Emerging role of roots in plant responses to aboveground insect herbivory

Insect Science (2013) 20, 286–296, DOI 10.1111/1744-7917.12004

INVITED REVIEW

Emerging role of roots in plant responses to abovegroundinsect herbivory

Vamsi J. Nalam1, Jyoti Shah2 and Punya Nachappa1

1Department of Biology, Indiana University-Purdue University, Fort Wayne, Indiana and 2Department of Biological Sciences and Center

for Plant Lipid Research, University of North Texas, Denton, Texas, United States

Abstract Plants have evolved complex biochemical mechanisms to counter threats frominsect herbivory. Recent research has revealed an important role of roots in plant responsesto above ground herbivory (AGH). The involvement of roots is integral to plant resistanceand tolerance mechanisms. Roots not only play an active role in plant defenses by actingas sites for biosynthesis of various toxins and but also contribute to tolerance by storingphotoassimilates to enable future regrowth. The interaction of roots with beneficial soil-borne microorganisms also influences the outcome of the interaction between plant andinsect herbivores. Shoot-to-root communication signals are critical for plant response toAGH. A better understanding of the role of roots in plant response to AGH is essential inorder to develop a comprehensive picture of plant-insect interactions. Here, we summarizethe current status of research on the role of roots in plant response to AGH and also discusspossible signals involved in shoot-to-root communication.

Key words jasmonic acid, secondary metabolites, shoot-to-root communication, soil-borne microorganisms

Introduction

Current understanding of plant–insect interactions isdrawn largely from the response of plant foliar tissue toinsect herbivory (Howe & Jander, 2008; Wu & Baldwin,2010). Plants combat insect feeding using both constitu-tive defenses and defenses that are induced only in re-sponse to attack (Karban & Baldwin, 1997). Inducibledefenses can be classified as either direct or indirect. Di-rect defenses affect the biology of the attacker directly,whereas indirect defenses, which are more relevant in de-fense against herbivores, affect the herbivore by attractingits natural enemies (Karban & Baldwin, 1997). Inducibledefenses offer several advantages compared to constitu-tive defenses, such as reduced cost and increased vari-

Correspondence: Punya Nachappa, Department of Biol-ogy, Indiana University-Purdue University, Fort Wayne, Indiana46805, USA. email: [email protected]

ability in the plant phenotype, resulting in increased effi-ciency of the inducible defense (Karban & Baldwin, 1997;Zangerl, 2002; Cipollini et al., 2003). Given that all planttissues (leaves, roots, stems, flowers, and fruits) are con-sumed by insect herbivores, our understanding of plant–insect interactions is skewed. In several plant species, thebiomass of roots is far greater than that of the shoots;hence, roots provide an incredibly attractive resource tovarious soil-dwelling insect pests. And indeed, herbivoryof roots by belowground herbivores (BGH) results in sub-stantial damage to plant roots and significantly impactsoverall plant fitness (Blossey & Hunt-Joshi, 2003). Stud-ies examining plant responses to BGH have revealed thatsimilar to aboveground responses, roots also employ di-rect and indirect induced defenses (Rasmann & Agrawal,2008; van Dam, 2009; Erb et al., 2012). The activationof defenses due to insect herbivory either belowgroundor aboveground often results in the induction of defensessystemically throughout the plant. Systemic defenses canthereby influence the outcome of not only plant–insect

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Root responses to aboveground herbivory 287

interactions but also link the belowground and above-ground biota (reviewed in Bezemer & van Dam, 2005;Johnson et al., 2008).

In terrestrial plants, roots serve many different purposesincluding, absorption of water and nutrients, anchoringthe plant to soil, and storage of photoassimilates (Opiket al., 2005). Roots are also increasingly being recog-nized as active participants in plant responses to AGH(Erb, 2012). The earliest report that root-derived sec-ondary metabolites are involved in plant defenses againstaboveground herbivores (AGH) was made as early as 1941when it was shown that the alkaloid nicotine was primarilysynthesized in the roots of tobacco plants (Dawson, 1941).Of late, there has been a surge of interest in elucidatingthe contribution of roots in shoot defenses against insectherbivores (Kaplan et al., 2008b; Rasmann & Agrawal,2008; Erb et al., 2009b; Erb et al., 2012). For example, arecent study shows that root-derived oxylipins contributeto host susceptibility by promoting population growth rateof an aboveground insect herbivore. Feeding by the gen-eralist aphid (Myzus persicae) resulted in the inductionof expression of a 9-lipoxygenase encoding LIPOXYGE-NASE5 (LOX5) gene and a corresponding increase inthe LOX5-synthesized oxylipins, 9-hydroperoxy, and 9-hydroxy-fatty acids only in the roots of aphid-infestedArabidopsis plants. These oxylipins were translocated tothe shoot, where they promoted aphid feeding, body watercontent and fecundity (Nalam et al., 2012). Studies such asthese and others highlight the need to include roots to de-velop a better understanding of plant–insect interactions.In this review, we will focus on recent advances in un-derstanding (i) the contribution of roots to plant defensesagainst AGH and (ii) the identity of potential signal(s)involved in integrating shoot and root responses to AGH.

Contribution of roots to defense against AGH

Root-derived defenses

Plants synthesize a variety of secondary metabolites towithstand insect attack. While some of these secondarymetabolites are toxic to the herbivore, others reducethe palatability of the plant to the insect. Alkaloids andterpenoids, which are among the most metabolically di-verse classes of secondary metabolites, represent a majorclass of insecticidal metabolites (Facchini, 2001; Aharoniet al., 2006; Ziegler & Facchini, 2008). Others includeglucosinolates, saponins, tannins, furanocoumarins, andcyanogenic glycosides (Wu & Baldwin, 2010; Yamaneet al., 2010). In addition to secondary metabolites, abroad array of proteins that are induced in response to

herbivory are also involved in plant defense responses(Zhu-Salzman & Liu, 2011). The elucidation of thebiosynthetic pathways for some of these metabolites andinduced proteins highlight roots as an important site ofsynthesis (Table 1; reviewed in van der Putten et al.,2001; Rasmann & Agrawal, 2008; Erb et al., 2009b; Erb,2012).

The most well studied insecticidal secondary metaboliteis nicotine, a neuroactive compound synthesized in largeamounts by plants of the genus Nicotiana. Nicotine is syn-thesized in roots from where it is translocated to shootsand stored in vacuoles of leaf cells, thus providing a con-stitutive defense against insects (Dawson, 1941; Moritaet al., 2009). In response to herbivory or methyl jasmonatetreatment, the accumulation of nicotine increased in rootsand lead to increased concentrations in shoots and thusenhanced protection against insect herbivory (Baldwinet al., 1994). The synthesis of alkaloids in roots is notlimited to plants of the genus Nicotiana. A similar patternis observed for the synthesis of tropane alkaloids that maybe involved in leaf defense in the Solanaceae family ofplants (Ziegler & Facchini, 2008).

In some instances, the precursors for secondary metabo-lites that participate in shoot defense are synthesizedin roots and then transported to shoots where they un-dergo further modifications. For example, the precursorfor pyrrolizidine alkaloids, senecionine N-oxide is pro-duced in the roots and then translocated throughout theplant tissue (Toppel et al., 1987; Hartmann & Ober, 2000).A second example is umelliferone, which is synthesizedin significant quantities in roots of the bishopweed (Ammimajus) (Sidwa-Gorycka et al., 2003). Umelliferone is theprecursor for several furanocoumarins that act as feedingdeterrents for insects and have antifungal and antibacterialproperties (Berenbaum, 1978; Yamane et al., 2010).

Another class of compounds, the glucosinolates foundmainly in plants belonging to Brassicaceae, function indefense against herbivores and pathogens. In black mus-tard (Brassica nigra), foliar herbivory by the larvae ofcabbage butterfly (Pieris brassicae) resulted in the ac-cumulation of higher levels of indole glucosinolates inthe roots (Soler et al., 2009). An increase in the levelsof indole glucosinolates was also observed in roots offield mustard (Brassica campestris), when shoots weretreated with the defense elicitors salicylic acid (SA) andjasmonic acid (JA; Ludwig-Muller et al., 1997). However,since glucosinolates can be readily loaded and transportedthrough the phloem (Chen et al., 2001), it is as yet unclearwhether these compounds are synthesized exclusively inthe roots or whether they are synthesized in infested shootsand then transported systemically throughout the plant in-cluding the root.

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288 V. J. Nalam et al.

Table 1 Insecticidal factors synthesized in roots in response to AGH.

Increase/ InfluencePlant Induction by Altered root defense decrease of on Reference

root defense AGH

Brassica nigra Pieris brassicae Indole glucosinolates Increase Yes Soler et al., 2009Zea mays Spodoptera frugiperda Mir1-CP Increase Yes Lopez et al., 2007Arabidopsis thaliana Myzus persicae 9-LOX derived oxylipins Increase Yes Nalam et al., 2012Senecio jacobea Mamestra brassicae Pyrrolizidone alkaloid Decrease Yes Hol et al., 2004Gossypium herbaceum Spodoptera exigua Terpenoid aldehydes Decrease NA Bezemer et al., 2004Brassica campestris JA, SA Indole glucosinolates Increase NA Ludwig-Muller et al.,

1997Abelmoschus esculentus SA PR proteins Increase NA Nandi et al., 2003Nicotiana attenuata MJ, MD Trypsin proteinase

inhibitorsIncrease NA van Dam et al., 2001

Nicotiana sylvestris MD Nicotine Increase NA Baldwin et al., 1994Cynoglossum offininale MD Pyrrolizidone alkaloid Increase NA van Dam & Vrieling,

1994Secale cereale MD Hydroxamic acids Increase NA Collantes et al., 1999

MD, mechanical damage; MJ, methyl jasmonate; SA, salicylic acid; JA, jasmonic acid; PR, pathogenesis proteins; NA, not applicable.

Arthropod-inducible proteins (AIPs) also provide abroad spectrum of resistance in several plant species byproviding postingesting plant defenses (Zhu-Salzman &Liu, 2011). In the case of one such AIP, the levels of Maizeinsect resistance 1-cysteine protease (Mir1-CP) increasedin the leaf tissue of a resistant maize (Zea mays) geno-type (Mp708) in response to foliar herbivory by the larvaeof fall armyworm (Spodoptera frugiperda) (Lopez et al.,2007). Mir1-CP accumulated in root xylem tissue 24 hafter foliar feeding and was also found in the xylem tissueof leaves. Furthermore, removal of roots prior to larvalfeeding prevented the accumulation of Mir1-Cp in leaves,suggesting that the protein is first synthesized in the rootsand transported to the leaf tissue through the vasculature.

The synthesis of defensive factors by roots in responseto foliar herbivory is not a universal phenomenon. In cer-tain instances, there is a reduction in the levels of planttoxins that are normally synthesized in roots. For exam-ple, the levels of pyrrolizide alkaloids, which are pro-duced in roots (Toppel et al., 1987) decreased in the rootsof ragwort (Senecio jacobea) in response to AGH by thecabbage moth (Mamestra brassicae) (Hol et al., 2004).In other cases, defensive compounds normally induced inroots in response to BGH are not induced during AGH. Forinstance, belowground herbivory by wireworms (Agrioteslineatus) resulted in increased accumulation of terpenoidsin both roots and shoots. However, a similar increase interpenoid content was observed only in shoots duringaboveground herbivory by beet armyworm (Spodopteraexigua) (Bezemer et al., 2003, 2004). This observation

suggests that although BGH may change the level anddistribution of defensive secondary metabolites, the samemay not hold true for all cases of AGH. One possibil-ity to explain the suppression of root-induced defense inthese cases is that herbivores themselves manipulate hostresponses to suit their needs by either suppressing hostdefenses or activating alternate mechanisms that promotethe AGH.

Roots limit resource availability to AGH

A major function of plant roots in many species isthe storage of food and nutrients. Roots can potentiallycontribute to the plants ability to tolerate AGH by act-ing as storage sites for photoassimilates. For instance,in response to AGH, photoassimilates are translocated tothe roots making them inaccessible to the herbivore. Thereallocation of stored photoassimilates aboveground canthen occur after AGH pressure has reduced, thus enablingaboveground growth and reproduction to resume. Thereare several lines of evidence that indicate that foliar her-bivory, shoot hormone applications or mechanical dam-age can result in reallocation to storage tissue (reviewedin Orians et al., 2011). In maize for instance, foliar in-sect herbivory by grasshoppers resulted in the mobiliza-tion of photoassimilates to roots (Holland et al., 1996). Asimilar process occurs in Nicotiana tabaccum after AGHby tobacco hornworm (Manduca sexta) larvae (Kaplanet al., 2008a). In Populus, treatment of the shoot with thedefense hormone JA or AGH by Gypsy moth (Lymantria



dispar) larvae resulted in the increased transport of leafphotosynthate to the stems and roots within hours of treat-ment (Babst et al., 2005; Babst et al., 2008). In tomato(Solanum lycopersicum), AGH by tobacco hornworm(M. sexta) resulted in a significant increase in the con-centrations of various sugars, sugar alcohols and organicacids in the roots (Steinbrenner et al., 2011).

To achieve an increase in the transport of photosynthateto the roots, plants can either increase loading into phloemand/or increase unloading into the roots (Turgeon & Wolf,2009). The increased carbon sink strength of the roots canbe achieved in part by an increase in the activity of in-vertases, a sugar-cleaving enzyme (Roitsch & Gonzalez,2004). Indeed, an increase in invertase activity was foundin roots in response to AGH by the tobacco hornworm(Kaplan et al., 2008a). Insect-derived elicitors present inthe regurgitant of chewing insects are also capable of in-ducing resource reallocation to roots (Schwachtje et al.,2006). The application of M. sexta regurgitant to leavesof tomato plants resulted in increased allocation of car-bon to the roots (Gomez et al., 2012). This herbivore-induced resource-reallocation is thought to be regulatedby SNF1-related kinases, which play a central role in cellenergy metabolism (Halford & Hey, 2009). In Nicotianaattenuata, the transcript levels of SNF1-related kinaseswere rapidly downregulated in leaves treated with insect-derived elicitors resulting in increased assimilates trans-ported to roots (Schwachtje et al., 2006). Although theregulatory mechanisms that initiate and control realloca-tion are not fully understood (Erb et al., 2009a; Erb, 2012),it is clear that roots play an active role in limiting resourceavailability to AGH.

Interaction of roots with beneficial soil-microbesinfluences AGH

The interaction of roots with beneficial soil-borne mi-crobes also influences the outcome of the abovegroundinteractions between the plant and herbivore. The asso-ciation of roots with certain plant growth-promoting rhi-zobacteria and mycorrhizal fungi not only results in thepromotion of plant growth but also the induction of resis-tance against a wide variety of AGH and pathogens. Thisphenomenon termed induced systemic resistance (ISR)provides protection against a wide range of diseases (vanOosten et al., 2008; Doornbos et al., 2010). Although, sev-eral different beneficial soil-borne microorganisms caninduce ISR, the mechanism of induction of ISR followssimilar patterns and is mediated by JA or jasmonic ethy-lene (ET) sensitive pathways which are commonly in-volved in plant defense responses (van Oosten et al.,2008; Doornbos et al., 2010). Beneficial soil-borne mi-

croorganisms can therefore indirectly influence with out-come of plant interaction with an AGH via plant-mediatedmechanisms. There are examples of both positive andnegative effects of such interactions (reviewed in Pinedaet al., 2010). For instance, the association of Acremo-nium alternatum Gams (Ascomycotina), an endophyticfungus with the roots of cabbage (Brassica oleracea) re-sulted in increased mortality and reduced growth rate ofthe surviving larvae of the diamond back moth (Plutellaxylostella) (Raps & Vidal, 1998). The association of aplant-growth promoting rhizobacteria, Bacillus amylo-quefaciens, with tomato or sweet pepper (Capsicum an-nuum) roots conferred protection against phloem-feedinginsects, the green peach aphid (M. persicae) and silver-leaf whiteflies (Bemisia argentifolii) (Murphy et al., 2000;Herman et al., 2008). In these cases it is plausible that rootassociation with the beneficial soil-microbes resulted inthe activation of ISR. In a more recent study, the roleof ISR was demonstrated in the association of Bacil-lus subtillis with the roots of tomato plants, which re-tarded silverleaf whitefly development (Valenzuela-Sotoet al., 2010). By comparison, the association of Rhizobiumleguminosarum with white clover (Trifolium repens) re-sulted in a positive effect on the Egyptian cotton leafworm(Spodoptera littoralis) and a neutral effect on the greenpeach aphid (Kempel et al., 2009). The species or thestrain of the beneficial soil-borne microorganisms alsoimpacts the outcome of plant interaction with a specificAGH. For instance, in rice (Oryza sativa) a combination ofdifferent Pseudomonas fluorescens strains had a strongerimpact as compared to the influence of the strains indi-vidually (Saravanakumar et al., 2007).

The impact of root-colonizing microbes on AGH canalso be influenced by the degree of specialization of theherbivore. Studies on Arabidopsis show that association ofroots with P. fluorescens results in the activation of JA/ETresponsive defense pathways which do not affect feed-ing by the specialist caterpillar, Pieris rapae. By contrast,activation of the same plant defenses negatively affectedfeeding by the generalist herbivore S. exigua (van Oostenet al., 2008). Another factor that determines the effec-tiveness of root-colonizing microbe induced defenses isthe insect feeding guilds. Chewing insects encounter sev-eral secondary metabolites when they feed on plant tissue.Piercing-sucking insects on the other hand avoid contactwith these compounds by inserting their slender needlelike stylets into the phloem sieve elements. Therefore, thedegree of specialization and the feeding guild should betaken into account while considering the impact of bene-ficial soil-microbes on the aboveground herbivore.

In order to recruit beneficial soil-dwelling organisms,plant roots produce copious amounts of exudates. The



production of root exudates can therefore indirectly im-pact the outcome of plant interaction with the AGH. Rootexudates comprise of an enormous range of small molec-ular weight compounds and the interactions mediated bythese exudates can be either positive or negative (reviewedin Walker et al., 2003; Bais et al., 2006; Hiltpold et al.,2011). For instance, a large number of soil organisms relyon root exudates as a major source of carbon (Walkeret al., 2003; Bais et al., 2006). On the other hand, rootexudates also contain compounds with antimicrobial, ne-maticidal, or insecticidal properties. Several studies haveshown that AGH influence soil microbial communities(Hamilton et al., 2008; van Dam, 2009). For example, sil-verleaf whitefly and green peach aphid feeding on pepperplants resulted in a significant increase in population den-sity of several beneficial rhizobacteria (Yang et al., 2011;Lee et al., 2012). Whether root association with theserhizobacteria results in ISR against the phloem-feedinginsects is unknown. It is however plausible to concludefrom these and other studies (Murphy et al., 2000; Hermanet al., 2008) that recruitment of beneficial rhizobacteriacan have a negative impact on the AGH. These studiesprovide new insights into the tritrophic interactions be-tween the AGH, the plant, and beneficial soil microbes.Herbivory induced root exudation can also result in uniquesoil legacy effects. For instance, AGH by M. brassicae onragwort plants resulted in the production of root exudatesthat altered the composition of soil fungi. Plants grownsubsequently in the same soil displayed increased biomassand higher content of pyrrolizidine alkaloids that enabledthem to counter future threats by AGH (Kostenko et al.,2012).

Roots are also involved in interplant communicationvia the interaction with the mycelia of mycorrhizal fungi.Mycorrhizal mycelia can interconnect roots of multipleplants to form common mycorrhizal netwroks (CMNs;Selosse et al., 2006). CMNs are known to act as conduitsfor the transfer of water and also nutrients such as ni-trogen, phosphorous and other elements from one plantroot to another (He et al., 2003; Meding & Zasoski, 2008;Mikkelsen et al., 2008). Exchange between plants con-nected by CMNs is not only limited to transfer of waterand nutrients but also to the exchange of signals. For in-stance, CMNs mediate plant to plant communication be-tween healthy and pathogen-infected tomato plants (Songet al., 2010). Pathogen-infected tomato plants transmita defence signal to healthy plants where the expressionof defence genes and activity is induced resulting in in-creased resistance to future attacks (Song et al., 2010).Although, a similar study with insects is lacking it is plau-sible to hypothesize that a similar exchange of defence sig-nals between plants connected physically by CMNs also

occurs during insect herbivory. The interaction of plantroots with mycorrhiza forming CMNs could therefore actas defence networks in plant communities.

Root-colonizing microbes also contribute to indirect de-fenses against AGH by stimulating shoots to emit volatileorganic compounds that attract natural enemies of AGH(Guerrieri et al., 2004). For instance, the rate of parasitismof the Bird cherry oat aphid, Rhopalosiphum padi, by theparasitic wasp, Aphidius rhopalosiphi, increased by 140%on timothy grass (Phleum pratense) that were associatedwith arbuscular mycorrhizal fungi (Glomus intraradices)(Hempel et al., 2009). Additionally, belowground inter-action of plants with root-colonizing microbes not onlypromotes plant growth but also has a beneficial effect onthe nutritional status of the plant (Pineda et al., 2010).Root associations with soil-dwelling microbes enable theincreased uptake of not only water but also a variety of nu-trients such as nitrogen and phosphorus. Further, some mi-crobes enhanced photosynthesis by modulating sugar andABA signaling, and also synthesized plant growth pro-moting hormones (van Loon, 2007; Zhang et al., 2008).In general, increased content of nitrogen and other limit-ing nutrients in plant tissues and phloem sap benefits bothchewing and phloem-sap feeding insects (Schoonhovenet al., 2005). The final result of root-colonizing microbeson AGH, therefore, depends on a fine balance between thepositive effect on AGH due to enhanced nutritional statusof the plant and negative effect on AGH due to promotionof induced resistance and indirect defenses in shoots.

Signal(s) involved in shoot-to-root communication

The involvement of roots in defense against AGH sug-gests communication by shoots with roots. Erb et al.(2009b) suggested the presence of a shoot–root–shootloop in which signal(s) generated in response to AGHspread systemically throughout the plant including theroots. The translocation of the signal(s) to the roots re-sults in the activation of root-based defenses, which thendirectly or indirectly influence the AGH. Several classesof compounds have the potential to act as signals. In orderto qualify as a defense signal however, the compound(s)must be synthesized at the site of attack, from where it issystemically translocated to induce defense responses.

Plant hormones such as JA and SA are critical signalsin plant defense regulatory networks that are involvedin long-distance signaling (Heil & Ton, 2008) and maytherefore play a critical role in shoot-to-root communi-cation. JA and associated compounds termed jasmonatesare involved in long-distance wound signaling and areconsidered to be central to governing plant responses tochewing insects (Wu & Baldwin, 2010; Woldemariam



et al., 2011). Furthermore, methyl jasmonate is readilytransported through the plants vasculature (Thorpe et al.,2007). Support for the role of jasmonates as shoot-to-root signals comes from studies on diverse plant–insectinteractions. In Nicotiana sylvestris, JA concentrations in-creased locally within 30 min of wounding and in the rootsafter 90 min resulting in the stimulation of nicotine synthe-sis (Baldwin et al., 1994; Winz & Baldwin, 2001). Foliartreatment of N. sylvestris with methyl jasmonate resultedin the upregulation of Putrescine N-methyltransferases,the enzymes that catalyze the first committed step of nico-tine biosynthesis (Shoji et al., 2000). In poplar, simulatedherbivory by the application of methyl jasmonate, or me-chanical wounding, also resulted in the induction of apoplar trypsin inhibitor (PtdT13), a marker for poplar de-fenses, in both the leaves and roots (Major & Constabel,2007). In Brassica rapa, foliar application of methyl jas-monate resulted in an increase in glucosinolate levels inthe roots (Loivamaki et al., 2004). Furthermore, methyljasmonate treatment resulted in the accumulation of Mir1-CP in maize leaves in a dose-dependent manner (Ankalaet al., 2009). Since Mir1-CP is synthesized exclusivelyin the roots of maize plants, it is plausible that JA or itsconjugates function as long-distance signals to stimulateMir1-CP synthesis. Taken together, these results highlightthe importance of jasmonates as important shoot-to-rootsignals during AGH by chewing insects.

The role of SA and its derivative methyl salicylate inshoot-to-root communication is less clear. SA-mediateddefenses play an important role in locally expressed de-fenses and in the enhancement of resistance to secondaryinfection in distal uninfected plant parts against biotrophicpathogens. The crosstalk between the SA and JA pathwaysis thought to modulate plant defense responses and limitthe expression of costly and ineffective defenses (Glaze-brook, 2005). Although, SA-based defenses are normallyinduced in response to pathogen attack, insect herbivorycan also result in an increase in the levels of endogenousSA and/or the activation of SA-inducible genes (Moran &Thompson, 2001; Heidel & Baldwin, 2004; Zarate et al.,2007; Kanno et al., 2012). However, the lack of a negativeeffect on herbivore performance due to the activation ofSA-mediated defenses (Moran & Thompson, 2001; Hei-del & Baldwin, 2004; Zarate et al., 2007; Kanno et al.,2012) raises the possibility of herbivore-mediated manip-ulation of plant defenses. Indeed, nymphs of silverleafwhitefly induce SA-mediated defenses in order to sup-press the more effective JA-mediated defenses (Zarateet al., 2007). However, the role of methyl salicylate as asignal molecule cannot be overlooked. Methyl salicylatein addition to being readily transported in the phloem isalso volatile and is a key signaling molecule involved in

plant-to-plant communication (Shulaev et al., 1997; Parket al., 2007). Furthermore, methyl salicylate mediates re-sistance against certain insects by attracting their respec-tive predators (van Poecke & Dicke, 2002). Therefore,although SA and methyl salicylate may not be directlyinvolved in shoot-to-root communication, they can indi-rectly influence the plants response to insect herbivory bymodulating JA-mediated defenses.

There may be yet undiscovered molecules that are in-volved in shoot-to-root communication. In maize plantsinfested with African cotton leafworm (S. littoralis), tran-scriptomic analyses revealed no overlap between the genesinduced in the shoots and the roots. Furthermore, althoughJA and SA-mediated genes were induced in shoots in re-sponse to the AGH, the same set of genes were not inducedin the roots during AGH suggesting the presence of alter-native shoot-to-root signals (Erb dissertation, Universityof Neuchatel, 2009). In plants, small interfering RNA andmicro RNA play an important role in plant defense re-sponses to AGH (reviewed in Padmanabhan et al., 2009).For example, herbivory induced large-scale changes in thesmall RNA transcriptome of N. attenuata (Pandey et al.,2008). These small RNAs are thought to contribute toplant defenses by playing a central role in coordinatingthe large-scale transcriptional changes that occur in re-sponse to AGH. However, small RNAs are highly mobileand are readily transported in the phloem tissue and thusmay have an important role in the regulation of systemicdefenses (Yoo et al., 2004; Kehr & Buhtz, 2008). Furtherexperimentation is however needed to confirm whethersmall RNAs play a role in shoot-to-root communicationduring AGH. The ability to simply and efficiently mi-crograft/graft various model species such as Arabidopsis,N. attenuata, Nicotiana benthamiana, and tomato (Voin-net et al., 2000; Turnbull et al., 2002; Kimura & Sinha,2008; Fragoso et al., 2011), can greatly aid in evaluatingthe role of small RNAs and other candidates as potentialshoot to root signals. In addition to plant-derived factorsacting as shoot-to-root signals during AGH, insect elici-tors may also function as signal molecules. Both chewingand piercing/sucking insects release a large repertoire ofelicitors that are capable of inducing characteristic plantdefense responses (Wu & Baldwin, 2009; Hogenhout &Bos, 2011). Insect elicitors have been identified in oral se-cretions, regurgitant, oviposition liquid, and saliva. Insectelicitors are not only capable of inducing JA, ethylene,and SA signaling but can also activate mitogen-activatedprotein kinases, produce reactive oxygen species and in-duce calcium ion fluxes (Wu & Baldwin, 2009). However,whether insect elicitors function as shoot-to-root signalsdirectly or indirectly through plant-mediated mechanismswarrants further research.



Conclusions

Roots are play an integral role in plant defense againstAGH by acting as sites of synthesis for various secondarymetabolites and proteins that either kill or deter the herbi-vore from feeding. Roots also contribute to plant defensesindirectly by acting as temporary sites of storage for pho-toassimilates. Furthermore, the association of roots withbeneficial soil-borne microorganisms not only aids in thegrowth and development of the plant, but also results inthe induction of ISR and aids in the recruitment of natu-ral enemies of insect herbivores. There is increasing evi-dence that plant signaling molecules such as JA and/or itsderivatives, play an important role in shoot-to-root com-munication. There are several questions that are yet to beanswered. For example, does the root response to AGHdepend on the insect feeding guilds? Are the signal(s)involved in shoot-to-root communication derived fromthe plant and/or the insect? Do other phytohormones be-sides JA play a role in shoot-to-root communication? DoesAGH alter root physiology to suppress host defenses?What is the metabolic cost to the plants due to root in-volvement in AGH defense? Answers to these and otherrelevant questions will provide a better understanding ofthe contribution of roots to plant defense against AGH.

Acknowledgments

We thank Dr. Keyan Zhu-Salzman for the invitation tocontribute to this special issue. We would like to thank Dr.David C. Margolies for helpful comments on an earlierversion of this manuscript. Work in the Shah lab was sup-ported by grants from the National Science Foundation(Division of Integrative Organismal Systems-0919192and Division of Molecular and Cellular Biosciences-0920600). This work was supported by start-up fundsfrom Indiana University – Purdue University Fort Wayneto Dr. Punya Nachappa.

Disclosure

The views presented in the review article represent theauthor’s views. The authors have declared no competinginterests exist and are not involved in any potential con-flicts of interest including financial interests, relationshipsand affiliations.

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Accepted November 7, 2012


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Emerging role of roots in plant responses to aboveground insect herbivory