
bind to the digestive enzymes in insect gut and inhibit their adducts with the nucleophilic groups of proteins due to their elec-
activity, thereby reduce protein digestion, resulting in the short- trophilic nature (e.g., -SH or e-NH2 of Lys).34,55,79 Other impor-
age of amino acids, and slow development and/or starvation of tant antioxidative enzymes include lipoxygenases, phenylalanine
the insects.76 The defensive function of many PIs against insect ammonia lyase, superoxide dismutase, etc. Induction of antioxi-
pests, directly or by expression in transgenic plants to improve dative enzymes in plants following herbivory has received consid-
plant resistance against insects has been studied against many erable attention in recent years.4-6,55-59

Peroxidases (POD). Oxidative state of the host plants has litura (Fab.), H. armigera, Bemisia tabaci (Gen.), Tetranychus
been associated with HPR to insects,19,80 which results in pro- cinnabarinus (Boisd.), Myzus persicae (Sulzer), Empoasca fabae
duction of ROS, that are subsequently eliminated by antioxi- (Harris), Aphis medicaginis (Koch), S. exigua, and Agelastica alni
dative enzymes. POD constitutes one such group of enzymes, (L.).4,5,19,34,85 However, induced PPO levels had no or limited
which scavenges the ROS besides having other defensive roles. impact on L. dispar, Orgyia leucostigma (JE Smith),86 and Blissus
PODs are an important component of the immediate response of occiduus Barber.81
plants to insect damage.4,5,55 PODs are monomeric hemoproteins Lipoxygenases. Lipoxygenases (LOXs) are another group of
distributed as soluble, membrane-bound, and cell wall-bound anti-oxidative enzymes involved in plant defense against many
within the cells, and are widely spread in plants and include sev- stresses through octadecanoid pathway.87 They catalyze hydro-
eral isozymes, whose expression depends on tissue, developmen- peroxidation of polyunsaturated fatty acids resulting in the for-
tal stage, and environmental stimuli.19,55 A number of process mation of fatty acid hydroperoxides. The latter are enzymatically
are regulated by PODs that have direct or indirect role in plant and/or chemically degraded to unstable and highly reactive alde-

defense, including lignification, suberization, somatic embryo- hydes, γ-ketols, epoxides,87 and ROS such as hydroxyl radicals,
genesis, auxin metabolism, and wound healing.19,81,82 Role of singlet oxygen, superoxide ion and peroxyl, acyl and carbon-cen-
PODs in plant resistance to insect pests has been studied in tered radicals.35,87 The unstable reactive products interact with
various plant systems(Table 1).5,6,55 Production of phenoxy and proteins resulting in protein-protein cross linking and amino
other oxidative radicals by the PODs in association with phenols acid damage that in turn affects the amino acid assimilation.35
directly deter the feeding by insects and/or produces toxins that In addition, lipid peroxidation end products also act as insect
reduce the plant digestibility, which in turn leads to nutrient repellents or antixenosis87 and are toxic to insect pests (antibio-
deficiency in insects with drastic effects on their growth and sis).34,35 Major substrates of LOX in plants are linoleic and lino-
development.57,83 In addition, PODs have been reported to have lenic acids. One of the most important aspects of LOX in plant
direct toxicity in guts of herbivores.78 PODs have been purified defense is the oxidation of linolenic acid in JA signaling pathway,
and characterized from many plants where they were induced in which in turn plays a leading role in activation of plant defense,
response to insect attack.19,55,84 both directly by production of oxidative enzymes and protease
Polyphenol oxidases (PPO). The PPOs are important inhibitors,88 and indirectly through the production of volatile
enzymes in plants that regulate feeding, growth, and develop- organic compounds (VOC) that attract the natural enemies of
ment of insect pests, and play a leading role in plant defense insect pests.87 Oxygenation of polyunsaturated fatty acids has
against the biotic and abiotic stresses.19,34 PPOs can function been found to be catalyzed by LOX, which results in the produc-
in following ways: a) PPO-generated quinones could alkylate tion of hydroperoxides that are metabolized to compounds such
essential amino acids, decreasing plant nutritional quality, (b) as JA and traumatin.89
quinones may produce oxidative stress in the gut lumen through Induction of LOX activity in response to herbivory has been
redox cycling, and (c) quinones and ROS produced by phenolic studied in many plants such as soybean in response to two-spot-
oxidation, could be absorbed and have toxic effects on herbi- ted spider mite, T. urticeae,90 (Table 1) in tomato in response to
vores. The PPOs are metallo-enzymes that catalyze the oxida- aphids, Macrosiphium euphorbiae Thom., and M. persicae,91 in
tion of monophenols and o-diphenols to quinones, which are N. attenuata following infestation by Myzus nicotianae Black.92
highly reactive intermediate compounds that readily polymer- and in wheat following Sitobion avenae (F.) infestation.80 The
ize, and react with nucleophilic side chain of amino acids and N. attenuata plants deficient in LOX are more vulnerable to
crosslink proteins, thereby reducing the availability of such pro- attack by M. sexta, which also attract the new herbivores such
teins, and affect the nutritional quality of the food.34,83 Under as Empoasca spp,92 as compared with the plants where LOX3-
acidic conditions, quinones form semiquinone radicals that in mediated defense reduced larval growth, food consumption,
turn give rise to ROS, while under basic conditions; quinines and frass production.93 Maize plants transformed with the wheat
react with cellular nucleophiles.34 Quinines are more toxic to oxalate oxidase gene had upregulation of LOX transcripts and
plant herbivores than the original phenols.34 In addition to their elevation of free phenolics (14-fold), which were positively asso-
role in digestibility and palatability of plant tissues, melanin for- ciated with resistance to the European corn borer, O. nubilalis.88
mation by PPOs increases the cell wall resistance to insects and Indirect defenses. The defensive response in plants to attract
pathogens.80 Induction of PPO activity under abiotic and biotic natural enemies of herbivores plays a pivotal role in protect-
stresses and by treatment with compounds related to the octa- ing the plants against herbivore attack.7 Indirect defenses can
decanoid pathway makes it an important tool in plant resistance be constitutive or induced as a result of combined action of
against different stresses.19,34 The PPO genes are differentially mechanical damage and elicitors from the attacking herbivore.
induced by signaling molecules and injury due to wounding, Production of volatiles and the secretion of extra floral nectar
and pathogen, or insect infestation.34,80 Correlation between (EFN) mediate interactions of plants with natural enemies of
induction of PPO activity and insect fitness has been reported in the insect pests (i.e., parasitoids or predators), which actively
many plants including tomato and lettuce.34,82 Although PPOs reduce the numbers of feeding herbivores.7,94 Induced indirect
accumulate in leaves, roots, stems and flowers of the plants, defenses have received increasing attention recently and have
young tissues with greater vulnerability to insect attack exhibit been studied on the genetic, biochemical, physiological, and
greater induction. The PPOs confer resistance to Spodoptera ecological levels.7,8,94

Herbivore induced plant volatiles (HIPVs). Plants indirectly the potential of attracting crop pests. For example, Colorado
defend themselves from herbivore feeding by emitting a blend of potato beetles, Leptinotarsa decemlineata (Say) is attracted to a
volatiles and non-volatile compounds. Herbivore-induced plant blend of volatiles consisting of cis-3-hexenyl acetate, linalool, and
volatiles (HIPVs) play an important role in plant defense by MeSA.102
either attracting the natural enemies of the herbivores or by act- Compounds such as ester methyl salicylate (MeSA), mono-
ing as feeding and/or oviposition deterrent.7,8 HIPVs are the lipo- terpenes myrcene and β-ocimene, homoterpene (E, E)-4, 8, 12-
philic compounds with higher vapor pressure which are released trimethyltrideca-1, 3, 7, 11-tetraene (TMTT), and sesquiterpene
from the leaves, flowers, and fruits into the atmosphere, and into (E, E)-α-farnesene are emitted hours after infestation.7 Systemic
the soil from the roots by plants in response herbivore attack.7 release of VOCs is one of the best studied responses specific to
The HIPV’s produced vary according to the plant and herbivore herbivores. The HIPVs defend the plants either directly by repel-
species, the developmental stage and condition of the plants and ling, deterring and toxicity to the herbivore or indirectly by
the herbivores.8,94 An optimum quantity of volatile compounds attracting the natural enemies of the attackers, and thus, protect

is normally released by the plants into the atmosphere, whereas a the plants from further damage.7,94 Lipoxygenase and Shikimic
different blend of volatiles is produced in response to herbivory.8 acid pathway metabolites and terpenoid pathway products (terpe-
The volatile blend released by plants in response to insect attack noids) play an important role in plant defense, both directly and
is specific for a particular insect-plant system, including natu- indirectly.79 Period specific volatile emission has been observed
ral enemies and the neighboring plants.8,95 The HIPVs mediate in many plants e.g., lima bean leaves attacked by S. littoralis,103
the interactions between plants and arthropods, microorgan- and hybrid poplar (Populus trichocarpa Torr. and A. Grey X del-
isms, undamaged neighboring plants, or intraplant signaling that toides) leaves infested by forest tent caterpillar, L. dispar emitted
warns undamaged sites within the plant.8,10 Depending upon a blend of volatiles containing (E)-β-ocimene and other mono-,
the modes of feeding of insect pests, different defense signaling sesqui- and homoterpenes.104 Maize plants when exposed to
pathways are activated, which induce the production of specific (Z)-3-hexanol induced the volatile blend emission that is usu-
volatile compounds.29 ally released after caterpillar infestation, and attracts the natural
The HIPVs include terpenes, green leafy volatiles (GLVs), enemies.105
ethylene, methyl salicylate and other VOCs.7,94 The well-studied Priming of the volatile emission signals has been reported in
metabolites of hydroperoxide lyase (HPL) branch of oxylipin- many plants.7,106 Engelberth et al.95 reported that application of
pathway producing stress-inducible compounds are the GLVs. GLV compounds such as (Z)-3-hexanal, (Z)-3-hexen-1-ol, and
GLVs are reactive electrophile species involved in stress and (Z)-3-hexenyl acetate individually and blend of volatiles to the
defense signals. GLVs consist of C6-aldehydes [(Z)-3-hexenal, maize seedlings enabled the seedlings to respond to wound-
n-hexanal] and their respective derivatives such as (Z)-3-hexenol, ing and beet armyworm, S. exigua caterpillar regurgitate, and
(Z)-3-hexen-1-yl acetate, and the corresponding E-isomers.8,96 To resulted in accumulation of JA and sesquiterpenes as compared
understand the role of C6-aldehydes and their respective deriva- with the control plants. Similar observations were recorded by
tives in plant defense, the GLVs levels have been altered either Kessler et al.106 in N. attenuata in response to M. sexta infestation,
by application of elicitors,96 or by manipulating genetically the where low damage was shown by plants primed with clipped
HPL expression in plants. GLVs play an important role in plant sagebrush-released volatiles. Thus, priming plays an important
defense by attracting natural enemies.3,7,8,96 Plant volatiles such as role in plant defense by incomplete turning on of defense related
methyl salicylates and the C16 - homoterpene 4, 8, 12-trimethyl-1, processes to reduce the biochemical investments until the onset
3(E), 7(E), 11-tridecatetraene [(E, E)-TMTT] have been found of actual attack.95,106 However, there are a few reports where some
to attract the predatory mites.97 The most frequent component non-target insect pests were also attracted on account of volatile
of the HIPVs is methyl salicylate (MeSA), and has been reported emission in infested plants, thereby, increasing the insect attack
in the headspace of many insect-infested plants including lima on the plant.107
bean,8 and Arabidopsis.98 MeSA is a ubiquitous component of Transgenic Arabidopsis with overexpression of strawberry
many leaf and floral blends and MeSA baited sticky cards attract nerolidol synthase, a terpene synthase (TPS) responsible for the
many insect predators including the big- eyed bug, Geocoris pal- production of sesquiterpene alcohol (3S)-(E)-nerolidol has been
lens Stal., ladybird beetle, Stethorus punctum picipes (Casey), green reported to attract the predatory mite, P. persimilis.108 The para-
lacewing Chrysopa nigricornis Burmeister,99 and other natural sitic wasp, Cotesia marginiventris (Cresson) was attracted to the
enemies.97 Ulland et al.100 reported the inhibition of oviposition lepidopteran larvae infesting transgenic maize plants with over-
of cabbage moths Mamestra brassicae L. by MeSA released during expression of the corn TPS10 gene responsible for the formation
infestation, suggesting that MeSA can also be detected by the of (E)-β-farnesene, (E)-α-bergamotene, and other herbivore
attacking herbivores. Methyl benzoate (MeBA), which structur- induced sesquiterpene hydrocarbons.109
ally resembles MeSA, has also been detected from insect-infested In addition to the plant volatiles released from aerial parts of
plants.98 S. frugiperda infestation in rice induces emission of the plant, roots have also been found to release diverse volatiles
about 30 volatiles, including MeSA and MeBA, which are highly that defend the plants from belowground insect pests by acting as
attractant to the natural enemies of S. frugiperda, such as, Cotesia antimicrobial and antiherbivore, and also by attracting the natu-
marginiventris (Cresson).101 However, there is an ecological cost ral enemies of the root feeding insect pests.7 Root feeding insect,
of using HIPVs to engineer natural enemies; because HIPVs have Diuraphis noxia (Mord.) triggers the emission of 1, 8-cineole,

a monoterpene volatile, which is toxic and repellent to some by the proteolytic fragmentation of plastidic ATP synthase,
insects.110 Sesquiterpene (E)-β-caryophyllene produced by maize γ-subunit,122 whereas caeliferins are sulfated fatty acids, in the
roots in response to feeding by the larvae of Diabrotica virgifera oral secretion of S. americana (Stal.), and other grasshopper spe-
virgifera LeConte attracts the nematode Heterorhabditis megidis cies.123 The lipase activity of grasshopper oral secretions evoked
Poinar.111 However, root emitted volatiles such as 1,8-Cineole an immediate and quick accumulation of various oxylipins, such
inhibits the growth of Brassica campestris seedlings due to the as, 13-hydroperoxy octadecatrienoic acid, 12-oxo-phytodienoic
inhibition cell proliferation more severely than cell elongation acid (OPDA), JA, and jasmonic acid-isoleucine in Arabidopsis.124
because root growth requires both elongation and proliferation Furthermore, there was increase in cytosolic calcium, ethylene
of the constituent cells,112 and also due to the interference with emission and activity of MAPKs on treatment with grasshopper
nuclear as well as organelle DNA synthesis in root apical meristem oral secretions.124
and alteration in root phospholipids and sterol composition.113 Role of phytohormones in induced resistance in plants.
Defense elicitors (insect oral secretion). Plants undergo a Plant defense against herbivore attack involves many signal

dynamic change in transcriptomes, proteomes, and metabolomes transduction pathways that are mediated by a network of phyto-
in response to herbivore-induced physical and chemical cues such hormones. Plant hormones play a critical role in regulating plant
as insect oral secretions (OS) and compounds in the oviposition growth, development, and defense mechanisms.2 A number of
fluids. It is generally believed that insect-induced plant responses plant hormones have been implicated in intra- and inter-plant
are mediated by oral secretions and regurgitates of the herbivore. communication in plants damaged by herbivores. Most of the
The defenses generated by various elicitors differ based on the plant defense responses against insects are activated by signal-
type of the elicitor and the biological processes involved.114 A transduction pathways mediated by JA, SA, and ethylene.79,125
potential elicitor of herbivore-induced plant volatiles from the Specific sets of defense related genes are activated by these path-
regurgitate of Pieris brassicae L. larvae has been identified as ways upon wounding or by insect feeding. These hormones may
β-glucosidase which results in emission of a volatile blend from act individually, synergistically or antagonistically, depending
mechanically wounded cabbage leaves that attract the parasitic upon the attacker.
wasp, Cotesia glomerata (L.).115 Jasmonic acid. Although various phytohormones are involved
Fatty acid-amino acid conjugates (FACs) are the major com- in plant defense against herbivores, JA is the most important
ponents in the oral secretions of insects. The first FAC elicitor phytohormone linked to plant defense against herbivores and
identified was volicition, N-(17-hydroxylinolenoyl)-L-glutamine activates the expression of both direct and indirect defenses.4,5,125
(volicitin), detected in the OS of beet armyworm larvae, S. JA is derived from linolenic acid through octadecanoid pathway
exigua.116 Volicitin when applied on Zea mays L. induced the and accumulates upon wounding and herbivory in plant tissues.83
emission of elicitor that attracts the natural enemies of the Chewing of plant parts by insects causes the dioxygenation of lin-
feeding larvae.116 N-linolenoyl-glu isolated from regurgitate of oleic acid (18:2) and linolenic acid (18:3) by specific LOXs at C9
tobacco hornworm, M. sexta has been found to be a potential or C13 to form (9S)- or (13S)-hydroperoxy-octadecadi(tri)enoic
elicitor of volatile emissions in tobacco plants.117 The FACs in acids, which are converted into 12-oxophytodienoic acid (12-
OS of insects have been found to activate mitogen-activated pro- OPDA) by allene oxide synthase and allene oxide cyclase. OPDA
tein kinase (MAPK) pathway, that regulate plant growth and is transferred to the peroxisome, where it is reduced by OPDA
development, and play an important role in signaling transduc- reductase 3 (OPR3), forming JA. Oxidative burst produces ROS,
tion in responses to various stresses including cold, heat, ROS, which convert linolenic acid into phytoprostanes that signal trans-
UV, drought, pathogen and insect attack.118 FACs in oral secre- duction pathways.93 A broad spectrum of defensive responses are
tions of M. sexta, when applied to the wounded leaves have been induced by jasmonates that include antioxidative enzymes, PIs,
found to activate signaling processes that lead to the activation VOCs, alkaloid production, trichome formation, and secretion
of MAPKs, salicylic acid-induced protein kinase (SIPK) and of EFN.88,102,114 A large numbers of genes involved in defense
wound-induced protein kinase (WIPK), and bursts of jasmonic against herbivores are regulated by JA.125 Concentration of indole
acid (JA), JA-isoleucine conjugate (JA-Ile), salicylic acid (SA), glucosinolate, an important defensive compound, is induced by
and ethylene.118,119 In wild rice, Oryza minuta Presl., expres- jasmonates. In addition to its role in the production of JA, OPDA
sion of putative MAPK, OmMKKI, is induced by brown plant signals the defense pathways individually. For example, OPDA
hopper, N. lugens feeding.120 Several other FAC elicitors such as signaling regulates the CORONATIN-INSENSITIVE 1 (COI1)
N-acyl Gln/Glu have been isolated from regurgitates of vari- -dependent and -independent transcription,126 alters the intracel-
ous lepidopteran species.8 The FACs has also been reported to lular calcium levels and cellular redox status.127 Jasmonates (most
induce accumulation of 7-epi-jasmonic acid, an octadecanoid- likely the JA-amino acid conjugate jasmonoyl-isoleucine) have
derived phytohormone, which is a potent elicitor of transcripts been found to interact with the COI1 unit of an E3 ubiquitin
of herbivore-responsive genes in tobacco plants.117 The FACs in ligase complex, termed SCFCOI1 (Skip/Cullin/F-box–COI1),
lepidopteran OS evoke specific responses such as transcriptomic which promotes binding of the COI1-unit to JAZ (jasmonate
and proteomic alteration, induction of nicotine, and proteinase ZIM-domain) proteins, resulting in degradation of JAZ proteins,
inhibitors in N. attenuate.121 Besides FACs, other groups of elici- which otherwise suppress JA-inducible gene expression.128 JA has
tors identified in insect oral secretions include inceptins,122 and also been reported to affect calcium-dependent protein kinases
caeliferins.123 Inceptins are disulphide-bonded peptides formed (CDPK) transcript, and activity in potato plants.129 CDPKs

comprise of a large family of serine/threonine kinases in plants signaling pathways.35 Herbivore induced signals rapidly spread
(34 members in Arabidopsis) and play an important role in plant over the leaf and leads to a strong Ca 2+ -dependent transmem-
defense against a variety of biotic and abiotic stresses through sig- brane potential (Vm) depolarization in the damage zone, and is
nal transduction.130 In addition to the role played by JA in direct followed by a transient Vm hyperpolarization in the surround-
resistance against insect pests through the induction of various ing area, and a constant depolarization at distances greater than
defensive compounds, its role in indirect resistance has also been 6–7 mm.35,139 Organelle and apoplastic fluid Ca 2+ concentration
well established.86 For example, EFN produced by JA is used as is generally higher (about 104 to 105 times) as compared with
an alternate food by natural enemies of insect pests.131 JA also that in the cytosol (100 and 200 nM.). However, upon insect
induces the defense enzymes such as POD,4,5,125 and PPO.4,5,80 attack, the cytosolic Ca 2+ increases, which in turn activates the
Salicylic acid. Salicylic acid (SA), a benzoic acid derivative, is an calcium-sensing proteins such as calmodulin, calmodulin-bind-
important phytohormone involved in regulation of plant defense.132 ing proteins, and calcium-dependent protein kinases (CDPKs)
It is an important endogenous plant growth regulator that gener- that promote the signaling events such as, phosphorylation and

ates a wide range of metabolic and physiological responses in plants transcriptional change.139,140 However, CDPKs are the impor-
involved in defense in addition to their impact on plant growth and tant proteins against biotic and abiotic stresses, which form Ca 2+
development.133 Responses to SA depend on a regulatory protein sensors that contain a protein kinase domain and a calmodulin
called Non-Expressor of Pathogenesis-Related Genes1 (NPR1).134 like domain (including an EF-hand calcium-binding site) in a
The NPR1 gene is activated through redox pathways by SA accu- single polypeptide.130,141 NtCDPK2 regulates the activation of
mulation and is translocated to the nucleus, however, it does not stress-induced MAP kinases in tobacco.142 Involvement of two
bind to DNA directly, but acts through transcription factors.134 SA Arabidopsis CPKs (CPK3 and CPK13) in herbivory-induced
induces greater defense against piercing and sucking type of insect signaling network through HsfB2a-mediated regulation of the
pests than the chewing ones.80 SA signaling molecule is involved in defense-related transcriptional machinery has been observed in
local defense as well as induction of systemic resistance. Production tobacco.139 Damage by S. littoralis larvae on Phaseolus lunatus L.
of ROS by SA pathway has been proposed to induce resistance induced Ca 2+ not only in cells adjacent to the feeding site, but
in plants against insect pests, e.g., in tomato plants against H. throughout the leaf.35 Expression of calmodulin binding pro-
armigera.135 H2O2 induced by SA in plants defends them against teins involved in plant defense signaling increased considerably
various insect pests since H2O2 actively damages the digestive sys- in wheat damaged by D. noxia and Arabidopsis by M. persicae.140
tem of insects leading to reduced growth and development.35,135 Role of reactive oxygen species (ROS) in plant defense.
Furthermore, SA signals the release of plant volatiles that attract Oxidative state of plants is an important tactic that enables plants
the natural enemies of insect pests, e.g., Lima bean and tomato to defend against various stresses. Rapid and transient genera-
plants infested by spider mite attract the natural enemies of spider tion of ROS is a common phenomenon in plants on account of
mite.97 However, it has been reported that SA and JA act antagonis- oxidative stress due to biotic and abiotic factors.35,141 ROS play
tically, where SA inhibits the activity of JA and vice versa.35 MeSA versatile signaling functions that mediate multiple responses,
serves as a volatile signal to trigger induced defenses in plants, and can also act directly as toxins. However, production of ROS
including HIPV emission, and a number of predaceous arthropods on account of biotic stress is still debatable.35 ROS include par-
are attracted to MeSA under field conditions.35,97 tially reduced forms of oxygen such as superoxide (O-), hydrogen
Ethylene. Ethylene is an important phytohormone, which plays peroxide (H2O2), and hydroxyl radicals (HO-).35,141,142 Distinct
an active role in plant defense against many insects.136 Ethylene signaling pathways are activated by different types of ROS espe-
signaling pathway plays an important role in induced plant defense cially the ones involving MAPKs.141,142 Rapid increase in ROS
against herbivores and pathogens both directly and indirectly,136 content under stress conditions is referred as “oxidative burst.”35
however, there are limited reports on its role in indirect defense Following insect attack, ROS accumulate in apoplastic as well as
through the emission of HIPVs.137 ET signaling pathway works in symplastic regions, besides their main concentration in exo-
either synergistically or antagonistically,138 with JA in expression of cellular matrix, peroxisomes/mitochondria, and plasma mem-
plant defense responses against pathogens and herbivorous insects. brane.35,141 Apoplastic burst of ROS acts as a first barrier against
It has been reported that ET and JA work together in tomato in PIs subsequent attack by the pathogens and herbivores.65 Being
expression.138 Infestation by A. alni induced the emission of ethylene highly reactive, ROS can potentially react with and/or cause
and release of various valatiles in Alnus glutinosa L. leaves in addi- damage to proteins, lipids, and nucleic acids. However, to prevent
tion to mono-, sesqui and homoterpenes.85 ET precursor, 1-amino- the self-toxicity of ROS, plant cells have developed ROS scaveng-
cyclopropane-1-carboxylic acid has been reported to enhance the ing systems for removing the excess ROS to maintain a relatively
volatile emission from the JA treated detached leaves.107 Ethylene low and constant ROS concentration.1,35
further induced the emission of volatiles induced by volicitin, JA or Among all the ROS, high stability and freely diffusible H2O2
(Z)-3-hexen-ol in maize.105 is a central component of induced defense response in plants
Role of Calcium ions (Ca 2+) in plant defense. Plant defense against different stresses.35,141,142 Although H2O2 is produced in
elicitors induced in plants upon herbivory undergo differ- various ways, the oxidative burst is supposed to occur through
ent signal transduction pathways. Ca 2+ signaling is one of the the activation of membrane bound NADPH complex. NADPH
early events in insect-plant interaction, where Ca 2+ acts as a oxidase generates superoxide anion at the plasma membrane or
second messenger, which in turn mediates a number of plant in the apoplast extracellularly, which is then converted to H 2O2

by superoxide dismutase (SOD).35,141 Besides having direct effect expression levels have also been used to analyze the differences
on the pathogens and herbivores, H2O2 stimulates a cascade of in transcriptional profiles of different genotypes within a plant
reactions that lead to the expression of defense genes, which pre- species.89,147 A large numbers of genes (2182) are expressed by the
vent the plants from subsequent attack by pathogens and her- aphid, M. persicae as compared with caterpillar, P. rapae (186)
bivores.141 H2O2 application in Arabidopsis results in up- and attack.149 Lepidopterans usually elicit changes in the expression
downregulation of many genes (113 and 62 genes, respectively), of genes involved in glucosinolate metabolism in Brassicaceae,
suggesting that ROS act as secondary messengers to control gene detoxification, cell survival, and signal transduction,149 while
expression.143 ROS also play an important role in mediating cross- the aphids regulate the expression of genes involved in cell wall
linking of cell wall components by peroxidase, and also for the modifications, oxidative stress, calcium-dependent signaling,
activation of many defenses related genes.141 Oxidative changes in and glucosinolate synthesis.146 Different attackers face different
plants after insect attack cause oxidative damage to insect mid- responses in plants based on the feeding behavior and the plant
gut, mainly due to accumulation of H2O2.35,141 Many physiologi- attacked; e.g., transcriptional changes in Arabidopsis thaliana (L.)

cal and molecular responses in plants against insect attack are in response to feeding by aphid, M. persicae and whitefy, Bemisia
triggered by H2O2, and its levels remain elevated as long as the tabaci (Gen.).151,152 Different plants respond differently to the
herbivore attack persists.35,141 Induction of H2O2 has been studied same herbivore, e.g., two white cabbage cultivars differ consid-
in oat, wheat, barley and groundnut against D. noxia, R. padi, erably in gene expression in response to feeding by P. rapae.147
Schizaphis graminum Rond., H. armigera and S. litura.4,5,132,139 Combination of various technologies such as genetic, genomic
Argandona et al.144 observed induction of H2O2 in barley infested tools including microarrays, deep sequencing, and transcrip-
with S. graminum after 20 min of infestation, indicating that tional profiling tools and proteomics through mass spectrometry
H2O2 could be the beginning of a cascade of physiological and will advance our understanding of molecular mechanisms of
molecular events leading to production of further defensive com- plant defense against insect herbivores to a greater extent.
ponents, and protection of plants from subsequent damage. ROS Transgenerational induced resistance to herbivores. Biotic
mediate the defensive gene activation and establish additional and abiotic stresses in plants have been found to induce resistance
defenses by regulating the transcription and/or by interacting not only in the maternal plants, but also in the offsprings.153 This
with other signal components like phosphorylation in plant sys- maternally induced resistance (transgenerational immunity) has
tems in response to a variety of stresses.35,141 been found to protect the progeny of plants exposed to herbivory
Gene expression: The basic process of plant defense. from insect pests, besides producing vigorous seeds and seed-
Extensive rearrangements in gene expression occur in plants in lings.153 However, there are only few reports on transgenerational
response to herbivory with hundreds, and even up to several immunity of plants against insect pests. Wild radish plants,
thousands of genes getting up- or downregulated.57,145 Advances R. raphanistrum damaged by P. rapae or treated with JA produce
in genomics and transcriptomics including availability of whole- offspring’s with high levels of induced resistance to this insect.154
genome sequence data, expressed sequence tags (ESTs), and Arabidopsis plants exposed to stresses such as, cold, heat and
microarrays, has led to better understanding of the changes in flood, resulted in a higher homologous recombination frequency
gene-expression profiles in response to insect attack.139,146,147 and increased genome methylation, which in turn induced the
DNA microarrays provide a closer and complete view of gene- resistance to stress in the progeny.155 Maternal plants with low to
expression patterns and signaling responses mediated by insect intermediate levels of herbivore damage could produce the seeds
elicitors and plant signals, and has proven to be exceptional that are more vigorous and seedlings that are resistant to insect
tools to monitor the expression of thousands of genes simultane- pests.154 However, further studies are required to understand the
ously.147 However, with the advent of next-generation sequenc- genetic and molecular mechanisms of such signaling interac-
ing (NGS) technologies, it is anticipated that microarrays will tions. Furthermore, research on plant-insect interactions should
be soon replaced by some new and innovative technologies be focused not only to genetic effects, but also toward the epigen-
like RNA-sequencing, RAD-sequencing, and reduced repre- etic regulation of plant defense pathways and insect responses,
sented sequencing etc., for measuring gene expression directly. because a substantial body of evidence has been demonstrated
Expression quantitative trait loci (eQTL) mapping has revolu- for mobile siRNA signals and inheritance of DNA methylation
tionized the area of gene expression. The eQTL mapping is hav- based changes in gene expression. There is much need for in-
ing the advantage of dealing with thousands of traits at a time depth studies on this subject to exploit it for pest management
and has been used in many plants including Arabidopsis and by manipulating the maternal ecology. An understanding of
rice.148 Investigation of inducible defenses in Arabidopsis against transgenerational induced resistance might answer some of the
P. rapae and Brassica oleracea var capitata L. and Brassica nigra intricate questions regarding the ability of plants to withstand
L., or the aphid Brevicoryne brassicae L. by microarrays has been herbivore damage.
studied extensively.147,149 Responses against feeding of D. noxia
(Mord.), S. graminum, M. nicotianae, M. persicae and S. avenae Future Outlook
on foliage of Arabidopsis, celery, sorghum, Apium graveolens L.
cereal, tobacco or wheat plants have been well established.80,92,150 Although induced resistance has attained a considerable
Change in gene expression profiles after herbivory has shown momentum recently, and has attracted the attention of scien-
a substantial reallocation of plant resources to defense. Gene tists in evolutionary ecology, entomology, plant physiology, and

biotechnology, much of the underlying mechanism have still for conferring resistance to the herbivores through genetic trans-
remained unanswered. There is a need to understand the herbi- formation. However, before using an elicitor effectively in agri-
vore-specific signal molecules, their identification, mode of action, cultural systems, it is important to understand the chemical
and further signal transduction. Since a single attribute can affect changes they induce in the plant, the effect of these chemicals
the herbivores and/or natural enemies positively and/or nega- on the herbivores especially in the field, and to see if there is any
tively, understanding of the multitrophic interactions is impor- alteration in plant growth and yield. The Eco-genomic approach
tant to know the consequences of supposed defensive traits of a which includes association and correlation studies, natural selec-
plant for use in pest management. An understanding of induced tion mapping, and population genomics enables the estimation
resistance in plants can be utilized for interpreting the ecologi- of variable selection at (sets of) loci, and differentiates this from
cal interactions between plants and herbivores and for exploiting processes acting on the whole genome, such as migration and
in pest management in crops. Since the biochemical pathways genetic drift. Eco-genomics needs to be much more explored and
that lead to induced resistance are highly conserved among the the consequences of (plasticity in) expression of genes for com-

plants, the elicitors of these pathways could be used as inducers munity processes need to be well understood, since the shape of
in many crops. The future challenge is to exploit the elicitors of a particular interspecific interaction is ubiquitous. Moreover, this
induced defense in plants for pest management, and identify the approach enables the linking of different sub cellular processes to
genes encoding proteins that are up and/or downregulated dur- particular community structures, and the big challenge ahead is
ing plant response to the herbivore attack, which can be deployed the implementation of these results in a spatial framework.
13. Agrawal AA, Janssen A, Bruin J, Posthumus MA, 22. Agrawal AA. Induced responses to herbivory in wild
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