Details :

Chemical Dialoguesbetween pests and their host plants:

Special reference to their role in Sweet potato pest’s Management

 

Rajasekhara Rao Korada* and TanmayeeSamantaray

 

ICAR-Central Tuber Crops Research Institute, Regional Centre, Bhubaneswar, Odisha 751019.

*Email: rajasekhararao.korada@gmail.com

 

 

            Plants are reported to produce distinct blends of herbivore-induced volatiles, and these are known to attract a range of herbivore enemies, including predators and parasitoids drawn from five insect orders, plus predatory mites, nematodes and birds. Herbivore associated plant volatiles have always been assumed to have real value for herbivore enemies, although this has rarely been subject to detailed analysis. Herbivorous insects respond to changes in plant odour production, which influence the herbivore fitness costs of plant volatile production on insect growth and survival.

 

Herbivore produced elicitors

 

            At the instant an insect begins to chew on a leaf there is a biochemical cascade of events that precedes changes in plant defense gene expression. The defense signaling that occurs following this physical injury is ultimately shaped by the interactions of a multitude of potential players—the plant, the insect and their associated microbes. Although often overlooked, the plant surface cuticle or phylloplane is frequently inhabited by diverse communities of bacteria, filamentous fungi, yeasts, and even free-living amoebae. FAC elicitors are clearly not the only compounds produced by chewing caterpillars with the potential to induce defensive reactions by plants or otherwise affect their biochemistry. Schmelzet al. (2006) demonstrated induced volatile release in cowpea seedlings fed on by fall armyworm caterpillars. While volicitin and N-linolenoyl-L-glutamine were found in the regurgitant of these caterpillars, they failed to stimulate any significant response. This finding led to the discovery of inceptins, a new class of peptide elicitors of cowpea volatiles from fall armyworm regurgitant (Schmelzet al., 2006). Inceptin is a disulfide bridged peptide ( ICDINGVCVDA_) derived from the chloroplastic ATP synthase of the plant on which the caterpillars feed. Amounts as low as 1 fmol per leaf induce increased levels of jasmonic acid and salicylic acid in cowpea leaves and release of ethylene and terpenoid volatiles (Schmelzet al., 2006).

 

 

 

 

Specificity in plant volatile emission

 

            Each plant species emit a distinct blend of volatile compounds, and thus be recognizable to herbivores and their enemies. However, perusal of the major herbivore-induced volatiles shows that the same constituents are released by most plant species, irrespective of their taxonomic affinities. For example, the monoterpenes (E)-β-ocimene and linalool, the sesquiterpenes(E, E)-α-farnesene and (E)-β-caryophyllene, the C11 homoterpene (E)-4,8-dimethyl-1,3,7-nonatriene (DMNT), and the fatty acid derivatives known as green leaf volatiles (GLVs), including (Z)-3-hexen-1-ol and (Z)-3-hexenyl acetate, are frequent components of volatile blends released after herbivore damage from a wide range of plant species. Koradaet al. (2010) Samantaray and Korada (2016) found that sweet potato weevil differently responds to volatiles emitted from different varieties of sweet potato and different plant parts (leaves, flowers, storage roots). Nevertheless, the relative amounts of these substances vary greatly among species and there are typically many differences in less abundant compounds that could contribute to specificity. If these differences are perceived by herbivore enemies, they could facilitate species recognition. Within a single species, plant volatile emission can vary with the herbivore present, as noted many years ago by Dicke and colleagues (Dickeet al., 1993). This variation provides herbivore enemies with valuable information on the identity of prey or hosts available on a plant and their feeding guilds. For example, Brassica rapa (turnip rape) plants damaged by the root herbivore Delia radicum (cabbage rootfly) emit a distinct blend of volatiles from their aboveground tissue that differs significantly from the blend that is released when the plants are attacked aboveground by caterpillars of Pierisbrassicae (large cabbage white butterfly). 4-Methyltridecane and salicylaldehyde are dominant compounds in the blend of D. radicum-damaged plants, whereas methyl salicylate is characteristic for P. brassicae-damaged cabbage. When roots and shoots are attacked simultaneously, the GLV hexyl acetate isreleased in high relative amounts.Despite these impressive examples of specificity in the herbivore-induced emission of plant volatiles, there are several reports in which different herbivore species, feeding guilds, developmental stages and number of attackers were not found to alter volatile emission significantly (Hare 2011; Hare and Sun, 2011; Kessler and Baldwin, 2011).

 

Heribivore induced volatiles above ground

 

            All grasses assayed to date respond to herbivore damage with the emission of a volatile blend consisting mostly of terpenes and products of the lipoxygenase pathway (Degenhardt 2009).The amount and composition of the volatile signal emitted by the plant is dependent on the type of herbivore cue. In Nicotianaattenuata, an Ile conjugate of jasmonic acid is crucial for the induction of nicotine production after herbivore damage to the plant. This conjugate interacts with the factor COI, an F-box protein essential for plant signaling processes (Pascholdet al., 2007). In rice, three herbivore-induced terpene synthases are sufficient to produce the majority of the terpene volatiles. The terpene blends of maize are formed by at least six sesquiterpene synthases. Three of these enzymes,TPS1, TPS10, andTPS23, are strongly induced by herbivore damage and produce the major sesquiterpene components of herbivore-induced volatiles. These terpene synthases can also be induced by jasmonic acid treatment of the plant.

 

The composition and biological activity of volatiles also changes over time after herbivore attack. At the onset of herbivory, the blend is dominated by the green leaf volatiles, (E)-2-hexenal and (Z)-3-hexen-1-ol, while mono- and sesquiterpenes appear about 2 h later. In grasses, the species of attacking herbivore does not seem to affect the composition of the volatiles very much. Only slight differences between the volatile blends were reported in maize attacked by the lepidopteran larvae S. littoralis and Ostrinianubilalis (Turlingset al., 1998), and rice infested with Pseudaletiaseparata and Helicoverpaarmigera (Yan andWang, 2006) possess no distinct differences in their volatile profiles. For some herbivore enemies, however, minor differences between the volatile blends that are undetectable by gas  chromatography can strongly affect host-seeking behavior. Electrophysiological studies indicated that the female SPWs showed a high depolarization of 0.2 mV to a compound emitted from Howrah flower extracts at 11.9 min, whereas the male antenna did not respond to the same extract with the same GC–EAD programme, thus providing evidence that female SPWs could detect specific compounds, even when they are present/emitted in very minute quantities (Koradaet al., 2013a).

 

Herbivore induced volatiles below ground

 

            Despite being covered by soil, roots are also subject to attack by herbivores. Although very little is known about indirect defense mechanisms below ground, it was often assumed that entomopathogenic nematodes are attracted to damaged roots via chemical cues. Recently, such a below-ground defense against arthropods was elucidated in detail. The defense is targeted against larvae of the beetle Diabroticavirgiferavirgifera(western corn rootworm), an important root pest of maize. In response to feeding by D. v. virgifera larvae, maize roots release a signal that strongly attracts the entomopathogenic nematode Heterorhabditismegidis(Rasmannet al., 2005). The attractive signal was identified as (E)-β-caryophyllene. Most North American maize lines do not release (E)-β-caryophyllene from their roots, whereas many European lines and the closest wild relatives of maize, teosinte, do so in response to D. v. virgifera attack. Field experiments showed a 5-fold higher nematode infection rate of D. v.virgifera larvae on a maize variety that produces the signal than on a variety that does not (Rasmannet al., 2005). The (E)-β-caryophyllene signal is produced by the (E)-β-caryophyllene synthase TPS23, which is independently regulated in leaves and roots in response to damage by different herbivores. Above and below ground, the signal is involved in the defense against herbivores with completely different sites and modes of attack. The ability of TPS23 to produce (E)-β-caryophyllene is widely distributed among the wild relatives of maize and was shown to be under positive selection pressure. However, the loss of (E)-β-caryophyllene production in most North American maize varieties is not due to inactive alleles of the TPS23 gene itself, but caused by an alteration of the signal transduction network that abolishes herbivore induced gene transcription (Kollneret al., 2008). (E)-β-caryophyllene diffuses more efficiently through soil than most other sesquiterpenes, making it a rather specific defense signal against soil herbivores (Hiltpold and Turlings, 2008).

 

            Within the same plant or crop, differences in chemical compounds they emit in space, differ between genotypes or varieties Differences in plant volatile expression in C. formicarius resistant and susceptible genotypes of sweet potato were present. A compound, 2-(2-butylcyclopropyl)-cyclopropanenonanoic acid methyl ester eluted from flower headspace volatiles of ‘Howrah’ genotype emitted as 9,12-(Z,Z)-octadecadienoic acid from the storage root periderm. 9,12-(Z,Z)-octadecadienoic acid is a precursor for production of several short-chain aromatic compounds through lipoxygenase (LOX) pathway, and is believed to operate in the storage roots (Koradaet al., 2013a). These compounds playing a role in C. formicarius resistance in ‘Howrah’ and ‘BX 86’ genotypes, were absent in SPW susceptible-genotype ‘Kishan’. Koradaet al. (2013a) proposed that the esters, i.e. cyclopropane fatty acid esters as a ‘diagnostic chemical marker’ to identify sweet potato weevil resistance in genotypes of sweet potato.

 

            Plants and storage roots of three sweet potato varieties, namely, Beaugard, Evangeline and Murasakhi emitted different types of compounds when infested by sweet potato weevil (Korada 2012).  Uninfested sweet potato plants emitted more number of volatile compounds than when the paltns were infested by female sweet potato weevil C. formicarius. Female weevil able to supress emission of trans-2-hexenyl acetate, β-ocimene, para-cymene, 1-methyl naphthalene, 2-hydroxy, phenyl benzoic acid and α-humulene from sweet potato plants. The female weevil also produced two compounds cyperene and geranyl acetate (Korada 2012). A difference between volatile compounds from sweet potato storage roots infested by male and female C. formicariuswas observed (Korada 2012). The number of volatile compounds emitted from female infested storage roots was more than the male infested roots. In case of Beaugard, female produced more no. of compounds than either healthy tubers or male induced tubers. Female weevils exclusively produced sabinene and (E)-2-decenal from roots, whereas they are not found in either healthy tubers or male infested tubers. In case of Evangeline, both male and female infested tubers suppressed some of the compounds those emitted from healthy tubers. There are not much differences in compounds released from either healthy or infested storage roots in case of var. Murasakhi. Murasakhi roots produced entirely a new compound gernanyl acetate and (E)-2-decenal, both are not produced by uninfested tubers (Korada 2012).

 

            Plants and storage roots of three sweet potato varieties, namely, Beaugard, Evangeline and Murasakhi emitted different types of compounds when infested by sweet potato weevil (Korada, 2012).  Uninfested sweet potato plants emitted more number of volatile compounds than when the plants were infested by female sweet potato weevil C. formicarius. Female weevil able to supress emission of trans-2-hexenyl acetate, β-ocimene, para-cymene, 1-methyl naphthalene, 2-hydroxy, phenyl benzoic acid and α-humulene from sweet potato plants. The female weevil also produced two compounds cyperene and geranyl acetate (Korada, 2012). A difference between volatile compounds from sweet potato storage roots infested by male and female C. formicariuswas observed (Korada, 2012).

 

 

 

Plant volatiles in relation to herbivore enemy complex

 

            The blends of volatiles released from damaged plants are frequently specific depending on the type of herbivore and its age, abundance and feeding guild. The sensory perception of plant volatiles by herbivore enemies is also specific, according to the latest evidence from studies of insect olfaction. Thus, enemies do exploit the detailed information provided by plant volatile mixtures in searching for their prey or hosts, but this varies with the diet breadth of the enemy (McCormick et al., 2012). The volatile blends released by grasses in response to herbivory vary greatly in quantity and composition. In a sample of 32 maize lines, release rates from 0.7 to 54.2µg/hr/gm leaf dry weight were observed and suggest that some maize varieties are much more capable of attracting herbivore enemies than others (Degenet al., 2004). The high variation between volatile blends argues against a single volatile signal that is common to grasses. Especially in maize, the variation in volatiles between different genotypes appears too large to be perceived as a specific signal. However, C. marginiventris, like most other parasitic wasps, can associate a successful oviposition experience with the volatiles encountered at that time (Turlingset al., 1990). Therefore, the parasitoid locates its hosts by both innate responses and associative learning of volatiles (Hoballah and Turlings, 2005). This allows the parasitoid to adapt and optimize its host-finding strategy toward the most rewarding plant signals. In field experiments, parasitic wasps even show cross-recognition between different grass species. Intercropping maize with the molasses grass, Melinisminutiflora, significantly increased larval parasitism of stem borers by Cotesiasesamiae and decreased levels of infestation by stem borers in the crop (Khan et al., 1997). This interaction is thought to occur since volatile components released by intact M. minutiflora are similar to those produced by herbivore-damaged maize plants (Khan et al., 1997).

 

Volatile communication among infested plants (priming)

 

            Another feature of the interesting and complex interplay between insects and plants is that plants can detect and react to chemical signals from neighboring plants. Chemical signals from a plant damaged by insect herbivores alert neighbors to prime their defenses so as to respond more strongly to subsequent attack than if they had not been forewarned. Thus, corn seedlings previously exposed to ‘green leaf’ volatiles (6-carbon aldehydes, alcohols, and esters) fromdamaged corn seedlings emitted at least twice the quantity of volatile terpenes when attacked by caterpillars as seedlings that had not been exposed to the ‘alarm’ signals (Engelberthet al. 2004).

 

Interactions between herbivores and plant pathogens/viruses

 

            Plant resistance mechanisms also affect plant quality in future interactions with attackers. Lazebniket al (2014) proposed hypothesis that (i) biotrophic pathogens can facilitate chewing herbivores, unless plants exhibit effector-triggered immunity, but (ii) facilitate or inhibit phloem feeders. (iii) Necrotrophic pathogens, on the other hand, can inhibit both phloem feeders and chewers. They also propose herbivore feeding mode as predictor of effects on pathogens of different trophic strategies, providing evidence for the hypotheses that (iv) phloem feeders inhibit pathogen attack by increasing SA induction, whereas (v) chewing herbivores tend not to affect necrotrophic pathogens, while they may either inhibit or facilitate biotrophic pathogens.

 

            It is well known that insects induce or suppress plant volatile compounds in such a way that they benefit from such plant alteration (Koradaet al 2013b).  Sucking insect pests such as Myzuspersicae and Bemisiatabaci have similar roles in vectoring sweet potato viruses as both insects suppress the same types of volatile compounds (Koradaet al., 2013b).   Volatile emissions from healthy sweet potato plants (var. Beauregard), SPFMV infected plants, and healthy plants infested by two aphid species, M. persicae and Aphis gossypii, and the whitefly Bemisiatabaci were analyzed.  Healthy sweet potato plants (var Beauregard) emitted 22 volatile compounds (Fig.1).  Colony forming aphid M. persicae suppressed 10 volatile compounds (1,2-dimethyl benzene, (E)-2-hexenal, (E)-2-heptenal, (E)-2-decenal, sabinene, para-diethyl benzene, methyl salicylate, α-gurjunene, and trans-caryophyllene, etc.); whereas, A. gossypii, which does not colonize sweet potato, suppressed only 7 compounds.  The whitefly B. tabaci, successfully suppressed the same 9 volatile compounds that M. persicae did, except (E)-2-decenal.  Furthermore, Sweet Potato Feathery Mottle Virus (SPFMV) infected plants (un-infested by any of the test insect) produced two extra volatile compounds, 2-hexenyl acetate and cyperene, which were not seen in healthy plants or vector-induced plants.  Hence, the success and establishment of the SPFMV in sweet potato may be partly attributed to the production of 2-hexenyl acetate and cyperene by SPFMV infected plants (Koradaet al. 2013b).

 

 

Herbivore effectors (suppressor of volatiles)

 

            There has been very limited work on identifying herbivore effectors, although the ability of herbivores to evade host defenses is becoming better appreciated. Insect herbivores produce a cocktail of effectors that can suppress plant defensive pathways, mimic plant hormones, and/or mask the perception of HAMPs. While the labial saliva of several noctuid species has been shown to suppress direct and indirect plant defenses, glucose oxidase (GOX) remains as the one identified salivary constituent contributing to this suppression. This enzyme, produced by the labial and mandibular salivary glands, oxidizes b-D glucose to form gluconic acid and H2O2. Secretion and synthesis of GOX is highly dependent upon the host plant and diet; indicating that the effects of the enzyme on plant defenses is likely to be context-dependent as described for HAMPs. Recent evidence indicates that in addition to suppressing direct defenses such as the induction of nicotine in tobacco, saliva (and perhaps GOX) can suppress the induction of volatile, indirect defenses.

 

Mechanisms of Herbivore-Induced Volatile Production

 

a)     Jasmonic acid triggered immunity (JATI)

            The plant hormone jasmonic acid (JA) exerts direct control over the production of chemical defense compounds that confer resistance to a remarkable spectrum of plant associated organisms, ranging from microbial pathogens to vertebrate herbivores. The underlying mechanism of JA-triggered immunity (JATI) can be conceptualized as a multistage signal transduction cascade involving: i) pattern recognition receptors (PRRs) that couple the perception of danger signals to rapid synthesis of bioactive JA; ii) an evolutionarily conserved JA-signaling module that links fluctuating JA levels to changes in the abundance of transcriptional repressor proteins; and iii) activation (de-repression) of transcription factors that orchestrate the expression of myriad chemical and morphological defense traits. Multiple negative feedback loops act in concert to restrain the duration and amplitude of defense responses, presumably to mitigate potential fitness costs of JATI (Campos et al. 2014).Pattern-triggered immunity (PTI) confers basal resistance and is mediated by cell surface-localized pattern recognition receptors (PRRs) that bind conserved foreign molecules, known collectively as microbial/pathogen-associated molecular patterns (MAMPs). A second layer of induced resistance, referred to as effector-triggered immunity (ETI), relies on polymorphic intracellular resistance (R) proteins to detect effector molecules that plant attackers deliver into host cells to counteract defense.

 

            In addition to cell surveillance systems that recognize foreign threats in the form of MAMPs/HAMPs and effectors, it has long been known that plant-derived (i.e., self) signalsalso are potent elicitors of local and systemic defense responses(Mousavi et al. 2013). These endogenous elicitors are produced in response to general cellular injury and may be classified as damage-associated molecular patterns (DAMPs). Because DAMPs are generated in response to diverse types of tissue injury, their role in cellular recognition of pathogen attack traditionally has been ignored. However, the recent identification of DAMP receptors and associated signal transduction components (Choi et al. 2014; Mousavi et al. 2013) is shaping a broader view of how plant cells perceive and respond to injurious threats. There is alsoevidence to indicate that PTI and ETI converge on similar downstream signaling components, including MAP kinase pathways, ROS production, and calcium-dependent signaling events (Romeis and Herde 2014).

 

            The central role of JA as an activating signal for induced immunity is grounded in three general observations. First, biotic attack and other forms of tissue injury result in the rapid synthesis of JA and its receptor-active derivative, jasmonoyl-L-isoleucine (JA-Ile). Stress-induced accumulation of JA-Ile occurs in both above- and below-ground tissues and, depending on the eliciting signal and tissue type, is a systemic response (Mousavi et al. 2013). Second, JA promotes the expression of virtually all major classes of secondary metabolites and proteins that have established roles in defense, including alkaloids, terpenoids, phenylpropanoids, amino acid derivatives, anti-nutritional proteins, and some pathogenesis-related (PR)proteins (DeVleesschauweret al. 2013). The JA pathway also promotes the development of morphological structures, including glandular trichomes, resin ducts, and nectaries that produce a rich variety of compounds serving direct and indirect roles in defense.

 

b)     Ca2 signaling, ROS and MAPKs

 

            JA synthesis is initiated in the plastid by stress-induced activation of lipases that release fatty acid precursors of JA (Wasternack and Hause 2013). Among the intracellular signals implicated in this process are calcium ions, reactive oxygen species (ROS), and mitogen-activated protein (MAP) kinase cascades.Calcium ions have long been recognized as ubiquitous second messengers in signal transduction pathways. The involvement of Ca2 in JATI is supported by studies showing that cytosolic Ca2 levels increase in response to herbivore feeding and treatment with exogenous MAMP/HAMP/DAMPs. Changes in membrane polarization caused by wounding and insect attack also increase the level of cytosolic Ca2 (Maffeiet al. 2006). Ca2 fluxes and associated Ca2 -binding proteins, including calmodulin and Ca2 -dependent protein kinases (CDPKs), exert control during the activation of JA-response genes (Romeis and Herde 2014; Yang et al. 2012a). Dynamic changes in cytosolic Ca2 levels during plant-attacker interactions are linked to the production of ROS, including hydrogen peroxide (Arimura and Maffei 2010). Studies in Arabidopsis, for example, show that a signal generated at the site of leaf injury travels rapidly (2–3 cm/min) to trigger JA-Ile synthesis and associated JA responses in undamaged leaves.

 

c)     Manipulation of JATI by herbivores

An important emerging paradigm in plant-herbivore interactions is the ability of herbivores to activate the SA pathway and thereby reduce the effectiveness of JATI as a basal defense(Hogenhout and Bos 2011). For example, phloem feeding by silverleaf whitefly (Bemisiatabaci) results in increased expression of SA-related defense genes and concomitant repression of JATI (Zhang et al.2013).

 

Conclusion

 

            The blends of volatiles released from damaged plants are frequently specific depending on the type of herbivore and its age, abundance and feeding guild. The sensory perception of plant volatiles by herbivore enemies is also specific, according to the latest evidence from studies of insect olfaction. Thus, enemies do exploit the detailed information provided by plant volatile mixtures in searching for their prey or hosts, but this varies with the diet breadth of the enemy. Chemical signals from a plant damaged by insect herbivores alert neighbors to prime their defenses so as to respond more strongly to subsequent attack than if they had not been forewarned.

 

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Source: OUAT Souvenir