Annals of Botany 119: 791–801, 2017

doi:10.1093/aob/mcw263, available online at www.aob.oxfordjournals.org

REVIEW: PART OF A SPECIAL ISSUE ON PLANT IMMUNITY

Terpenoids in plant and arbuscular mycorrhiza-reinforced defence against

herbivorous insects
Esha Sharma, Garima Anand and Rupam Kapoor*
Department of Botany, University of Delhi, Delhi 110007, India
*For correspondence. E-mail kapoor_rupam@yahoo.com

Received: 29 July 2016 Returned for revision: 24 October 2016 Editorial decision: 22 November 2016 Published electronically: 12 January 2017

 Background Plants, though sessile, employ various strategies to defend themselves against herbivorous insects
and convey signals of an impending herbivore attack to other plant(s). Strategies include the production of volatiles
that include terpenoids and the formation of symbiotic associations with fungi, such as arbuscular mycorrhiza
(AM). This constitutes a two-pronged above-ground/below-ground attack–defence strategy against insect
herbivores.
 Scope Terpenoids represent an important constituent of herbivore-induced plant volatiles that deter herbivores
and/or attract their predators. Terpenoids serve as airborne signals that can induce defence responses in systemic
undamaged parts of the plant and also prime defence responses in neighbouring plants. Colonization of roots by
AM fungi is known to influence secondary metabolism in plants; this includes alteration of the concentration and
composition of terpenoids, which can boost both direct and indirect plant defence against herbivorous insects.
Enhanced nutrient uptake facilitated by AM, changes in plant morphology and physiology and increased transcrip-
tion levels of certain genes involved in the terpenoid biosynthesis pathway result in alterations in plant terpenoid
profiles. The common mycorrhizal networks of external hyphae have added a dimension to the two-pronged plant
defence strategy. These act as conduits to transfer defence signals and terpenoids.
 Conclusion Improved understanding of the roles of terpenoids in plant and AM defences against herbivory and of
interplant signalling in natural communities has significant implications for sustainable management of pests in ag-
ricultural ecosystems.

Key words: Terpenoids, herbivorous insects, indirect defence, induced defence, priming, arbuscular mycorrhiza,
common mycorrhizal networks.

INTRODUCTION
(GLVs), serve as airborne signals that can be perceived by
Terpenoids represent the largest and structurally the most di- undamaged systemic parts of the same plant (Frost et al., 2007;
verse group of volatiles released by plants. Biologically, a wide Heil and Silva Bueno, 2007) and by neighbours (Karban et al.,
array of terpenoids can enable plants to interact with other or- 2000). In response to perceived volatile signals, plants express
ganisms, such as insects, pathogens and neighbouring plants defence genes and synthesize secondary metabolites (Shulaev
(Kant et al., 2004; Mercke et al., 2004; Kappers et al., 2005; et al., 1997; Arimura et al., 2000b; Sugimoto et al., 2014) or
Cheng et al., 2007a, b). Terpenoids are emitted either constitu- prime their defences against pests (Engelberth et al., 2004; Heil
tively or induced in response to biotic (Dudareva et al., 2006, and Kost, 2006; Ton et al., 2006). Although primed plants do
2013; Unsicker et al., 2009; Rasmann et al., 2012) and abiotic not show any trait of resistance, they become prepared to re-
(Gouinguené and Turlings, 2002; Loreto and Schnitzler, 2010) spond more rapidly and more intensely when attacked (Conrath
stresses. et al., 2006; Heil and Ton, 2008).
Attack by insects induces plants to emit a blend of volatile The synthesis of terpenoids can be altered by numerous bi-
organic compounds (VOCs). Terpenoids are important mem- otic and abiotic factors (Owen and Pe~nuelas, 2005; Pe~nuelas
bers of the class of herbivore-induced plant volatiles (HIPVs) and Munné-Bosch, 2005; Brunetti et al., 2013). Among such
(Gershenzon and Dudareva, 2007; Mumm et al., 2008). Some influencing factors is the formation of arbuscular mycorrhiza
terpenoids serve as repellents (Laothawornkitkul et al., 2008; (AM), defined as a symbiotic association of plant roots with
Unsicker et al., 2009; Maffei, 2010), while others function in soil fungi belonging to the phylum Glomeromycota. Arbuscular
indirect plant defence by attracting arthropods that prey upon or mycorrhizal fungi are heterokaryotic, obligate symbionts that
parasitize herbivores (Kessler and Baldwin, 2001; Rasmann confer on plants multifarious benefits, like improved access to
et al., 2005; Schnee et al., 2006). Additionally, terpenoids are nutrients and water and enhanced resistance to biotic and abi-
produced in response to oviposition and are involved in the at- otic stresses (Finlay, 2008; Smith and Read, 2008; Miransari,
traction of egg-parasitizing insects (Conti et al., 2008; Büchel 2010; Ruiz-Lozano et al., 2012; Evelin et al., 2013). In return
et al., 2011; Tholl et al., 2011; Hilker and Fatouros, 2015). for such colossal benefits, the fungus obtains carbon from the
In addition to their roles in direct and indirect defences, plant plants (Smith and Gianinazzi-Pearson, 1988; Smith and Read,
terpenoids, along with other HIPVs, such as green leaf volatiles 2008). Arbuscular mycorrhiza interconnects plants by means of
C The Author 2017. Published by Oxford University Press on behalf of the Annals of Botany Company.
V
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an extensive subterranean hyphal network. This network is spe- 2-C-methyl-D-erythritol 4-phosphate (MEP) pathway (Aharoni
cialized for nutrient (primarily phosphate) and water uptake et al., 2005; Rodrıguez-Concepcion, 2006; Cheng et al., 2007a).
(Miller et al., 1995). The bidirectional exchange of nutrients be- Both pathways generate universal precursors for terpenoid syn-
tween the symbionts takes place at highly branched intracellular thesis from IPP and its isomer dimethylallyl diphosphate
structures called arbuscules, which are formed in the inner cor- (DMAPP). While monoterpenes are synthesized via the MEP
tex of the plant root by the mycobiont (Harrison, 2005; pathway, sesquiterpenes are produced by the MVA pathway. In
Parniske, 2008). This interaction plays a crucial role in plant contrast to the conventional allocation, which suggests the MVA
ecosystem functioning, as more than 80 % of the terrestrial and MEP pathways are strictly independent, there is emerging
plant species rely on AM fungi for their mineral nutrition evidence that the two pathways cross-talk by allowing IPP to
(Smith and Read, 2008). shuttle between different compartments (Piel et al., 1998; Bick
The formation of AM changes the physiology and ecology of and Lange, 2003; Bartram et al., 2006; Rodrıguez-Concepcion,
the plant. Arbuscular mycorrhiza potentially strengthens both 2006). However, it has been found that 80 % of the IPP derived
direct and indirect plant defence systems (Pozo and Azcon- from the MEP pathway contributes to sesquiterpene biosynthesis
Aguilar, 2007; Jung et al., 2012; Borowicz, 2013) by altering following herbivory (Bartram et al., 2006; Arimura et al., 2008).
the secondary metabolism of the plant (Hohnjec et al., 2005; Condensation of C5 units gives rise to all-trans or all-cis
Walker et al., 2012). Formation of AM has been demonstrated prenyl diphosphate precursors that are converted by the terpene
to change the concentration and composition of terpenoids synthase (TPS) enzymes of different subfamilies into acyclic,
(Copetta et al., 2006; Khaosaad et al., 2006; Kapoor et al., mono-, bi- or tricyclic monoterpenes, sesquiterpenes or semivo-
2007; Rapparini et al., 2008). This alters the plant’s attractive- latile diterpenes (Chen et al., 2011). Terpene synthases are gen-
ness and also the insect’s behaviour (Schausberger et al., 2012; erally multiproduct enzymes, and thus even a single TPS can
Babikova et al., 2014a; Shrivastava et al., 2015). Cascading ef- significantly enhance the diversity of terpenoids (Gershenzon,
fects on higher trophic levels have also been reported (Gange 1994; Tholl, 2006; Arimura et al., 2008). The primary terpene
et al., 2003), as have indirect effect on predators and parasitoids skeletons may be further modified through secondary enzy-
of herbivores (Gange et al., 2003; Guerrieri et al., 2004; Laird matic reactions, such as dehydrogenations, hydroxylations,
and Addicott, 2007). Consequently, increased knowledge of the methylations and acylations (Dudareva et al., 2006).
mechanisms that influence production of terpenoids in AM Some terpenoids, such as b-ionone, are produced not directly
plants will make important contributions to the biocontrol and from IPP, but instead from tetraterpenes such as carotenoids, by
integrated management of pests. carotenoid cleavage dioxygenases (Dudareva et al., 2013).
In this review, readers are first introduced to the terpenoids Homoterpenes such as DMNT and TMTT are synthesized by
that contribute to HIPVs, and their synthesis in the plant cell. oxidative degradation of the sesquiterpene (3S)-(E)-nerolidol
The review emphasizes the role of terpenoids in plant defence and the diterpene geranyl linalool by cytochrome P450 en-
against herbivorous insects (Fig. 1) and discusses their probable zymes (Arimura et al., 2009; Maffei, 2010).
role in airborne signalling within the plant and to nearby plants.
It then focuses on the significance of terpenoids in AM-mediated
reinforcement of direct and indirect defences against herbivory TERPENOIDS IN DEFENCE AGAINST
(Fig. 2), further discussing various mechanisms underlying HERBIVORY
changes in the concentration and composition of terpenoids in
mycorrhizal plants. Finally, it outlines the prospects for bioengi- Direct interaction
neered terpenoid-producing plants and AM symbiosis in the sus- Terpenoids can serve as repellents and reduce larval feeding
tainable management of pests in agricultural systems. and oviposition by herbivores (De Boer et al., 2004;
Laothawornkitkul et al., 2008; Unsicker et al., 2009; Maffei,
2010). For example, linalool (a monoterpenoid) and (E)-b-far-
TERPENOIDS IN HIPVS nesene (a sesquiterpene) produced by plants repel herbivores
and aphids, respectively (Aharoni et al., 2003; Unsicker et al.,
Terpenoids are one of the important constituents of volatiles 2009; Maffei, 2010). Although the exact mechanisms by which
that are released by plants in response to herbivore attack terpenoids affect insect pests are not known, probable processes
(Gershenzon and Dudareva, 2007; Mumm et al., 2008). They include the inhibition of ATP synthase, alkylation of nucleo-
are low molecular weight compounds derived from the basic philes and interference with moulting (Langenheim, 1994).
five-carbon building blocks of isopentenyl diphosphate (IPP). Terpenoids such as a-pinene and b-pinene have been shown to
The key players among the terpenoid volatiles that significantly disturb the nervous system in insects by inhibition of
contribute to HIPVs are monoterpenes (C10), sesquiterpenes acetylcholinesterase (Yeom et al., 2012).
(C15) and homoterpenes such as 4,8-dimethylnona-l,3,7-triene
(DMNT) and 4,8,12-trimethyltrideca-1,3,7,11-tetraene (TMTT)
(Leitner et al., 2005; Arimura et al., 2008; Mithöfer and
Indirect above-ground interactions
Boland, 2012). Isoprene (2-methyl-1,3-butadiene), although not
produced by many plants, has also been demonstrated to play Terpenoids emitted as a result of herbivore attack have an
an important role in defence against insect herbivory important role in a plant’s indirect defences, attracting predators
(Laothawornkitkul et al., 2008). or parasites of herbivores and facilitating location of the at-
There are two pathways for the production of terpenoids: tacked plants (Heil, 2008). For example, infestation of lima
the cytoplasmic mevalonate (MVA) pathway and the plastidial bean leaves by spider mites (Tetranychus urticae) triggers the

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Induced defence response

Prime defence response

Priming memory lasts
up to 5 days

Monoterpenoids

Sesquiterpenoids
TMTT
OIPVs DMNT

Insect carnivore
HIPVs
Egg laying insect
Extra floral
nectaries

Leaf herbivore

Egg parasitic wasp

Predatory ants

Endoparasitic
nematodes
Ca2+ Ca2+
Calcium spiking
Root b-Caryophyllene b-Caryophyllene
herbivore
Heterospecific Conspecific

Membrane
Infested plant Uninfested plant
depolarization

FIG. 1. Overview of terpenoids in plant defence against herbivorous insects. Volatile terpenoids that belong to the HIPVs (herbivore-induced plant volatiles) and
OIPVs (oviposition-induced plant volatiles) are released in response to herbivore attack and oviposition, respectively. Terpenoids induce defence responses in the
systemic parts of the same plant. These volatiles attract insect carnivores that feed on the herbivores, thereby inducing indirect defence in plants, and prime neigh-
bouring conspecific and heterospecific plants. The perception of terpenoids by neighbouring plants results in influx of calcium ions and membrane depolarization.
Epigenetic regulation of this priming response is reported to evoke the priming memory for up to 5 d. Terpenoids also affect tritrophic interactions in soil.

de novo production of terpenoids such as (E)-b-ocimene, linal- 2006). Interestingly, changes in HIPV blends emitted at differ-
ool, DMNT and TMTT (Dicke et al., 1990, 1999; De Boer ent times can impact the interactions among a plant, its herbi-
et al., 2004; Shimoda et al., 2005), which lure the predacious vores and their parasitoids, and stimulate different preferences
mites (Phytoseiulus persimilis) that prey on spider mites for herbivores and their parasitoids (Mathur et al., 2013;
(Takabayashi and Dicke, 1996). The volatiles from spider mite- Pashalidou et al., 2015). The generalist Spodoptera littoralis
infested lima beans, treated with fosmidomycin (an inhibitor of preferred undamaged Brassica juncea plants, whereas its para-
the MEP pathway) were less attractive to the predatory mites sitoid (C. marginiventris) preferred 48-h damaged plants
than those from infested control plants, indicating the signifi- (Mathur et al., 2013). In Brassica nigra, parasitoid wasps
cance of terpenoids in indirect defence (Mumm et al., 2008). (Cotesia glomerata) were attracted to plants infested with eggs
The high chemical diversity within HIPV mixtures compli- just before and shortly after larval hatching of Pieris brassicae
cates identification of the compound(s) actually responsible for (Pashalidou et al., 2015). The authors have correlated this pref-
signalling herbivore enemies. However, it has been demon- erence to temporal changes in the blend of HIPVs (terpenoids).
strated by investigation of individual compounds that terpe-
noids such as the homoterpene TMTT can attract predatory
mites (De Boer et al., 2004). Genetic engineering for enhanced
Response to oviposition
expression of genes encoding enzymes for the formation of ter-
penoids has ascertained the role of individual compounds in tri- Plants may respond to herbivore egg deposition and activate
trophic interactions. Transgenic Arabidopsis thaliana defences before actual feeding injury is initiated, which might
overexpressing strawberry nerolidol synthase, a TPS, attracted be a successful tactic to reduce impending herbivory (Hilker
more predatory P. persimilis mites (Kappers et al., 2005). et al., 2002; Mumm and Hilker, 2006; Pashalidou et al., 2015).
Similarly, overexpression of a corn TPS gene (TPS10) in A. Analogous to HIPVs, plant volatiles induced specifically by in-
thaliana augmented the attractiveness of these transgenic plants sect oviposition are termed oviposition-induced plant volatiles
to the parasitic wasp Cotesia marginiventris (Schnee et al., (OIPVs) (Hilker and Fatouros, 2015). Terpenoids are important

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Induced defence response

Monoterpenoids
Prime defence response
Sesquiterpenoids DMNT
Insect TMTT
Insect carnivores
carnivores

Increased
glandular
trichome
density
Aphids Increased
HIPVs herbage

HIPVs HMGR?
DXS DXR
TPS
Altered
blend of
terpenoids

Leaf
herbivore

JA JA JA
SA SA
SA

Root b-Caryophyllene b-Caryophyllene

herbivore

Endoparasitic
nematodes

Cu, P
Non-mycorrhizal infested plant Zn
N,
Mn
Infested plant with Uninfested plant with
mycorrhizal association Enhanced nutrient mycorrhizal association
uptake

FIG. 2. Overview of arbuscular mycorrhiza (AM)-reinforced defence against herbivorous insects. Plants colonized by AM fungi are more tolerant by virtue of supe-
rior growth and nutrient uptake. Formation of AM may result in increased glandular trichome density, availability of substrates, induction of MEP (higher expression
of DXS and DXR) and MVA (higher expression of HMGR) pathways, and induction of terpene synthases (TPSs). These factors in various combinations result in
changes in the terpenoid profile in mycorrhizal (M) plants, inducing both direct and indirect defence responses against herbivore attack in the plant. Mycorrhizal col-
onization results in amplification of a wound signal, leading to priming of neighbouring plants. Common mycelial networks (CMNs) serve as signalling conduits be-
tween interconnected plants under herbivore attack. JA, jasmonic acid; SA, salicylic acid.

members of the class of OIPVs (Conti et al., 2008; Tholl et al., tritrophic interactions (Rasmann and Turlings, 2008). The most
2011). The OIPV-specific terpenoids attract egg parasitoids well-studied example is the induction of (E)-b-caryophyllene by
(Wegener and Schulz, 2002; Mumm and Hilker, 2005; Büchel maize roots infested by larvae of the leaf beetle Diabrotica virgi-
et al., 2011). Intriguingly, the attractiveness of egg-laden fo- fera virgifera, which attracted the entomopathogenic nematode
liage to the egg parasitoid has been related to an increase in Heterorhabditis megidis (Rasmann et al., 2005). On the other
transcription levels of sesquiterpene synthase (Köpke et al., hand, (E)-b-caryophyllene also served as an attractant aiding
2010; Beyaert et al., 2012). Oviposition on Pinus sylvestris nee- D. virgifera larvae to identify a susceptible host (Robert et al.,
dles by the sawfly Diprion pini induced both local and systemic 2012). One possible explanation for the contradictory observa-
emission of terpenoid volatiles (Hilker et al., 2002; Mumm and tions in the above studies is that as maize roots only emit (E)-b-
Hilker, 2006). This response was specific to oviposition, and caryophyllene (Hiltpold and Turlings, 2008), it can be presumed
could not be induced by artificial wounding (Hilker and that the entomopathogenic nematode H. megidis has developed
Fatouros, 2015). However, volatile cues to attract egg parasit- an adaptation to take cues from the (E)-b-caryophyllene emitted
oids have not yet been identified. by maize roots for efficient prey-searching.

Response to below-ground infestation Multiple herbivore infestations

Below-ground VOC patterns are generally distinct from vola- In nature, plants are generally infested by two or more herbi-
tiles released from above-ground plant tissues (Pe~nuelas et al., vore species, either concurrently or serially. However, most of the
2014). Terpenes are the most prominent VOCs emitted from studies in this area have been conducted on single-herbivore at-
below-ground tissues (Rasmann et al., 2005; Ali et al., 2011; tack under controlled conditions. Infestation by two or more in-
Palma et al., 2012; Pe~nuelas et al., 2014), and among these ses- sect species causes complex variations in volatile profile, and
quiterpenes are the compounds that show the greatest diffusion cannot be predicted on the basis of observations on single herbi-
in the soil (Hiltpold and Turlings, 2008). Terpenoids have been vores. When two or more herbivores co-infest, the effects may be
shown to play a crucial role in the specificity of below-ground negative or additive, or one type of herbivore takes priority. For

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example, concurrent occurrence of herbivory above- as well as Green-leaf volatiles and terpenoids are two important compo-
below-ground by S. littoralis and D. virgifera, respectively, nents of HIPVs. Green-leaf volatiles, which are aldehydes, al-
negatively influenced tritrophic signalling due to decreased cohols and esters resulting from lipoxygenase cleavage of fatty
(E)-b-caryophyllene production by maize roots (Rasmann and acids, account for the distinctive odour of damaged leaves
Turlings, 2007). This may be explained by reduced availability of (Paré and Tumlinson, 1999). Although evidence for GLVs as
a C source required for the synthesis of the terpenoid precursors. priming signals has been observed in several plant species
On the other hand, HIPVs emitted by lima beans and pepper (Farag and Paré, 2002; Ruther and Fürstenau, 2005; Ruther and
plants infested by two herbivore species attracted more predatory Kleier, 2005; Kost and Heil, 2006; Sugimoto et al., 2014), re-
mites and predatory mirid bugs, respectively, compared with vo- ports on terpenoids have been variable. The role of volatile ter-
latiles emitted by plants infested by either herbivore separately penes in plant–plant interactions was initially reported in lima
(Dicke et al., 2009). Furthermore, most studies are performed un- bean, where terpenoids such as b-ocimene, DMNT, TMTT and
der highly controlled conditions, which impedes application of linalool, released upon feeding of T. urticae, induced the ex-
the results in natural environments. Thus, a major challenge is the pression of defence genes encoding lipoxygenase (synthesis of
development of experimental designs that consider the ecological jasmonic acid) and the pathogenesis-related protein PR-2 (b-
reality of infestations. 1,3-glucanase) (Arimura et al., 2000b). In maize, however, ter-
penoids were not associated with priming defence responses in
the receiver plants (Ruther and Fürstenau, 2005).
AIRBORNE SIGNALLING TO NEIGHBOURING Early events in the perception of volatile signals comprise an
PLANTS AND SYSTEMIC PARTS OF THE SAME alteration of the plasma membrane potential (Vm) and an in-
PLANT crease in cytosolic calcium ([Ca2þ]cyt) (Zebelo et al., 2012). It
was observed that GLVs such as (E)-2-hexenal, (Z)-3-hexenal
The airborne volatile signals from herbivore-damaged plants and (Z)-3-hexenyl acetate induced stronger Vm depolarization
(emitters) enable nearby conspecific and heterospecific undam- and a greater increase in cytosolic calcium flux compared with
aged plants (receivers) to foresee the impending arrival of herbi-
terpenoids such as a-pinene and b-caryophyllene. These terpe-
vores and tailor their defence accordingly (Baldwin and Schultz,
noids induced a significant Vm depolarization with respect to
1983; Arimura et al., 2000a; Engelberth et al., 2004; Karban
controls, but did not exert any significant effect on [Ca2þ]cyt ho-
et al., 2006; Heil and Silva Bueno, 2007; Ramadan et al., 2011).
meostasis (Zebelo et al., 2012). Moreover, Vm depolarization
Herbivore-induced plant volatiles serve as external signals for
was found to increase with increasing GLV concentration.
within-plant communication, and elicit a defence response in sys-
Green-leaf volatiles are immediately released after damage and
temic parts of the affected plant (Karban et al., 2006; Frost et al., their release ceases within a few minutes of damage (Arimura
2007; Heil and Silva Bueno, 2007; Park et al., 2007; Das et al., et al., 2009), while the release of monoterpenes typically starts
2013). Damaged leaves immediately release VOCs and commu- 24 h after attack (Dudareva et al., 2006; Pichersky et al., 2006).
nicate more quickly with leaves located nearby that are not di- The emission of terpenoids is often systemic and extended
rectly connected by vasculature (Heil and Ton, 2008). Plants (Paré and Tumlinson, 1999). These observations indicate that
may react to the signals connected with the presence of herbi- GLVs are better candidates than terpenoids for conveying air-
vores by upregulating defence genes (Arimura et al., 2000b), borne signals of herbivore attack. Further studies are required
leading to increased production of defence-related metabolites to identify the messengers (volatiles) involved in transmitting
such as phytohormones, proteinase inhibitors, terpenoids and/or signals within and to nearby plants. The complementary ap-
extrafloral nectar (Tscharntke et al., 2001; Engelberth et al., proach of using plant mutants deficient in various components
2004; Kost and Heil, 2006; Frost et al., 2008a; Blande et al., of HIPVs (GLVs or terpenoids) has enabled the role of individ-
2010). These changes are ultimately translated into reduced her- ual compounds in plant–plant signalling to be deciphered
bivory and improved fitness of receiver (Karban and Maron, (Baldwin et al., 2006). However, using this technique, Paschold
2002; Kost and Heil, 2006; Muroi et al., 2011). The responses in- et al. (2006) observed that neither GLVs nor terpenoids prime
clude a combination of priming and induced defences, according the expression of defence genes in Nicotiana attenuata. The
to the allocation cost of different classes of defence, with plants role of various HIPVs as volatile priming signals has continued
priming more expensive responses and inducing less costly me- to be uncertain because in most studies healthy plants were
tabolites, such as extrafloral nectar or HIPVs, to attract natural treated with synthetic volatiles, a procedure that does not satis-
enemies of the herbivore (Kost and Heil, 2006; Frost et al., factorily mimic the exact timing and concentrations of HIPV
2008b). Participation of volatiles in interplant below-ground in- emissions in nature. Furthermore, genetic manipulation of
teractions is not well elucidated (Schenkel et al., 2015; Delory plants for enhanced synthesis of HIPVs may result in several
et al., 2016). Whether VOCs emitted by roots in the rhizosphere undesirable effects (Erb et al., 2015). As individual volatile
can diffuse into the phyllosphere and convey signals to prime compounds do not participate in plant–insect interactions in iso-
above-ground parts of the same plant is also not effectively docu- lation, another key issue for exploration is the interactive effects
mented (Erb et al., 2008). of different VOCs in these interactions. Furthermore, tech-
niques based on the limit of detection of terpenoids do not take
ROLE OF TERPENOIDS IN AIRBORNE into consideration the sensitivity of perception by biological
systems (insects), and hence do not necessarily provide biologi-
SIGNALLING
cally useful information.
An important step in understanding the mechanistic foundations After herbivore departure, plants likely cease to release
of airborne priming is the elucidation of the actual messengers. HIPVs that attract parasitoids (Puente et al., 2008). If emission

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were to continue, signals would deliver unreliable information indirect effect of AM on herbivore defence has been corre-
to parasitoids, which would then be incapable of tracking their lated to changes in the blend of terpenoids that alter plant at-
hosts. Receiver plants are not aware of how much later the her- tractiveness and insect behaviour (Babikova et al., 2014a).
bivores will arrive, and therefore have no clues regarding how In Phaseolus challenged by spider mites, for example, AM
long the primed state should be maintained. However, very lit- symbiosis with Funneliformis mosseae increased the emis-
tle is known about how receiver plants control the duration of sion of b-ocimene and b-caryophyllene, resulting in in-
the primed state, which is of importance in terms of the arrival creased attraction of predators of spider mites (Schausberger
time of herbivores. The molecular mechanisms involved in sus- et al., 2012). Similarly, Shrivastava et al. (2015) observed a
taining the primed state are also unresolved. Ali et al. (2013) greater defence response against beet armyworm
demonstrated that the priming effect of HIPVs on resistance (Spodoptera exigua) in AM than in non-mycorrhizal plants,
against herbivores is memorized and stored by plants through partly attributable to the difference in levels and blends of
epigenetic regulation of DNA, with plants able to evoke this terpenoids. Arbuscular mycorrhiza formation led to en-
memory when attacked by herbivores. Treatment with HIPV hanced levels of monoterpenes and sesquiterpenes, including
was shown to result in demethylation of cytosine sites in the monoterpenes such as myrcene, which were not detected in
promoter region of a herbivore-responsive gene for Bowman– non-mycorrhizal plants. Myrcene is a semiochemical utilized
Birk-type trypsin inhibitor (TI). Further experiments are re- by insects for communication, e.g. to deter thrips (Broughton
quired to substantiate understanding of the epigenetic control of and Harrison, 2012) or to attract aphidophagous hoverflies in
airborne signalling between plants. a terrestrial orchid (Stökl et al., 2011).

ARBUSCULAR MYCORRHIZA AND

HERBIVOROUS INSECT RESISTANCE
EFFECTS OF ARBUSCULAR MYCORRHIZA ON
Arbuscular mycorrhizal fungi are reported to affect the perfor- TERPENOIDS
mance of herbivores (Gange and West, 1994; Vicari et al.,
2002; Pozo and Azcon-Aguilar, 2007; Gehring and Bennett, Arbuscular mycorrhiza symbiosis can affect a number of vola-
2009; Borowicz, 2013). Arbuscular mycorrhiza symbioses ad- tile organic compounds, including terpenes. Arbuscular mycor-
versely affect root-feeding insects, while their effects on leaf- rhiza fungal colonization has been shown to enhance the
feeding insects are variable (Pozo and Azcon-Aguilar, 2007; production of triterpenoids (Akiyama and Hayashi, 2002),
Gehring and Bennett, 2009; Borowicz, 2013). The extent of apocarotenoids (Klingner et al., 1995; Fester et al., 2002;
protection also changes with the feeding style of the attacking Strack and Fester, 2006; Akiyama, 2007; Walter and Strack,
herbivore. Arbuscular mycorrhiza symbiosis seems to benefit 2011) and abscisic acid (Meixner et al., 2005) in roots of vari-
phloem-sucking insects (aphids) (Gange et al., 1999; Koricheva ous plants. Systemic effects of AM on the quantity and quality
et al., 2009), while effects on chewing and leaf-mining insects of terpenoids in above-ground parts of plants have also been
are largely adverse (Gange and West, 1994; Vicari et al., 2002; mooted (Kapoor et al., 2002a, b; Copetta et al., 2006;
Hoffmann et al., 2009); counter-examples, however, also exist Khaosaad et al., 2006; Kapoor et al., 2007; Zubek et al., 2010;
(Babikova et al., 2014b; Shrivastava et al., 2015). This consid- Weisany et al., 2015; Rydlova et al., 2016). These studies have
erable variation can be ascribed to some extent to the species so far been largely confined to the effects of AM on individual
(plant, fungus and herbivore) involved in the tripartite interac- components of terpenoids or a suite of terpenoids (essential oil
tions (Bennett and Bever, 2007; Gange, 2007; Leitner et al., composition) that have pharmaceutical value. Arbuscular my-
2010; Pineda et al., 2010). Akin to the complexity of plant–her- corrhiza may enhance the biosynthesis of an individual terpe-
bivore–natural enemy tripartite interactions, AM also affects noid either by increase in isoprene precursors through the
predators and parasitoids of herbivores (Gange et al., 2003; induction of biosynthesis pathways and/or by induction of ter-
Guerrieri et al., 2004; Laird and Addicott, 2007). pene synthase enzymes (Shrivastava et al., 2015). Increases in
Participating AM fungi may induce resistance to neighbour- the level of substrates by enhanced P uptake and increased pho-
ing plants, via hyphal networks functioning as plant–plant un- tosynthetic efficiency have been described (Wright et al.,
derground communication systems (Song et al., 2010; 1998a, b; Kapoor et al., 2002a, b; Rasouli-Sadaghiani et al.,
Babikova et al., 2013). Common mycorrhizal network serve as 2010). The role of P is perceptible in the synthesis of terpenoids
conduits facilitating the transfer of defence signals and also ter- both via the MVA pathway, which requires acetyl-CoA, ATP
penoids between neighbouring plants under herbivore attack and NADPH, and via the MEP pathway, requiring glyceralde-
hyde phosphate and pyruvate, of which P is a constituent.
(Song et al., 2014).
Photosynthesis provides ATP and carbon substrate (glyceralde-
hyde-3-phosphate or pyruvate) for isoprene synthesis. Increased
ROLE OF TERPENOIDS IN AM-REINFORCED foliar biomass in AM plants results in greater photosynthetic
RESISTANCE AGAINST HERBIVOROUS capacity and thus increased production of total photosynthates
required for terpenoid biosynthesis (Niinemets et al., 2002; Cao
INSECTS
et al., 2008; Hofmeyer et al., 2010). However, P nutrition alone
The significance of below-ground interactions between plant fails to explain terpenoid accumulation in AM fungus-co-
and AM fungi for assessing VOC emission rates and their con- lonized plants (Copetta et al., 2006; Khaosaad et al., 2006;
sequent ecological role in the deployment of indirect defences Rydlova et al., 2016). This is not unanticipated, assuming that
by plants has been emphasized (Rapparini et al., 2008). The the biosynthesis of isoprene precursors is regulated by complex

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 Sharma et al. — Terpenoids in plant defence against herbivorous insects 797

mechanisms, some of them independent of P nutrition (Kirby control of emission (augmenting or repressing) in plants
and Keasling, 2009; Vranova et al., 2012; Kumari et al., 2013). (Vickers et al., 2014). Genetic manipulation of plants for terpe-
The enzyme 1-deoxy-D-xylulose 5-phosphate synthase (DXS) noid emission is a promising method to alter tritrophic interac-
catalyses the rate-limiting step of the MEP pathway. Walter tions. In recent years, transgenic plants producing terpenoids
et al. (2000) first demonstrated fungal-induced upregulation of have been used to repel herbivores (Aharoni et al., 2003), deter
DXS and DXR (1-deoxy-D-xylulose 5-phosphate reductoisomer- oviposition (McCallum et al., 2011) and attract predators
ase) transcript levels in AM-colonized roots of various cereals. (Bouwmeester et al., 2003; Kappers et al., 2005; Beale et al.,
This was followed by a series of reports on the upregulation of 2006) and parasitoids (Schnee et al., 2006). The physiological
DXS transcripts in mycorrhizal roots of various plants (Hans cost of terpenoid production has been assumed to be minor,
et al., 2004; Strack and Fester, 2006; Floß et al., 2008). given their low molecular weight and the relatively low concen-
Transcription of genes encoding DXS and DXR enzymes is trations emitted (Dicke and Sabelis, 1990; Halitschke et al.,
upregulated by AM symbiosis and correlated with quantitative 2000). On the other hand, a number of studies have demon-
terpenoid concentration in leaves (Mandal et al., 2015a). This strated that constitutive transgenic production of terpenes can
increase in transcription and terpenoid content has been ascribed result in negative physiological effects on the plant (Aharoni
to an increased concentration of the phytohormone jasmonic et al., 2003; Robert et al., 2013). These effects may be mani-
acid (Mandal et al., 2015a; Nair et al., 2015) and/or improved fested as stunted growth, reduced reproductive yield and also
mineral nutrient availability (Mandal et al., 2015a), and may enhanced conspicuousness and attractiveness of plants to pests
therefore be influenced by both nutritional and non-nutritional (Robert et al., 2013). Furthermore, constitutive emission of
mechanisms (Mandal et al., 2013). Results obtained so far sug- HIPVs by transgenic plants would render these emissions unre-
gest that the AM fungal-mediated increase in concentrations of liable as cues for natural enemies that might waste hunting time
terpenoids is due to enhanced production of IPP/DMAPP de- in prey-free environments (Gish et al., 2015). Therefore, syn-
rived from the MEP pathway (Mandal et al., 2015a). There chronized engineering strategies that consider herbivore-
were have been no reports of AM-mediated changes in the induced emissions are required to circumvent these cost effects.
MVA pathway in the literature until recently, when Further studies are required to evaluate the physiological and
Venkateshwaran et al. (2015) reported that mevalonic acid is ecological costs of terpenoid manipulation in the field to deter-
crucial for the transduction of symbiotic signals produced by mine the future of this approach for environmental pest man-
AM fungi to induce symbiotic gene expression in plants. agement strategies (Robert et al., 2013).
Arbuscular mycorrhiza influences the concentration of spe- Engineering of tritrophic interactions to successfully protect
cific terpenoids and their derivatives in plants by upregulating crop species requires consideration of a number of aspects
the transcription of downstream genes of the dedicated biosyn- (Bouwmeester et al., 2003; Degenhardt et al., 2003). For exam-
thesis pathway (Mandal et al., 2015a, b). Induction of TPS fam- ple, identification of an appropriate carnivore species for effec-
ily genes TPS31, TPS32 and TPS33 in mycorrhizal tomato tive control of herbivore populations is required – one that is
(Zouari et al., 2014) further suggests a probable mechanism un- naturally present in the cultivation area and attracted by manip-
derlying the change in terpenoid profile observed in AM plants. ulating a known terpenoid (Vickers et al., 2014). Engineered
Glandular trichomes are one of the most common secretory emissions, however, should not attract other herbivores. The
structures that produce and accumulate terpenoids in plants overall benefit of manipulated terpenoid emissions can be sig-
(Karban and Baldwin, 1997; Van Schie et al., 2007; Kang nificantly enhanced by making the release inducible, by insert-
et al., 2010; Schilmiller et al., 2010). A direct relation between ing a herbivore-inducible tissue-specific promoter with the
augmented concentration of terpenoids and glandular trichome terpene synthase gene (Degenhardt et al., 2009). Such con-
density has been observed in a number of plants (Ringer et al., trolled release would prevent the attraction of herbivores by
2005; Bartram et al., 2006; Behnam et al., 2006; Mu~noz- healthy plants and would lead to recruitment of natural enemies
Bertomeu et al., 2006). Correspondingly, an increase in tri- only when the plant is attacked by herbivores (Robert et al.,
chome density upon colonization by AM fungi has often been 2013). The lack of understanding of mechanisms by which
proposed to augment concentration of terpenoids (Copetta plants recognize and respond to olfactory cues restricts the
et al., 2006; Kapoor et al., 2007; Morone-Fortunato and Avato, prospects for the utilization of terpenoids in crop plants. The
2008). It was demonstrated in Artemisia annua that AM en- highly simplified community structure of large-scale agricul-
hances glandular trichomes by inducing the transcription of tural plantings is another challenge for the effective application
TTG1 (transparent testa glabra 1), a transcription factor that of HIPVs, as natural enemy attraction may be ineffective in
acts at the top of the regulatory hierarchy of trichome develop- controlling pests in the core regions of large agricultural fields
ment (Mandal et al., 2015a). However, continued studies are re- (Gish et al., 2015).
quired to elucidate the mechanisms of enhanced production of Alteration of the terpenoid profile in AM plants appears to
glandular trichomes and further ascertain the role of phytohor- be one of the important mechanisms for augmented defence
mones in AM plants. against herbivorous insects. Different AM fungal species have
variable effects on terpenoid blends (Kapoor et al., 2002b;
Sailo and Bagyaraj, 2005; Arpana et al., 2008), and conse-
quently likely differentially influence plant–herbivore and
CONCLUSIONS AND FUTURE PROSPECTS
higher trophic level interactions. In this context, comparative
The volatile nature of terpenoids confers the ability to act as ef- studies using different AM fungal species are warranted, to en-
ficient signalling molecules. Potential deployment in pest man- able differentiation of universal from species-specific re-
agement practices in agriculture depends upon the efficient sponses, and also to identify those AM fungal species efficient

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in defence against specific herbivores. As the efficiency of AM Beale MH, Birkett MA, Bruce TJ, et al. 2006. Aphid alarm pheromone pro-
symbiosis may be limited by nutrient availability in agricultural duced by transgenic plants affects aphid and parasitoid behavior.
Proceedings of the National Academy of Sciences of the USA 103:
fields, comprehensive studies are also required to evaluate the 10509–10513.
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growth and response to herbivory. Ecology 88: 210–218.
We are grateful to Professor R. Geeta, Professor Rajesh Beyaert I, Köpke D, Stiller J, Hammerbacher A, et al. 2012. Can insect egg
deposition ‘warn’ a plant of future feeding damage by herbivorous larvae?
Tandon and Professor Sudheshna Mazumdar-Leighton for Proceedings of the Royal Society, B 279: 101–108.
critically reviewing the manuscript and for their valuable com- Bick JA, Lange BM. 2003. Metabolic cross talk between cytosolic and plastidial
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Delhi, Delhi, India, for financial assistance. ates across the chloroplast envelope membrane. Archives of Biochemistry
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