Insect Science (2018) 25, 2–23, DOI 10.1111/1744-7917.

12436

REVIEW

Indirect plant defense against insect herbivores: a review

Zainab Aljbory1 and Ming-Shun Chen1,2

1 Department
of Entomology, Kansas State University, Manhattan, Kansas, USA and 2 Hard Winter Wheat Genetics Research Unit,
USDA-ARS, Kansas State University, Manhattan, Kansas, USA

Abstract Plants respond to herbivore attack by launching 2 types of defenses: direct

defense and indirect defense. Direct defense includes all plant traits that increase the
resistance of host plants to insect herbivores by affecting the physiology and/or be-
havior of the attackers. Indirect defense includes all traits that by themselves do not
have significant direct impact on the attacking herbivores, but can attract natural en-
emies of the herbivores and thus reduce plant loss. When plants recognize herbivore-
associated elicitors, they produce and release a blend of volatiles that can attract preda-
tors, parasites, and other natural enemies. Known herbivore-associated elicitors include
fatty acid–amino acid conjugates, sulfur-containing fatty acids, fragments of cell walls,
peptides, esters, and enzymes. Identified plant volatiles include terpenes, nitrogenous
compounds, and indoles. In addition, constitive traits including extrafloral nectars, food
bodies, and domatia can be further induced to higher levels and attract natural enemies
as well as provide food and shelter to carnivores. A better understanding of indirect
plant defense at global and componential levels via advanced high throughput technolo-
gies may lead to utilization of indirect defense in suppression of herbivore damage to
plants.

Key words elicitor; indirect plant defense; natural enemies; volatile

During the long course of interactions and coevolution,
both plants and insect herbivores have obtained diverse
mechanisms to fight against each other. Plants, which
usually have greater biomass but less mobility, possess
various chemical and physical traits to counter attack
from insects. Plant defense traits can be preformed (also
called constitutive defense) or induced upon insect attack
(inducible defense). Inducible defense is turned off un-
til insect attack is detected and therefore can minimize
the metatolic cost of defense for plants (Dicke & van
Poecke, 2002). Inducible defense can be classified into
direct defense and indirect defense. Direct defense in-
cludes traits that can reinforce the endogenous ability of
Correspondence: Ming-Shun Chen, Department of Entomol-
ogy, Kansas State University, Manhattan, KS 66506, USA. Tel:
785-532-4719; fax: 785-532-6232; Email: mchen@ksu.edu or
ming-shun.chen@ars.usda.gov
plants to counter insect attacks, whereas indirect defense
incites an exogenous intervention by carnivores (Turlings
& Wäckers, 2004; Van Poecke & Dicke, 2004; Chen,
2008; Heil, 2008; Mumm & Dicke, 2010; Zhuang et al.,
2012; Hagenbucher et al., 2013; Xu et al., 2015). In in-
direct defense, plants produce and emit a unique blend of
volatile compounds, also called herbivore-induced plant
volatiles (HIPVs) (Clavijo McCormic et al., 2012). Many
predators and parasitoids can use HIPVs as a cue to
find their prey (Van Poecke & Dicke, 2004; Pichersky
et al., 2006; Clavijo McCormic et al., 2012). Mycoph-
gous mite or omnivores can also be attracted by HIPVs to
find plants that harbor foliar pathogenic fungi (Da Silva
et al., 2014; O’Connell et al., 2015). In a previous article,
we have reviewed inducible direct plant defenses (Chen,
2008). In this article, we intend to provide a detailed re-
view on indirect plant defense against insect herbivores,
including elicitors, plant hormones, plant volatiles, and

2

C 2016 Institute of Zoology, Chinese Academy of Sciences
 Indirect plant defense against insects 3

Herbivore attack

Inducible
defense
Plant indirect defense
Elicitors
• Fatty-acid-amino acid conjugates
• Sulfooxy fatty acids
• Enzymes
• Fragments of cell walls
• Peptides
• Ester

Reduce the load

of herbivores
• Extrafloral nectar
Hormone pathways
• Food body • JA
• Domatia • SA
• ET

Volatiles compounds
• Terpenes and terpenoids
Constitutive defense • Nitrogenous compounds
• Volatile indoles
• Fatty acid derivatives

Natural enemies
• Predators
• Parasitic wasps
• Omnivores

Fig. 1 Major components and pathways involved in indirect plant defense. Indirect plant defense can be both constitutive and inducible.
Constitutive defense includes extrafloral nectar, food bodies and domatia. Inducible defense is initiated with the production of various
elicitors, including enzymes, fatty acid–amino acid conjugates, sulfooxy fatty acids, fragments of cell walls, peptides, and esters.
Elicitors trigger the activation of hormone pathways, such as jasmonic acids (JA), salicylic acids (SA), and ethylene (ET). The activation
of plant hormone pathways results in the synthesis of a broad spectrum of volatiles such as terpenes, volatile indoles, aldehydes, ketones,
esters, alcohols, and nitrogenous compounds. These volatiles can be used as cue to attract natural enemies including predators, parasites,
and omnivores, resulting in the suppression of the pest population.

natural enemies that are involved in indirect plant defense
(Fig. 1).
Elicitors that trigger plant defense
The first step for launching plant defense is the recog-
nition of insect attack by plants. Plants perceive insect
attack by specific recognition of elicitors, which are pro-
duced by various mechanisms (Kessler & Baldwin, 2002).
Some elicitors are produced in attacking insects and then
injected into plant tissues as part of insect oral secre-
tions or oviposition fluid (Turlings et al., 1993; Kessler
& Baldwin, 2002; Musser et al., 2002; Erb et al., 2009;
Diezel et al., 2009; Bonaventure et al., 2011). Other elic-
itors are produced in plants in response to insect damage


C 2016 Institute of Zoology, Chinese Academy of Sciences, 25, 2–23
4 Z. Aljbory & M. S. Chen
(Erb et al., 2012). The following sections provide a list
of well characterized elicitors that induce indirect plant
defense.
Fatty acid–amino acid conjugates
Fatty acid–amino acid conjugates consist of saturated
and unsaturated fatty acids (16 or 18 carbons), which
conjugate to amino acids, typically α-Glutamine or α-
Glutamic acid (Alborn et al., 1997; Halitschke et al.,
2001; Truitt et al., 2004; Christensen et al., 2013). Differ-
ent forms of fatty acid–amino acid conjugates have been
identified in different insect species (Mori et al., 2003;
Yoshinaga et al., 2007; Yoshinaga et al., 2010; Mori &
Yoshinaga, 2011; Yoshinaga et al., 2014). Volicitin, the
compound N-(17-hydroxylinolenoyl)-l-Gln is the most
extensively characterized fatty acid–amino acid conju-
gate. Volicitin was first identified in the regurgitant of
Spodoptera exigua, and was found to induce volatiles
in corn plants (Alborn et al., 1997). Later volicitin and
other structurally related fatty acid–amino acid conju-
gates have been found in other lepidopteran species as
well as nonlepidopteran species, but the abundance of
these conjugates varies widely from species to species
(Halitschke et al., 2001; Mori et al., 2001; Alborn et al.,
2003; Mori et al., 2003; Yoshinaga et al., 2007; Yoshi-
naga et al., 2010; Hettenhausen et al., 2013; Yoshinaga
et al., 2014). A comparative study with different types of
elicitors revealed that volicitin possesses the widest range
of phytohormone and volatile-inducing activity in differ-
ent plant species including maize, eggplant and soybean
(Schmelz et al., 2009). In addition to their elicitor roles in
plants, fatty acid–amino acid conjugates in insects must
have a role that benefits the herbivores. Even though the
exact functions of fatty acid–amino acid conjugates are
not clear at present, it has been suggested that they may
act as biosurfactants that facilitate the transport and di-
gestion of food, or they may neutralize the effects of plant
toxins in the gut of the caterpillar larvae (Halitschke et al.,
2001).
The elicitation mechanism for fatty acid–amino acid
conjugates in plant defense remains to be revealed in gen-
eral. A plasma membrane protein has been found to be
capable of binding with volicitin in corn plants, and the
interaction between the binding protein and volicitin initi-
ates plant defenses (Truitt et al., 2004). However, specific
steps in the signal transduction pathway remain to be de-
lineated. It also remains to be determined the relationship
among volicitin and other acid–amino acid conjugates in
eliciting the release of a specific set of volatiles that at-
tract natural enemies specific to the pest (Turlings et al.,
2000).

C 2016 Institute of Zoology, Chinese Academy of Sciences, 25, 2–23
Sulfooxy fatty acids
Sulfooxy fatty acids (also called sulfur-containing fatty
acids) are another type of elicitor. The most exten-
sively characterized sulfooxy fatty acids are caeliferins
(O’Doherty et al., 2011). Caeliferins are composed of
saturated and monounsaturated sulfated α-hydroxy fatty
acids, in which the ω-carbon is functionalized with either
a sulfated hydroxyl or a carboxyl conjugated to glycine
via an amide bond (Felton & Tumlinson, 2008; Schäfer
et al., 2011). Caeliferins were first identified to be active
elicitors from the regurgitant of Schistocerca americana
in corn plants (Alborn et al., 2007). Recently, the caelif-
erin A16:0 has also been detected in the oral secretions of
the grasshopper Schistocerca gregaria and other species
in the suborder Orthoptera (Felton & Tumlinson, 2008;
Schäfer et al., 2011).
Chemical synthesis of various caeliferins has been
achieved (O’Doherty et al., 2011; Peng et al., 2016).
Synthetic caeliferin A16:0 is able to induce significant
production of Jasmoic acid (JA) and ethylene (ET) in
Arabidopsis when it is delivered at concentrations corre-
sponding to those found in grasshopper saliva (Schmelz
et al., 2009; O’Doherty et al., 2011). The availability of
chemically synthesized caeliferins should allow scientists
to study the mode of action of this group of elicitors, in-
cluding the identification of plant receptors and the signal
transduction cascade.
Ester (bruchins)
A group of 3-hydroxypropanoate esters of long-chain
α,ω-diols can also elicit plant defense reactions (Doss
et al., 2000). These groups of ester elicitors are collec-
tively called bruchins. Unlike elicitors, which are pro-
duced in insects and delivered into plant tissues through
oral sections, bruchins are produced in insects, but deliv-
ered into plant tissues when insects deposit eggs (Doss
et al., 2000; Oliver et al., 2000). So far bruchins are
only found in pea weevil Bruchus pisorum and cowpea
weevil Callosobruchus maculatus, and it is not clear if
they are also present in other insect species. However,
oviposition of butterflies Pieris brassicae and P. rapae
can induce changes in plants that are capable to attract
Trichogramma egg parasitoids, indicating that elicitors
are likely delivered into plant tissues during their egg
deposition (Fatouros et al., 2005; Fatouros et al., 2009;
Pashalidou et al., 2010). Bruchins are highly potent elic-
itors and can elicit plant responses with application of
as little as 1 fmol (Oliver et al., 2002). Application of
bruchins induces the expression of the gene MtN19-
like (function unknown) and the gene CYP93C18, which

encodes an isoflavone synthase involved in the formation
of the isoflavonoid phytoalexin pisatin (Cooper et al.,
2005). Bruchins stimulate cell division at the sites of egg
attachment, and as a result, tumor-like growth of undif-
ferentiated cells is activated beneath the egg, resulting in
impeding larval entry into the pod (Doss et al., 2000).
Despite the high potency of bruchins in elicitation, the
linkage between bruchins and the induction of volatiles for
attraction of natural enemies in indirect defense remains
to be established (Bruessow et al., 2010). The types of
natural enemies attracted by plants treated with bruchins
needs to be documented too. On the other hand, it is clear
that the neoplastic growth at the infested site prevents
weevil larvae entering into plant tissue and exposes them
to predators, parasites, and desiccation, achieving similar
results observed in a classic indirect defense (Fatouros
et al., 2008).
Peptides
It has been known for a long time that insects can syn-
thesize proteins and peptides in salivary glands and in-
ject them into plant tissues during feeding (Miles, 1999).
These secreted proteins and peptides perform functions
ranging from plant manipulation to partial digestion of
pre-ingested food (Ribeiro, 1995). Some of the secreted
proteins from insects are also likely to serve as elicitors
to activate plant defense (Kessler & Baldwin, 2002). The
most extensively studied peptide elicitor in indirect plant
defense is a peptide named inceptin (Schmelz et al., 2006).
Interestingly, inceptin, a disulfide-bridged peptide (ICD-
INGVCVDA), is derived from the plant chloroplastic ATP
synthase g-subunits. When chloroplastic ATP synthase g-
subunits in plants are ingested into the gut of insects, the
proteins are converted into inceptin through proteolytic
cleavage (Schmelz et al., 2006; Schmelz et al., 2007;
Felton, 2008; Felton & Tumlinson, 2008). Inceptin is then
delivered back into plant tissue as a component of insect
oral secretions. Inceptin and its related peptides are also
identified from plants attacked by different insect species
(Schmelz et al., 2009). Like other elicitors, inceptin can
trigger increased levels of ethylene (ET), JA, and salicylic
acid (SA) in plants, leading to the release of terpenoid
volatiles (Schmelz et al., 2006; Schmelz et al., 2007).
The mechanisms for the perception of inceptin by plants
and for distinguishing between inceptin and its own na-
tive chloroplastic ATP synthase γ -subunit are not clear.
The recognition mechanism for inceptin appears very
specific since deleting 1 amino acid at the C-terminal
abolish the activity of the elicitor (Schmelz et al., 2007),
suggesting a possible ligand–receptor interaction in the
signaling pathway.

C 2016 Institute of Zoology, Chinese Academy of Sciences, 25, 2–23
Indirect plant defense against insects 5
Alamethicin is another small peptide that is a
potent elicitor to activate indirect plant defense
(Engelberth et al., 2001). Alamethicin contains 20 amino
acid residues (Ac-Aib-P-Aib-A-Aib-A-Q-Aib-V-Aib-G-
L-Aib-P-V-Aib-Aib-EQ-Phl; Ac = acetyle, Phl = pehny-
lalaninol, Aib = 2-aminoiobutyric acid) and is highly
hydrophobic. The peptide is derived from the fungus Tri-
choderma viride and has been used as antibiotic (Matic
et al., 2005). There are 2 forms of alamethicin that differ
only in the residue 18, Glu in one form and Gln in the other
form (Sansom, 1993). The likely mechanism for alame-
thicin elicitation is through forming a voltage-dependent
ion channel, inducing cell membrane potential depolariza-
tion (Matic et al., 2005; Maischak et al., 2007). Alame-
thicin regulates the expression of terpene synthases, the
enzymes involved in insect-induced release of volatiles
(Herde et al., 2008; Huang et al., 2010). Treatment of
lima bean plants with alamethicin can result in release
of volatiles that are comparable to those released when
the JA cascade is antagonized by the salicylic acid (SA)
cascade. However, channel-forming peptides like alame-
thicin have not yet been found in the saliva of insect
herbivores (Kessler & Baldwin, 2002).
Enzymes
Oral secretions of insects contain various enzymes in-
cluding proteases, glucodidases, and oxidases that are in-
volved in different functions such as digestion of pre-
ingested food (Lenz et al., 1991). However, some of these
enzymes can also elicit indirect plant defense responses
(Kessler & Baldwin, 2002; Felton & Tumlinson, 2008;
Bonaventure et al., 2011; Xu et al., 2015).
Glucose oxidases catalyze the oxidation of D-glucose
to produce hydrogen peroxide and D-glucono-δ-lactone
(Wong et al., 2008; Eichenseer et al., 2010). The en-
zymes are produced in the labial glands of lepidopteran
species including Helicoverpa zea (Eichenseer et al.,
1999; Musser et al., 2002; Musser et al., 2005; Peiffer
& Felton, 2005), S. exigua (Bede et al., 2006), and M.
sexta (Diezel et al., 2009). Several insect species other
than lepidopterans have also been found to possess glu-
cose oxidase activity, including honey bees Apis mellifera
(Iida et al., 2007), aphid Myzus persicae (Harmel et al.,
2008), and grasshopper S. americana (Candy, 1979). Glu-
cose oxidases are found to induce rapid and delayed de-
fense reactions in certain plant species (Tian et al., 2012).
Salivary signals, which contain glucose oxidases, can in-
duce indirect defense in tomato (Louis et al., 2013).
β-Glucodidases catalyze the hydrolysis of the glyco-
sidic bonds to terminal nonreducing residues in beta-D-
glucosides and oligosaccharides, with release of glucose
6 Z. Aljbory & M. S. Chen
(Cox et al., 2000). β-glucosidase has been found to trig-
ger the induction of volatile terpenes from cabbage, lima
bean, and corn plants (Hopke et al., 1994; Mattiacci et al.,
1995; Stotz et al., 2000; Kessler & Baldwin, 2002; Felton
& Tumlinson, 2008; Bonaventure et al., 2011).
The elicitation mechanisms for both glucose oxi-
dases and β-glucodidases remain to be ascertained. It
is unlikely that plants recognize these proteins in a
ligand-receptor interaction as the case in other elici-
tors. For glucose oxidases, hydrogen peroxides released
by the enzyme might serve as a signal for volatile
production. It is likely that elicitation activity of β-
glucodidase is also linked with its enzymatic activity. If
that’s the case, both glucose oxidases and β-glucodidases
are themselves not elicitors, but rather elicitor
producers.
Fragments of cell walls
Fragments of cell walls including oligogalacturonides
produced in plants as a result of herbivore attack can
also serve as elicitors to activate both indirect plant de-
fenses. Elicitors that arise due to the damage of plant cells
are called plant damage-associated molecular patterns
(DAMPs) (Erb et al., 2012). An important type of plant
damage-associated molecular patterns are oligogalactur-
onides, which are oligomers of alpha-1,4 linked galac-
turonosyl residues released from plant cell walls upon
partial degradation of homogalacturonan (Creelman &
Mullet, 1997a; Bonaventure et al., 2011; Ferrari et al.,
2013; Benedetti et al., 2015). Limited evidence also in-
dicates that oligogalacturonides activate plant defenses
through the octadecanoid pathway (Doares et al., 1995),
suggesting that JA are involved in the function of elicitor
oligogalacturonides (John et al., 1997).
At present, research on elicitors is still in the initial
phase of identifying elicitors and their potential signal
transduction components. Considering the vast number of
insect species and host plants, known elicitors are proba-
bly representing only a small portion of elicitors involved
in plant–insect interactions. More research with improved
sensitity instruments may lead to identify new or even
new types of elicitors. Some known elicitors may hold
great promise in integrated pest management. For exam-
ple, volicitin, caeliferens, and bruchins need only tiny
amount to trigger plant response, and might be manufac-
tured industrially. If these elicitors are applied artificially
to plants prior to heveay hervivore infestation, it could
result in effective control of pest damage. Further studies
on industrial synthesis of elicitors with low cost and field
efficacy tests are needed for practical application of the
identified elicitors.

C 2016 Institute of Zoology, Chinese Academy of Sciences, 25, 2–23
Plant hormones involved in indirect defense
Plant hormones act as signal molecules to regulate plant
growth and development and participate in regulation
of plant responses to various abiotic and biotic stresses
(Verma et al., 2016). Extensive research has been con-
ducted to investigate the roles of plant hormones in the
induction of plant defenses when plants are attacked by
arthropods and pathogens in the past few decades (Dicke
et al., 1999; Runyon et al., 2010; Wei et al., 2014; Vos
et al., 2015). In both indirect and direct defenses, plants
increase the production of hormones to the level needed to
initiate a cascade of signal transduction. Plant hormones
that have been found to play a role in indirect plant de-
fense include JA, SA, and ET (Erb et al., 2012; Thaler
et al., 2012; Zhang et al., 2013).
Jasmonic acid
The crucial role of JA in inducible indirect defense has
been investigated in the past decades (Gatehouse, 2002;
Liechti & Farmer, 2002; Howe & Jander, 2008; Wu &
Baldwin, 2010; Hettenhausen et al., 2013). JA is synthe-
sized from linolenic acid through the action of several
enzymes including phospholipases, lipoxygenases, allene
oxide synthases, and allene oxide cyclases in chloroplast
membranes in response to herbivory (Hyun et al., 2008;
Wasternack & Hause, 2013). The induction of the JA path-
way by herbivore-associated elicitors have been reported
in many cases, including M. sexta, M. quinquemaculata
(Halitschke et al., 2001); S. gregaria (Schmelz et al.,
2009; Schäfer et al., 2011); and S. frugiperda (Schmelz
et al., 2006; Schmelz et al., 2007). Plants treated with
JA exhibit stronger attraction to predators and parasitoids
under both laboratory and field conditions (Hopke et al.,
1994; Thaler et al., 1996; Dicke et al., 1999; Gols et al.,
1999; Thaler, 1999; Ozawa et al., 2000).
In plants, JA is modified into different active forms
including JA-Ile, methyl jasmonate (MeJA), and the JA
precursor 12-oxophytodienoic acid (OPDA) (Staswick &
Tiryaki, 2004; Wang & Jiang, 2007; Woldermariam et al.,
2012). Each different JA derivative plays certain roles in
plant physiology and their exact roles in indirect defense
remain to be determined. The roles of MeJA in inducible
indirect defense have been studied relatively extensively.
When plants are exposed to MeJA, they initiate series JA-
mediated defense responses, resulting in increased plant
resistance to herbivores (Farmer & Ryan, 1992; Grimes
et al., 1992; Melan et al., 1993; Kahl et al., 2000; Truitt
et al., 2004). The MeJA-treated plants increase volatile
emissions and attract predators and parasitoids at lev-
els comparable to those in plants elicited with herbivore

elicitors (Dicke et al., 1999; Thaler, 1999; Meiners &
Hilker, 2000; Kessler & Baldwin, 2001; Mumm et al.,
2003; Heil, 2004; Bruinsma et al., 2009).
Salicylic acid
SA is a monohydroxybenzoic acid derived from cin-
namate produced from phenylalanine by the activity of
phenylalanine ammonia lyases (Chen et al., 2009). Like
other plant hormones, SA plays essential roles in regulat-
ing plant growth and development (Rivas-San Vicente &
Plasencia, 2011), and are involved in plant defense against
herbivores (Ryals et al., 1996; Potlakayala et al., 2007;
Benedetti et al., 2015; Khan et al., 2015). More and more
evidence suggests that SA-related signaling pathways are
involved in indirect defense by inducing the emission of
volatiles (Ozawa et al., 2000; Kessler & Baldwin, 2002; de
Boer et al., 2004; Maffei et al., 2007; Diezel et al., 2009).
First, SA can be modified directly to form the bioac-
tive SA derivative MeSA. Elevated levels of MeSA and
its direct attraction to natural enemies of herbivores have
been observed in lima bean and tomato plants upon spider
mite infestation (Dicke et al., 1990; Dicke et al., 1998;
Ozawa et al., 2000), pear plants upon spider mite attack
(de Boer et al., 2004); pear plants in responding to psyllid
infestation (Scutareanu et al., 1997); and potato plants in
responding to Colorado potato beetle infestation (Bolter
et al., 1997). Poplar tree leaves treated with MeSA exhibit
induced expression of defense genes and increased emis-
sion of volatile compounds (Arimura et al., 2004). Lima
bean plants treated with MeSA also exhibit to elevated
emission of 2 homoterpenes, which are able to attract for-
aging predatory mites (Dicke et al., 1999; Ozawa et al.,
2000). These results suggest that MeSA itself can attract
natural enemies of insect herbivores and MeSA can also
induce the emission of other volatiles to enhance indirect
defense. However, not every type of insects can induce
the formation of MeSA. Caterpillar damage does not in-
duce emission of MeSA although it induces increased
levels of SA and activates SA-inducible genes (Turlings
et al., 1993; Bi et al., 1997; Ozawa et al., 2000; Diezel
et al., 2009). Similarly, not every plant species responds
to MeSA treatments. Wild tobacco plants treated with
MeSA are not attractive to predatory foragers (Kessler
& Baldwin, 2001). Arabidopsis plants treated with SA
is not attractive to the parasitoid Cotesia rubecula, a
parasite of caterpillar P. rapae, whereas JA treatment does
(van Poecke et al., 2001). These observations suggest that
JA is mainly involved in defense against leaf-chewing
herbivores, whereas SA induces greater defense against
piercing and sucking insects (Walling, 2000; van Poecke
& Dicke, 2004; Zhao et al., 2009). The down-stream

C 2016 Institute of Zoology, Chinese Academy of Sciences, 25, 2–23
Indirect plant defense against insects 7
pathways that lead to the production of different blend
of effective volatiles for specific natural enemies remain
to be revealed.
Ethylene
One of the earliest detectable events in plants after a
herbivore attack is a rapid increase in ET biosynthesis
(Ecker & Davis, 1987; Ecker, 1995; Bari & Jones, 2009).
ET is produced from methionine through the sequential
enzymatic activity of S-adenosylmethionine synthetases,
aminocyclopropane-1-carboxylic acid (ACC) synthases,
and ACC oxidases (Wang et al., 2002). Elevated levels of
ET are produced in response to not only herbivory, but also
mechanical wounding (Dicke & van Poecke, 2002; Wu &
Baldwin, 2010). However, the induction of an ET burst
by insects’ oral secretions or elicitors is much greater
than that induced by just mechanical wounding (Wu &
Baldwin, 2010). Rapid ET induction after insect damage
has been observed in various plant species including pine
trees (Shain & Hillis, 1972), onions (Kendall & Bjostad,
1990), and tomato plants (O’Donnell et al., 1996). Block-
age of ET perception with 1-MCP diminishes herbivory-
induced volatile emission (Schmelz et al., 2003), suggest-
ing that ET plays a role in inducible indirect plant defense.
The pathways leading to increased production of volatiles
and the components of volatile blend effective for natural
enemy attraction remains to be studied.
Cross-talk among plant hormones in indirect plant
defense
The effect of plant hormones on the regulation of
plant growth, development, and differentiation is achieved
through cross-talk among different hormones (Dicke &
van Poecke, 2002; Kessler & Baldwin, 2002; van Poecke
& Dicke, 2004; Felton & Tumlinson, 2008; Wu & Bald-
win, 2010; Erb et al., 2012). Likewise, the induction
of plant defenses against herbivores is also regulated
through cross-talk among these plant hormones. Interac-
tions among plant hormones can be both synergistic and
antagonistic under different conditions. It is these positive
and negative interactions that help plants to minimize en-
ergy costs by tuning plant defense responses more specific
to different invaders (Reymond & Farmer, 1998; Pieterse
et al., 2001; Koornneef & Pieterse, 2008).
Antagonistic interactions between JA and SA pathways
are well documented (Doares et al., 1995; Maffei et al.,
2007; Zarate et al., 2007; Dicke et al., 2009; Diezel et al.,
2009; Zhang et al., 2013). Because of the negative cross-
talk between SA and JA, activation of SA pathways should
theoretically render plants more susceptible to attackers
8 Z. Aljbory & M. S. Chen
that are suppressed via JA-dependent defenses, and vice
versa (Koornneef & Pieterse, 2008). However, synergis-
tic interactions between JA and SA pathways have been
also observed in indirect plant defenses against herbivores
(Schenk et al., 2000; Mur et al., 2006; Bari & Jones, 2009).
Possible ways to reduce negative interference and to in-
crease synergistic effects between JA and SA pathways in
indirect defense are likely through spatial and temporal
separation of these 2 plant hormones. In general, acti-
vation of JA pathways is more associated with chewing
insects, whereas activation of SA pathways is more asso-
ciated with pierce-sucking insects (Zhao et al., 2009). In
response to attack from chewing insects, JA pathways are
activated, whereas SA molecules are converted via methy-
lation to MeSA volatiles, which are emitted as attractants
for natural enemies, resulting in synergistic effects be-
tween these plant hormones in indirect plant defenses
(Dicke & van Poecke, 2002).
JA and ET signaling pathways are often operated syn-
ergistically to activate the expression of some defense-
related genes (Glazebrook, 2005). ET usually modulates
defense responses, particularly those mediated by the JA
cascade, rather than eliciting defense responses on its own
(von Dahl & Baldwin, 2007). ET is also likely to facilitate
unfettered JA-mediated defenses in response to herbivores
by suppressing SA activity (Diezel et al., 2009). Syner-
gistic action between ET and JA has been observed in
eliciting a number of plant defense-associated responses
in tomato and Arabidopsis plants (O’Donnell et al., 1996;
Lorenzo et al., 2003).
The regulatory pathways and impact of hormones on
plant normal metabolisms and defense responses are com-
plex. The potential negative impact of plant hormones
activiated with arthropod elictors on crop production re-
mains to be determined from system to system. Both
MeJA and MeSA have the potential to be applied directly
to plants for the attraction of natural enemies. Because of
the roles of plant hormones in both plant development and
defense responses, the impact of increased levels of MeJA
and MeSA on both plant normal growth/development and
plant defense need to be evaluated. The impact of arti-
ficial release of MeJA and MeSA to local environments
and surronding ecosystems needs to be evaulated under
specific conditions as well.
Major volatiles involved in indirect defense
Major volatiles detected in different plants following at-
tack from different herbivores share notable similarity
even though the composition of these volatiles may differ
from case to case (van Poecke & Dicke, 2004; Arimura

C 2016 Institute of Zoology, Chinese Academy of Sciences, 25, 2–23
et al., 2005; Felton & Tumlinson, 2008; Mumm & Dicke,
2010; Hare, 2011; Clavijo McCormick et al., 2012). This
structural commonality of volatiles suggests that com-
mon pathways shared by a wide range of plant species are
activated, and that a specific volatile can be recognized
by a broad spectrum of natural enemies of herbivores
(Pichersky et al., 2006; Hare, 2011, Maffei et al., 2011;
Dong et al., 2016). At present, major volatiles identified
from various plants following herbivory include volatile
terpenoids, volatile phenylpropanoid (indole), fatty acid
derivatives (also called green-leaf volatiles), and nitrogen-
containing compounds.
Terpenes and terpenoids
Terpenes belong to a large group of organic chemicals
and are among the main components of plant volatiles.
Terpenoids are modified terpenes containing additional
functional groups (Dewick, 2002). Terpenes and ter-
penoids can attract natural enemies of herbivores in var-
ious systems (Kessler & Baldwin, 2001; Kost & Heil,
2006; Chen, 2008). Elevated levels of terpene and per-
penoids in plants and subsequent attraction to natural ene-
mies following a herbivore attack are documented in many
plant species (Dicke et al., 1990; Turlings et al., 1990;
Boland et al., 1992; Dicke, 1994; Alborn et al., 1997;
Turlings & Benrey, 1998; Halitschke et al., 2001; Arimura
et al., 2004; Schnee et al., 2006; Shiojiri et al., 2006;
Arimura et al., 2008; Halitschke et al., 2008; Mumm et al.,
2008b; Kigathi et al., 2009; Schaub et al., 2010; Schuman
et al., 2014).
The important roles of terpenes and terpenoids in plant
physiology and defense are also highlighted by the exis-
tence of a large number of genes involved in the synthesis
of these chemicals. In the Arabidopsis genome, 32 genes
are found to encode putative terpene synthases, including
6 monoterpene synthases and at least 2 sesquiterpene syn-
thases, which are involved in synthesis of hemi-, mono-,
sesqui-, and diterpene (Starks et al., 1997; Bohlmann
et al., 1998; Dudareva et al., 2004; Tholl et al., 2005;
Chen et al., 2011). Numerous terpene synthase genes have
been characterized from other plants including Populus
trichocarpa, which are responsible for synthesizing ma-
jor terpene volatiles upon attack by gypsy moth Lymantria
dispar (Danner et al., 2011).
To enhance indirect plant defense, plants have been
engineered to produce specific terpenes and green-leaf
volatiles. These transgenic plants appeared to be more
attractive to carnivores than wild type (Schnee et al.,
2006; Shiojiri et al., 2006; Robert et al., 2013). Overex-
pression of terpene synthase tps10 in Arabidopsis result
in high emission of sesquiterpenes, and the transgenic

Arabidopsis plants are more preferred by the parasitic
wasps than the wild type (Shiojiri et al., 2006). Transgenic
N. attenuata, which express a maize terpene synthase
(ZmTPS10) under control of the 35S promoter, exhibit
enhanced emission of sesquiterpenes with no changes de-
tected in their emission of any other volatiles (Schuman
et al., 2014). However, the cost of constitutive overexpres-
sion of these genes to plants has not been examined, and
conditional expression systems may need to be developed
to avoid defense cost and unwant ecological impact of
constitutive gene overexpression.
Nitrogenous compounds
Nitrogenous compounds such as nitriles and oximes
are among many other volatile compounds that are com-
monly emitted from herbivore-damaged plants (van Den
Boom et al., 2004; Knudsen et al., 2006; Wei et al.,
2006; Mumm et al., 2008a; Pope et al., 2008; Irmisch
et al., 2014). In contrast to the abundant and widespread
compounds such as monoterpenes, sesquiterpenes, and
green-leaf volatiles, nitrogenous volatiles are emitted in
minor amounts (Clavijo McCormick et al., 2014). How-
ever, nitrogenous volatiles do play crucial roles as active
gradients of cues for carnivore attraction (D’Alessandro
& Turlings, 2005). The proportion of nitrogenous com-
pounds in a volatile blend can contribute to the specificity
of the volatile mix for different plant–carnivore systems
(Clavijo McCormick et al., 2012).
Biosynthetic pathways of nitrogenous compounds are
different in different plants. In crucifers, the secondary
metabolite glucosinolates are the main intermediates
for the production of nitrogenous volatiles (Mattiacci
et al., 1994; Pope et al., 2008; Hopkins et al., 2009),
whereas amino-acid derivatives catalyzed by cytochrome
P450 enzymes are likely the main source for produc-
ing nitrogen-containing volatiles in other plant species
such as cucumber, lima bean, or gerbera (Dicke et al.,
1990; Takabayashi et al., 1994; Krips et al., 1999; Irmisch
et al., 2014). Nitrogen-containing compounds including
aldoximes, nitriles, and methylbutyraldoximes, phenylac-
etaldoxime, methylbutyronitriles, benzyl cyanides, and
phenylnitroethanes have been detected in the volatile
blends of many cottonwood species including Populus
trichocarpa, P. trichocarpa, P. nigra, and P. canescens
in response to attack from insects such as gypsy moth
caterpillars (Lymantria dispar) (Arimura et al., 2004;
Danner et al., 2011; Irmisch et al., 2013; Clavijo
McCormick et al., 2014; Irmisch et al., 2014). Electro-
physiological and behavioural experiments suggest that
nitrogenous compounds are key attractants for parasitic
Hymenopterans (Smid et al., 2002; Wei & Kang, 2006;

C 2016 Institute of Zoology, Chinese Academy of Sciences, 25, 2–23
Indirect plant defense against insects 9
Wei et al., 2007; Kugimiya et al., 2010; Ngumbi et al.,
2010; Clavijo McCormick et al., 2014).
Volatile indoles
Indole and indole-alkaloid molecules also contain ni-
trogen, but the nitrogen contained in them is present in
the pyrrole ring rather than as an independent, charac-
teristic group in the nitrogenous compounds described
in the previous section. Indoles have been detected after
an insect attack in many plant species, including maize
(Turlings et al., 1990; Alborn et al., 1997; Turlings &
Benrey, 1998; Frey et al., 2000), rice (Yuan et al., 2008;
Zhuang et al., 2012), gerbera (Krips et al., 1999), lima
bean (Dicke et al., 1999; de Boer et al., 2004), and cotton
(McCall et al., 1993). Indoles have also been detected in
plants treated by the elicitor volicitin (Frey et al., 2000).
The effect of indoles on natural enemies of herbivorous
insects is very specific to different species under differ-
ent conditions. In the laboratory, the blend of indoles
and terpenoids released by plants after being attacked
by lepidopteran larvae are attractive to the endoparasitic
wasp Cotesia marginiventris (Turlings & Berney, 1998).
However, indoles alone are not effective in attraction of
this parasitic wasp, nor to Braconid wasps (D’Alessandro
et al., 2006). On the other hand, indoles alone can attract
big-eyed bug (Geocoris) predators and some species of
Micro-Hymenoptera (James, 2005). In addition to their
roles in attracting natural enemies directly, indoles also
play roles in regulating emission of other volatiles. In
maize plants, indole emission precedes the release of other
volatiles by more than 2 h, and the release of indoles is
essential for priming the synthesis of mono- and homoter-
penes in the attacked plants, suggesting that indoles may
act as a potent aerial priming agent that prepares other tis-
sues and neighboring plants for incoming insect attacks
(Erb et al., 2015).
Fatty acid derivatives (also called green-leaf volatiles)
Fatty acid derivatives are common volatiles in plants
and are often referred to as green-leaf volatiles be-
cause they impart the typical odor of green leaves
(Ramachandran et al., 1991; Avdiushko et al., 1995;
Ruther, 2000; Dicke & van Poecke, 2002; Kessler&
Baldwin, 2002; Pichersky et al., 2006; Shiojiri et al.,
2006; Pinto et al., 2007; Christensen et al., 2013; Clavijo
McCormick et al., 2014). Green-leaf volatiles are emitted
at elevated levels when leaf tissues are disrupted. Mul-
tiple pathways can lead to the production of green-leaf
volatiles. C18 unsaturated fatty acids, such as linoleic
acid and linolenic acids released from plasma membranes
10 Z. Aljbory & M. S. Chen
due to cell damage (Feussner & Wasternack, 2002), are
oxidized and decarboxylated by hydroperoxide lyases, re-
sulting in the production of volatiles C6-aldehydes, C6-
alcohols and esters such as (Z)-3-hexen-1-yl acetate (18,
19) (Paré & Tumlinson, 1999). Green-leaf volatiles can
also be produced through lipoxygenases via the oxylipin
pathway in many plants (Grimes et al., 1992; Melan et al.,
1993; Avdiushko et al., 1995).
In early literature, green-leaf volatiles are thought to
be a general wound signal that is lacking any herbivore-
specific information. However, recent studies demon-
strate that green-leaf volatiles are emitted in response to
artificial damage as well as herbivory (Dicke et al., 1990;
Turlings et al., 1990; Mattiacci et al., 1994; James, 2005;
Allmann & Baldwin, 2010). The application of M. sexta’s
oral secretions to the wounds of wild-type N. attenuata
plants leads to a remarkable change in composition by de-
creasing in the (Z)/(E) isomers ratio in green-leaf volatile
emission, resulting in increased foraging efficiency of
predators in nature (Allmann et al., 2010; Allmann &
Baldwin, 2010). Unlike other HIPVs, green-leaf volatiles
are released immediately (within minutes) upon herbi-
vore damage. Indole emission started 45 min after elic-
itation and reached a peak at 180 min. Terpenoid emis-
sion started 180 min after elicitation (Erb et al., 2015).
Therefore, green-leaf volatiles likely provide rapid infor-
mation about the exact location of a feeding herbivore
(Gouinguené et al., 2005; James & Grasswitz, 2005; Zhu
et al., 2005; Chen & Fadamiro, 2007; Yu et al., 2008). Ear-
lier emission of green-leaf volatiles in herbivore-attacked
plants are able to induce the emission of other herbivore-
induced plant volatiles and therefore may play a potential
role in intra- and interplant signaling (Ruther & Fürstenau,
2005; Karban et al., 2006; Frost et al., 2008; Allmann &
Baldwin, 2010). Exposure of plants to synthetic green-
leaf volatiles induces rapid production of JA and emis-
sion of sesquiterpene in maize (Engelberth et al., 2004;
Farag et al., 2005; Ruther & Kleier, 2005; Engelberth
et al., 2007; Ton et al., 2007), activates the transcription
of the genes involved in the biosynthesis of ethylene in
lima bean (Arimura et al., 2001; Arimura et al., 2002),
and triggers the emission of local and systemic terpenes
in tomato (Farag & Pare, 2002). Genetic mutants with
impaired lox10 lead to significant reductions in emission
of herbivore-induced plant volatiles and in attractiveness
to parasitoids (Christensen et al., 2013).
Genetic engineering is apparently 1 way to develop
plants with high levels of volatiles that can attract nat-
ural enemies. However, care must be taken regarding to
potential fitness penalty by constitutively expressing pro-
teins that produce volatile chemicals. Elevated levels of
volatiles could also have negative impact on plant phys-

C 2016 Institute of Zoology, Chinese Academy of Sciences, 25, 2–23
iology directly. Alternatively, a blend of volatiles can be
produced industrially and applied to the field prior to
outbreaks of insect pests in an extended release format
(Sharma et al., 2015). In either case, a fully understanding
of composition and efficacy of volatile blends is needed
for a specific insect under a specific environment.
Natural enemies of herbivores involved
in indirect defense
Natural enemies of herbivorous insects using plant
volatiles as cues to find their prey can be broadly divided
into 2 categories, predators and parasitoids (Turlings &
Wäckers, 2004; Mumm & Dicke, 2010). Identified nat-
ural enemies in literature are very diverse, belonging to
5 orders of insects, mites, and nematodes (Dicke, 1999;
Clavijo McCormick et al., 2012; van Poecke & Dicke,
2004). These identified natural enemies may just repre-
sent a small proportion of carnivores in natural ecosys-
tems.
Predators
So far 24 species of predators from 12 families of
insects and mites have been found to be attracted by
volatiles emitted from plants damaged by various insect
herbivores or artificial blend of volatiles (Table S1). The
families of attracted predators include Chrysopidae, Miri-
dae, Geocoridae, Anthocoridae, Syrphidae, Empididae,
and Coccinellidae (Flint et al., 1979; Flint et al., 1981;
Reddy, 2002; James & Price, 2004; James, 2003, 2005;
Hagenbucher et al., 2013). The most commonly ob-
served predators attracted by volatiles are lady beetles,
including Stethorus punctum, S. gilvifrons, Coccinella
septempunctata, Chilocorus kuwanae, and Aiolocaria
hexaspilota; and predatory mites, including Phytoseiulus
persimilis, Amblyseius andersoni, A. finlandicus, A. cali-
fornicus, and A. womerleyi (Table S1) (Dicke & Sabelis,
1988; Dicke, 1999; Krips et al., 2001; Horiuche et al.,
2003; van den Boom et al., 2004). Other observed
predators included minute pirate bug, bigeyed bug, frit
fly, predatory thrips, predatory bug, plant bug, green
lacewings, 2-lined collops, and 2-spotted stink bug (Flint
et al., 1979; Rapusas et al., 1996; Venzon et al., 1999;
James, 2003; Hagenbucher et al., 2013). The effectiveness
of individual predator species for controlling specific pest
insects remains to be examined.
Parasites
A total of 34 parasitic wasp species belonging to
10 families have been reported to be attracted by

volatiles emitted from plants infested by insect herbivores
(Table S2). The families of attracted parasitic wasps in-
cluded Braconidae, Mymaridae, Pteromalidae, Scelion-
idae, Eulophidae, Aphelinidae, Ichneumonidae, Figiti-
dae, Encyrtidae, Aphidiidae. Among them, parasites from
the family Braconidae (Hymenoptera), especially Cote-
sia spp., are the most commonly attracted parasites by
volatiles emitted from plants attacked by lepidopterans,
coleopterans, aphids, and some dipterans (Turlings et al.,
1990; Turlings & Wäckers, 2004; Bruinsma et al., 2009;
Poelman et al., 2009; Girling et al., 2011). Parasites
from other hymenopteran families have also been ob-
served to be attracted to insect-damaged plants (Nadel
& Alphen, 1987; Finidori-Logli et al., 1996; Pettersson,
2001a; Hilker et al., 2002; Lou & Cheng, 2003; Colazza,
2004; Snoeren et al., 2010). In addition to hymenopter-
ans, parasitic dipterans have been reported to be attracted
to artificially damaged plants (Hanyu et al., 2009, 2011),
or sticky traps with blends of synthetic volatiles as well
(James, 2005). Future research should focus on the effi-
cacy of specific parasites, effective distances and effec-
tive concentrations of plant volatile blends for parasite
attraction.
Noninsecta invertebrates
Noninsecta invertebrates are also attracted to plant
volatiles. Two species of parasitoid nematodes, Het-
erorhabditis megidis and H. bacteriophora, have been
reported to reduce population size of western corn
rootworm Diabrotica virgifera virgifera (Coleoptera:
Chrysomelidae) in responding to corn emissions (Ras-
mann & Turlings, 2008). H. bacteriophora is in-
volved in below-ground defense of common milk-
weed (Asclepias syriaca) against attack from the root-
boring beetle Tetraopes tetraophthalmus (Rasmann et al.,
2011).
Omnivores
Some predator mites, such as mites from the families
Tydeidae and Phytoseiidae, are able to feed on different
types of food under different conditions. When prey den-
sity is low, these predators can survive by feeding on al-
ternative foods, such as foliar pathogenic fungi and some-
times pollen (Duso et al., 2005; Pozzebon et al., 2009).
Plants damaged by insect herbivores are vulnerable to sec-
ondary infections from fungi. Omnivores such as preda-
tor mites attracted to the damaged plants are beneficial in
tritrophic interactions (Norton et al., 2000; English-Loeb
et al., 2005, 2007; Tempfli et al., 2015).

C 2016 Institute of Zoology, Chinese Academy of Sciences, 25, 2–23
Indirect plant defense against insects 11
Inducible constitutive traits in indirect plant
defense
Many plant traits are expressed constitutively, but also
inducible under certain conditions. In many cases, these
inducible constitutive traits are for multiple functions. A
few examples for these inducible constitutive traits are
extrafloral nectar, food bodies, and domatia (Turlings &
Wäckers, 2004; Heil, 2008).
Extrafloral nectar
Extrafloral nectar is an aqueous solution containing
sugars and amino acids which is secreted from extrafloral
nectary organs (Koptur, 1992). Extrafloral nectar has been
observed on shoots, leaves, and inflorescences of plants
in more than 1000 plant species (Koptur, 1992; Wäckers
et al., 2001; Turlings & Wäckers, 2004). Extrafloral nec-
tar attracts both predators and parasitoids (Heil & McKey,
2003). Most plants excrete some extrafloral nectar re-
gardless the presence of herbivores (Turlings & Wäckers,
2004). The baseline secretion of this constitutive nectar
allows plants to harbor and nourish some natural enemies
(Wäckers et al., 2001). On the other hand, extrafloral nec-
tar can be induced to a much higher level in the presence
of herbivores (Heil et al., 2001; Wäckers et al., 2001;
Huntzinger et al., 2004; González-Teuber & Heil, 2009),
in response to mechanical damage (Mondor & Addicott,
2003), and by exogenous JA application (Heil et al., 2001;
Heil et al., 2004; Kost & Heil, 2005, 2008). Parasites fed
on extrafloral nectar have significantly higher reproduc-
tion rates and live much longer (Röse et al., 2006).
Extrafloral nectars are often used in combination with
other defense mechanisms (Arimura et al., 2005). In
lima bean, both volatile emission and extrafloral nec-
tars secretion increase when plants are exposed to exoge-
nous application of JA (Heil, 2004). Lima bean plants
treated with volatiles, including (Z)-3-hexenyl acetate,
and several other structurally related compounds; (E)-3-
hexenyl acetate, (E)-2-hexenyl acetate, 5-hexenyl acetate,
(Z)-3-hexenylisovalerate, and (Z)-3-hexenylbutyrate, also
secrete elevated levels of extrafloral nectars (Kost & Heil,
2008). Activation of both extrafloral nectars release and
volatile emission after herbivore attack is also common
in other plants from many plant taxa (Kost & Heil, 2006;
Choh et al., 2006). It is not clear if the increased release
of extrafloral nectars is activated by herbivore attack di-
rectly, or as secondary effect activated through emitted
volatiles. Plant leaves receiving airborne volatiles can in-
crease extrafloral nectars secretion in the same plant (Heil
& Silva Bueno, 2007) and in neighboring plants of the
same species (Kost & Heil, 2006).
12 Z. Aljbory & M. S. Chen
Food body (pearl body)
Composition of nutrients contained in food bodies on
different plants vary, but polysaccharides, lipids, and pro-
teins are common components (O’Dowd, 1982; Silva &
Machado, 1999; Heil et al., 2004; Webber et al., 2007;
Paiva et al., 2009). Like extrafloral nectar, food bodies
can attract and provide food for ants and other natural
enemies of herbivores (Turlings & Wäckers, 2004).
Domatia
Domatia are small morphogenetic hollow structures on
plants and can serve as shelters for mites and other arthro-
pods (Norton et al., 2000; Heil & McKey, 2003; Romero
& Benson, 2004, 2005). In return, mites and other arthro-
pods living in domatia provide benefit to the plants by
removing spores and hyphae of pathogenic fungi and by
preying on phytophagous mites and other harmful arthro-
pods (O’Dowd & Willson, 1997; Norton et al., 2000;
Romero & Benson, 2004, 2005; Duso et al., 2005; Zemek,
2005; English-Loeb et al., 2005, 2007; Monks et al., 2007;
Pozzebon et al., 2009; O’Connell et al., 2015; Tempfli
et al., 2015). Most arthropod species living in domatia
are mites and ants, even though other arthropods such as
thrips may also take the advantage of the protection of-
fered by this structure (Monks et al., 2007; O’Dowd &
Willson, 1997).
Future perspective
The benefit of utilizing indirect plant defense to control
herbivores is obvious, including cost effectiveness and the
lack of environmental pollution. Several attributes in in-
direct plant defense are advantageous for widespread pest
control. These attributes include communication among
plants in perceiving and propagating defense signals,
common components in volatile blends for the attraction
of different natural enemies, and common types of elici-
tors. Yet, there are few successful stories in utilization of
indirect defense in plants to suppress herbivore damage.
The lack of success in utilizing indirect defense in pest
control is likely due to our very limited understanding
of the complex interactions among components involved
in indirect plant defense. In a natural ecological system,
plants face numerous challenges to survive and prosper,
and have optimized strategies to fight against these chal-
lenges through co-evolution with interacting abiotic and
biotic challengers. Inducible indirect defenses are evolved
in plants to fight against herbivorous pests effectively with
minimum metatolic cost. The chemicals and pathways in-
volved in inducible defense often have other functions in

C 2016 Institute of Zoology, Chinese Academy of Sciences, 25, 2–23
plant physiology. Any effort to achieve success in manipu-
lating plant defense pathways to suppress herbivore dam-
age needs a comprehensive understanding of the impact of
these pathways on herbivores, natural enemies, and plants
themselves. Fortunately, researches in biology and ecol-
ogy have arrived at a revolutionary turning point due to
recent advances in technologies of genomics, proteomics,
gas chromatography mass spectrometry, high throughput
production and testing of various types of chemicals, wide
area monitoring system, and instant online communica-
tion. The availability of these advanced technologies will
accelerate global, systematic, and integrated research on
various aspects involved in indirect plant defense, leading
to better understanding of the interactions among plants,
herbivores, and natural enemies. A better understanding
of global and componential aspects on indirect plant de-
fense provides necessary conditions for its utilization in
pest management.
Disclosure
The authors have declared that they have no conflicts of
interesting.
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Manuscript received October 4, 2016
Final version received December 6, 2016
Accepted December 20, 2016
Supporting Information
Additional Supporting Information may be found in the
online version of this article at the publisher’s web-site:
Table S1. Predators attracted by volatiles emitted by
plants after insect damage or by artificial blends of
volatiles.
Table S2. Parasites attracted by volatiles emitted by
plants after insect damage or by artificial blends of
volatiles.
References cited in the Supplementary Tables.