Stahl Et Al., 2018 Agroecología Interacciones Plantas Artrópodos Herbivoría MIP

The Plant Journal (2018) 93, 703–728 doi: 10.1111/tpj.
13773
SI PLANT BIOTIC INTERACTIONS
Plant–arthropod interactions: who is the winner?

Elia Stahl, Olivier Hilfiker and Philippe Reymond*
Department of Plant Molecular Biology, University of Lausanne, Biophore Building, 1015 Lausanne, Switzerland
Received 13 September 2017; revised 27 October 2017; accepted 31 October 2017; published online 20 December 2017.
*For correspondence (e-mail [email protected]).
SUMMARY
Herbivorous arthropods have interacted with plants for millions of years. During feeding they release chemi-
cal cues that allow plants to detect the attack and mount an efficient defense response. A signaling cascade
triggers the expression of hundreds of genes, which encode defensive proteins and enzymes for synthesis
of toxic metabolites. This direct defense is often complemented by emission of volatiles that attract benefi-
cial parasitoids. In return, arthropods have evolved strategies to interfere with plant defenses, either by pro-
ducing effectors to inhibit detection and downstream signaling steps, or by adapting to their detrimental
effect. In this review, we address the current knowledge on the molecular and chemical dialog between
plants and herbivores, with an emphasis on co-evolutionary aspects.
Keywords: arthropods, plant defense signaling, elicitors, effectors, defense metabolites, co-evolution, arms
race.
INTRODUCTION
Plants and herbivorous arthropods have co-evolved for Will and van Bel, 2006; Howe and Jander, 2008; Wu and
millions of years, and it is commonly believed that these Baldwin, 2010; Hogenhout and Bos, 2011; Farmer, 2014;
interactions have generated the large variety of plant and Jaouannet et al., 2014; Hilker and Fatouros, 2015; Schuman
arthropod species that inhabit our planet. Although a large and Baldwin, 2016). In this review, we place emphasis on
fraction of arthropods provide service to plants in the form the molecular and chemical dialog that underlies these
of pollination or protection against enemies, they also con- interactions. We present the current knowledge on arthro-
stitute a threat as they are generally herbivorous. Whether pods elicitors and effectors, provide examples of plant
they chew leaf or root material, feed on cell content, mine defense compounds and adaptations by arthropods, to
mesophyll tissue or suck phloem, arthropods from differ- illustrate a fascinating co-evolution between organisms
ent feeding guilds impose a stress that plants have to that are generally foes but can also engage in mutualistic
resist. Depending on the type of attack, plants have a bat- relationships.
tery of strategies that include preexisting constitutive
PERCEPTION OF FEEDING HERBIVORES
defenses complemented by the induction of direct (toxic
secondary metabolites and proteins) and indirect (emission Plants have evolved exquisite ways to detect their ene-
of volatiles to attract predators) defenses (Figure 1. These mies. When infected by bacterial or fungal pathogens,
responses depend on precise perception of the aggressor, hosts recognize pathogen-derived molecules from the
followed by a signal transduction cascade that culminates attacker that have been termed pathogen-associated
in a transcriptional reprogramming and synthesis of speci- molecular patterns (PAMPs) or microbe-associated molec-
fic defense compounds. Efficient plant resistance imposes ular patterns. These PAMPs are highly conserved and are
a selection pressure on herbivores, which in turn develop generally associated with a class of attacker. PAMP percep-
ways to interfere with defense mechanisms or adapt to the tion is achieved by plasma membrane-bound pattern
detrimental effect of toxins. In recent years, a wealth of recognition receptors (PRRs), which are either receptor-like
information has accumulated on molecular components kinases (RLKs) or receptor-like proteins that lack a cytoplas-
that control this ongoing arms race. Several aspects of mic kinase domain (Boller and Felix, 2009; Couto and Zip-
plant–arthropod interactions have been reviewed else- fel, 2016). Upon ligand binding, PRRs associate with
where (Schoonhoven et al., 2005; Zhu-Salzman et al., 2005; regulatory receptor kinases, including the well-studied
© 2017 The Authors 703

The Plant Journal © 2017 John Wiley & Sons Ltd
704 Elia Stahl et al.
Figure 1. Overview of plant responses to herbivory.

Upon perception of herbivorous larvae or eggs,
plants activate direct defenses [synthesis of toxic
metabolites and proteins, localized cell death (HR)]
and indirect defenses (emission of volatiles to
attract larval or egg parasitoids and root nema-
todes). These responses occur both above- and
belowground. EIPVs, egg-induced plant volatiles;
Parasitoids HIPVs, herbivore-induced plant volatiles; HR, hyper-
sensitive-response.
HIPVs
HR
Defense compounds
EIPVs
Parasitoids
Direct defenses
Indirect defenses
ryophyllene
)-β-ca
(E
Nematodes
Defense compounds
BRI1-ASSOCIATED RECEPTOR KINASE 1 (BAK1; Couto and difficult for herbivores to eliminate them and hence avoid
Zipfel, 2016). PAMP recognition leads to a transcriptional recognition.
defense program called pattern-triggered immunity (PTI), One of the first and best-known examples is volicitin, a
which restricts growth of the invading pathogens through fatty acid–amino acid conjugate (FAC) purified from OS of
local and systemic production of defense proteins and the beet armyworm caterpillar Spodoptera exigua (Alborn
metabolites (Li et al., 2016). In analogy to plant–pathogen et al., 1997). When applied to maize leaves, volicitin trig-
interactions, scientists have identified herbivore-associated gers the emission of a bouquet of volatile terpenoids and
molecular patterns (HAMPs; Mitho € fer and Boland, 2008; indoles that attract parasitic wasps. Volicitin is composed
Bonaventure et al., 2011; Hogenhout and Bos, 2011; of 17-hydroxylinolenic acid coupled to glutamine. Interest-
Jaouannet et al., 2014; Acevedo et al., 2015), but knowl- ingly, chemical analysis established that linolenic acid orig-
edge about their corresponding PRRs is scarce. inates from the plant and is further hydroxylated and
conjugated to glutamine by the insect (Pare et al., 1998;
Arthropod-derived HAMPs
Lait et al., 2003). Volicitin and related FACs (fatty acids of
Initially termed ‘elicitors’ because they elicited defense different length and saturation coupled to glutamine or
responses from the plant, HAMPs have been found in a glutamate) were further identified in OS from different
variety of sources, including saliva, oral secretions (OS), Lepidoptera (Pohnert et al., 1999; Halitschke et al., 2001;
reproductive glands, whole body or eggs (Table 1). HAMPs Mori et al., 2003) and even in other insects (Yoshinaga
(like PAMPs) constitute essential patterns, making it et al., 2007). The physiological role of FACs is not yet clear,
© 2017 The Authors

The Plant Journal © 2017 John Wiley & Sons Ltd, The Plant Journal, (2018), 93, 703–728
Plant–arthropod interactions 705
Table 1 HAMPs and effectors from arthropods
Name Origin Response Reference
HAMPs
FAC (volicitin) Spodoptera exigua OS Volatiles attract parasitoids Alborn et al. (1997)
2-HOT Manduca sexta OS Volatiles attract parasitoids Gaquerel et al. (2009)
Caeliferins Schistocera americana OS Volatiles attract parasitoids Alborn et al. (2007)
b-Glucosidase Pieris brassicae OS Volatiles attract parasitoids Mattiacci et al. (1995)
Inceptin Spodoptera frugiperda OS Volatile and defense gene induction Schmelz et al. (2006)
Lipase Schistocera gregaria OS Release of esterified OPDA Scha€fer et al. (2011)
b-Galactofuranose Spodoptera littoralis OS Plasma membrane depolarization Bricchi et al. (2013)
polysaccharide
Bacterial porin-like Spodoptera littoralis OS Channel-forming activity Guo et al. (2013)
Protein (< 10 kDa) Myzus persicae saliva Defense gene induction de Vos and Jander (2009)
Mp56, Mp57, Mp58 Myzus persicae saliva Lower aphid fecundity Elzinga et al. (2014)
Bacterial GroEL Macrosiphum euphorbiae OS Lower aphid fecundity Chaudhary et al. (2014)
Phosphatidylcholine Sogatella furcifera female Production of ovicidal compound Yang et al. (2014)
12 kDa protein Diprion pini oviduct secretion Egg parasitoids attraction Hilker et al. (2005)
Benzyl cyanide Pieris brassicae ARG Arrest of egg parasitoids Fatouros et al. (2008)
Indole Pieris rapae ARG Arrest of egg parasitoids Fatouros et al. (2009)
Lipid extract Pieris brassicae eggs Defense gene induction, necrosis Bruessow et al. (2010)
Bruchin Callosobruchus maculatus female Neoplasm formation under eggs Doss et al. (2000)
Effectors
Modified inceptin Anticarsia gemmatalis OS Plant defense suppression Schmelz et al. (2012)
Bacteria (flagellin) Leptinotarsa decemlineata OS Inhibition of the JA pathway Chung et al. (2013)
Apyrase Helicoverpa zea saliva Lower defense gene expression Wu et al. (2012)
GOX Helicoverpa zea saliva Lower nicotine production Musser et al. (2002)
Unknown (< 3 kDa) Spodoptera littoralis, Pieris rapae OS Reduced defense gene expression Consales et al. (2012)
Unknown (10–30 kDa) Leptinotarsa decemlineata OS Reduced defense gene expression Lawrence et al. (2007)
Unknown Manduca sexta OS Reduced gene expression Schittko et al. (2001)
FACs Manduca sexta OS Reduced volatile emission Gaquerel et al. (2009)
Chitinases Spodoptera exigua frass Increased larval performance Ray et al. (2016)
MIF (cytokine) Acyrthosiphon pisum saliva Plant defense suppression Naessens et al. (2015)
Ca2+-binding protein Megoura viciae saliva Inhibition of sieve tube plugging Will et al. (2007)
Me23, Me10 (unknown) Megoura euphorbiae saliva Higher aphid fecundity Atamian et al. (2013)
Mp1 (unknown) Myzus persicae saliva Higher aphid fecundity, targets VSP52 Rodriguez et al. (2017)
Mp10 (CSP) Myzus persicae saliva Suppress ROS production Bos et al. (2010)
MpC002 (unknown) Acyrthosipho pisum saliva Higher aphid performance Mutti et al. (2008)
Mp55 (unknown) Myzus persicae saliva Higher aphid fecundity Elzinga et al. (2014)
Tu28, Tu84 (unknown) Tetranychus urticae heads Higher mite performance Villarroel et al. (2016)
F-box-LRR proteins Mayetiola destructor saliva Induce ETI in HF-resistant wheat Zhao et al. (2015)
Lipid extract Pieris brassicae eggs Inhibition of the JA pathway Bruessow et al. (2010)
ARG, accessory reproductive gland secretion; CSP, chemosensory protein; ETI, effector-triggered immunity; FAC, fatty acid–amino acid con-
jugate; GOX, glucose oxidase; GroEL, chaperone; HAMP, herbivore-associated molecular pattern; HF, Hessian fly; 2-HOT, 2-hydroxy-octade-
catrieonic acid; JA, jasmonic acid; LRR, leucine-rich-repeat receptor; MIF, migration inhibitory factor; OPDA, 12-oxo-phytodienoic acid; OS;
oral secretions; ROS, reactive oxygen species; VSP52, vacuolar protein sorting associated protein52.
but it has been suggested that they are important for nitro- tobacco Nicotiana attenuata. In plants, 2-HOT is produced
gen assimilation in larvae (Yoshinaga et al., 2008). In addi- from linolenic acid by the action of a-dioxygenases. Occur-
tion, the amphiphilic nature of these molecules might rence of 2-HOT in M. sexta OS may allow plants to sense
emulsify the ingested food. herbivore feeding by the presence of a modified mem-
Caeliferins are sulfated hydroxy fatty acids isolated from brane constituent (Gaquerel et al., 2009). Bruchins are fatty
OS of the grasshopper Shistocera americana. In maize, acid-derived long-chain a,x-diols, esterified at one or both
they elicit emission of volatiles similar to those triggered ends with 3-hydroxypropanoic acid. They were isolated
by volicitin, although there is no evidence for natural ene- from pea and cowpea weevil oviposition fluid and induce
mies of grasshoppers (Alborn et al., 2007). 2-Hydroxy tumor-like growth of undifferentiated cells (neoplasms) on
octadecatrieonic acid (2-HOT) was detected in OS of the pea pods, like naturally deposited eggs. Neoplasms serve
tobacco hornworm Manduca sexta, and triggers the emis- as direct defense by blocking larval entry (Doss et al.,
sion of the sesquiterpene trans-a-bergamotene in wild 2000). Eggs of the white-backed planthopper Sogatella
© 2017 The Authors

furcifera stimulate the production of the ovicidal substance unknown (de Vos et al., 2005; Abe et al., 2008; Kant et al.,
benzyl benzoate in certain rice varieties. Purification of 2008; Zhurov et al., 2014).
female extracts yielded active phospholipids, including Interestingly, recognition can be mediated through bacte-
phosphatidylcholine and phosphatidylethanolamine (Yang rial PAMPs that are present in OS. A porin-like protein from
et al., 2014). Finally, oviposition by the large white Pieris Ralstonia was purified from Spodoptera littoralis OS and
brassicae induces defense gene expression, local necrosis activated early defense responses, including channel forma-
and production of reactive oxygen species (ROS) in Ara- tion and calcium fluxes (Guo et al., 2013). The bacterial
bidopsis (Little et al., 2007). The inducing activity is found chaperonin GroEL was identified in saliva of the potato
in egg extracts from different insects and is enriched in the aphid Macrosiphum euphorbiae. This protein originated
lipid fraction (Bruessow et al., 2010). from the endosymbiont Buchnera aphidicola and induced
All the above examples seem to indicate that lipid- PTI responses that depended on BAK1 in Arabidopsis
derived HAMPs are prevalent in OS from chewing (Chaudhary et al., 2014). These two examples expand the
herbivores. However, known HAMPs also include proteins, range of potential sources of HAMPs to the gut microbiome.
peptides and small metabolites. A b-glucosidase in P. bras-
HAMP recognition by potential PRRs
sicae OS is responsible for volatile emission in cabbage
(Mattiacci et al., 1995), a lipase in the grasshopper Schisto- Strikingly, contrary to the case of bacterial and fungal
cera gregaria OS induces defense gene expression (Scha€fer PAMPs where direct binding to a PRR has been demon-
et al., 2011), and an uncharacterized 12-kDa protein from strated (Boller and Felix, 2009; Couto and Zipfel, 2016),
oviduct secretions of the sawfly Diprion pini induces vola- there is yet no evidence for a bona fide PRR that perceives a
tile emission in pine (Hilker et al., 2005). Inceptin is a pep- HAMP. However, M. persicae-derived HAMPs were shown
tide that originates from the digestion of plant proteins, to elicit defenses characteristic of PTI responses in a BAK1-
illustrating the ability of plants to detect feeding-dependent dependent manner (Prince et al., 2014; Vincent et al., 2017).
modification of self. This cyclic peptide of 11 amino acids These studies provide evidence for detection of aphid
was purified from OS of the fall armyworm Spodoptera fru- HAMPs by (unknown) PRRs that are distinct from PRRs that
giperda, and derives from proteolytic cleavage of a plant detect bacterial and fungal PAMPs (Prince et al., 2014).
chloroplastic ATPase in the insect mid-gut (Schmelz et al., More than a decade ago, a biochemical study using a radio-
2006). When applied to cowpea (Vigna unguiculata) or labeled form of volicitin reported binding to a plasma mem-
maize, inceptin induces the production of defense-related brane protein from maize leaves (Truitt et al., 2004).
hormones, volatiles and defense compounds. Small However, this protein has not been further characterized
metabolites include, for example, benzyl cyanide and indole and no gene has been cloned. A cluster of three lectin
from reproductive accessory glands of P. brassicae and receptor kinase (LecRK) genes conferred resistance to the
Pieris rapae, respectively. They are associated with eggs brown planthopper (BPH) in rice, but whether these LecRK
and induce indirect plant defense by arresting egg para- bind to yet unknown HAMPs from BPH or mediate down-
sitoids at the oviposition site (Fatouros et al., 2008, 2009). stream events is unknown (Liu et al., 2015). Arabidopsis
The feeding mode and physiology of phloem-sucking LecRK-I.8 is involved in the perception of egg-derived
aphids have rendered HAMPs isolation difficult. Aphids HAMPs. Indeed, a lecRK-I.8 mutant displayed a significantly
deliver minute amounts of saliva with their syringe-like sty- reduced expression of the defense gene PR1 in response to
let when probing and navigating through different cell lay- egg extract treatment (Gouhier-Darimont et al., 2013). This
ers to reach sieve elements. Proteomic and genomic interesting observation will however await chemical identi-
analyses of secreted proteins from the green peach aphid fication of the lipid-derived HAMP and binding assays.
Myzus persicae salivary glands have nevertheless identi- Recently, a LecRK receptor for extracellular ATP was dis-
fied candidate HAMPs that induced defense gene expres- covered in Arabidopsis. DORN1 (LecRK-I.9) bound ATP
sion or lowered aphid fecundity when overexpressed in with high affinity and ectopic expression triggered plant
Arabidopsis (Table 1; de Vos and Jander, 2009; Elzinga responses associated with wounding. It was concluded
et al., 2014). In addition, Thrips and phytophagous mites that DORN1 may mediate perception of feeding herbivores
have different feeding mode than chewing herbivores or by detecting ATP liberated from cell content after physical
aphids. Although they belong to different classes (insects damage (Choi et al., 2014). Although ATP is not formerly a
or arachnids), both pierce plant tissues and feed on cell HAMP but rather a damage-associated molecular pattern
content. The Western flower thrips Frankliniella occiden- (DAMP), this finding reinforces the hypothesis that LecRKs
dalis and the two-spotted spider mite Tetranychus urticae may be important components of HAMP perception.
have been used as a model to study Arabidopsis and
Wound responses
tomato plant defenses. Whereas transcriptional changes
similar to those induced by lepidopteran herbivores were It has long been recognized that wounding is an important
observed, the nature of the eliciting activity is still component of plant responses to chewing herbivores
© 2017 The Authors

(Green and Ryan, 1972; Howe and Jander, 2008). Early ROS and MAPK are also involved in plant responses to
work in Solanaceae identified systemin, an 18-aa polypep- pathogens, how they specifically trigger anti-herbivore
tide wound signal that regulates the production of anti- defense is currently unknown. For oviposition, there is little
insect proteinase inhibitors (for review, see Ryan and information on early signaling steps; however, ROS accu-
Pierce, 1998). Although some early responses to herbivory mulation under eggs has been reported (for review, see
are not or only partially mimicked by mechanical damage Reymond, 2013; Hilker and Fatouros, 2015). Following early
(Bricchi et al., 2010) and emission of volatiles is specifically responses to arthropods, alteration in hormonal profile
triggered by insect-derived cues (Alborn et al., 1997), plays a crucial role. JA is the predominant signal that regu-
wounding and feeding activate overlapping sets of genes lates downstream defense steps. Depending on the
(Reymond et al., 2000; Major and Constabel, 2006). In addi- attacker and its developmental stage, a role for salicylic
tion, jasmonic acid (JA), the main signal controling acid (SA), ethylene (ET) and other plant hormones as pri-
defenses (see below), rapidly accumulates in response to mary signals or modulators has also been reported.
mechanical damage (Reymond et al., 2000; Glauser et al.,
JA pathway
2008). For aphids, turgor changes associated with stylet
penetration of the phloem may also contribute to some A large body of literature has detailed the importance of
defense responses, like for instance the rapid plugging of the JA pathway in response to necrotrophs and herbivores
sieve plates by callose or protein aggregates (reviewed in (Howe and Jander, 2008; Browse, 2009; Acosta and Farmer,
Will and van Bel, 2006). 2010; Wu and Baldwin, 2010; Pieterse et al., 2012). In brief,
Because many studies on the role of HAMPs involve upon damage fatty acids are released from plastidic galac-
exogenous application of OS on wounded leaves, conclu- tolipids. 13-Lipoxygenases oxygenate 18:3 and 16:3 fatty
sions from such experiments have to be assessed critically. acids to produce hydroperoxides, which are further con-
Future experiments aiming at removing HAMPs genetically verted by allene oxide synthase and allene oxide cyclase to
or physically from the herbivore, as in the case of salivary 12-oxo-phytodienoic acid (OPDA) and dinor-oxo-phytodie-
gland ablation (Musser et al., 2002), will be necessary to noic acid (dnOPDA), respectively. OPDA and dnOPDA are
demontrate the specific role of these elicitors. transferred to peroxisomes where they are reduced by
OPDA reductase 3 (OPR3) and subjected to a series of
Open questions
b-oxidation cycles to yield JA (Acosta and Farmer, 2010).
In several cases, the defense-inducing activity of HAMPs is Conjugation with Ile by the enzyme JAR1 in the cytosol
associated with crude extracts or unknown proteins, but generates the bioactive (+)-7-iso-JA-Ile (JA-Ile; Staswick
their exact chemical nature is unknown. For most HAMPs, and Tiryaki, 2004; Fonseca et al., 2009). After importation
information on their role in arthropod biology is lacking. into the nucleus, JA-Ile forms a complex with its receptor,
This role must be essential since HAMPs have been kept the F-box CORONATINE INSENSITIVE 1 (COI1) and a
although they alert the plant about the attack. In addition, JASMONATE-ZIM DOMAIN PROTEIN (JAZ). This leads to
genes responsible for HAMP synthesis need to be identi- ubiquitination and degradation of the JAZ proteins by the
fied. Host specificity and distribution in different arthropod proteasome. JAZs are repressors of transcription factors,
taxa should also be addressed. For instance, FACs have a including the Arabidopsis bHLH MYC2, MYC3 and MYC4,
broad-range activity but do not elicit volatile emission in which control JA-dependent responses additively (Chini
lima bean and cotton (Spiteller et al., 2001; Schmelz et al., et al., 2007; Thines et al., 2007; Browse, 2009; Fernandez-
2009). Inceptin action is restricted to Fabaceae, while Ara- Calvo et al., 2011; Figure 2). In Arabidopsis, transcriptome
bidopsis only responds to caeliferins (Schmelz et al., 2009). analyses revealed that herbivory alters the expression of
Finally, there is a clear lack of knowledge on potential hundreds of genes, and that a majority of these genes are
PRRs, and efforts should be placed in finding ligand/bind- regulated by COI1 and MYC2/3/4 (Reymond et al., 2004; de
ing pairs and defining downstream steps to establish if Vos et al., 2005; Schweizer et al., 2013a,b). As a conse-
plants use the same molecular machinery to detect HAMPs quence, coi1-1 and myc234 mutants were significantly
and PAMPS. more susceptible to herbivory by the generalist herbivore
S. littoralis (Fernandez-Calvo et al., 2011; Schweizer et al.,
SIGNALING
2013b). In addition, the role of the JAZ1/3/4/9/10-MYC2/3/4
Upon feeding, early signaling events include membrane Arabidopsis module in resistance against the generalist
depolarization, Ca2+ influx, production of ROS and activa- Trichoplusia ni was recently demonstrated (Major et al.,
tion of mitogen-activated protein kinases (MAPK; Howe 2017).
and Jander, 2008; Wu and Baldwin, 2010; Vincent et al., That the JA pathway is central to resistance against
2017). These fast responses have been observed in differ- arthropods in plants was demonstrated using mutants. An
ent plant species, and thus seem to constitute a general original study using the Arabidopsis fad3–2 fad7–2 fad8 tri-
mechanism to transduce HAMP perception. Because Ca2+, ple mutant deficient in the jasmonate precursor linolenic
© 2017 The Authors

(a) (b)
? ?
HAMPs HAMPs
RLK
peroxiso RLK
me
OPDA OPR3 EDS1 PAD4
t
las 18:3 β-ox
op t
r
JA ICS1
chlo
as
LOX AOS AOC
chloropl
O2-
JAR1 us
OPDA C2B59B
SA cle
nu
s JA-Ile NPR1
leu H2O2 TFs
nuc
COI1
SCF
JAZs NPR1
MYC2,3,4 Δ redox
NPR1
Glucosinolates HR PR-1 Pip
Cell death SAR
Figure 2. Signaling of plant responses to herbivory in Arabidopsis. Current model for signaling steps activated by feeding larvae (a) and oviposition (b). (a)
Upon recognition of HAMPs from larval oral secretions by yet unknown receptors, a signal transduction cascade generates the bioactive hormone JA-Ile. JA-Ile
induces the interaction of SCFCOI1 with JAZs transcriptional repressors, which are further ubiquitinated and degraded. MYC2,3,4 can then regulate the transcrip-
tion of numerous genes, including glucosinolate biosynthesis genes. (b) Egg-derived HAMPs are perceived by yet unknown receptors, which trigger both ROS
accumulation and activation of SA-biosynthesis enzyme ICS1 through lipase-related EDS1 and PAD4. SA accumulation provokes a redox change that leads to
monomerization of NPR1, entry in the nucleus and activation of transcription factors. Expression of PR-1 is associated with a HR-like response that culminates in
localized cell death, presumed to inhibit egg development. In addition, local and distal accumulation of Pip is mediated by the biosynthesis enzyme ALD1 and
triggers inhibition of infection by biotroph pathogens in local and distal tissues through SAR. There is evidence for a general conservation of both models in
other plant species. HAMPs, herbivore-associated molecular patterns; RLK, receptor-like kinase; LOX, lipoxygenases; AOS, allene oxide synthase; AOC, allene
oxide cyclase; OPDA, 12-oxo-phytodienoic acid; OPR3, OPDA-reductase 3; b-ox., b-oxidation; JA, jasmonic acid; JAR1, jasmonate-resistant 1; JA-Ile, jasmonate-
isoleucine; SCFCOI1, SCF complex with F-box coronatine-insentive 1 receptor for JA-Ile; JAZs, jasmonate-ZIM domain proteins; MYC2,3,4, MYC2, MYC3, MYC4
bHLH transcription factors; EDS1, enhanced-disease susceptibility 1; PAD4, phytoalexin-deficient 4; ICS1, isochorismate synthase 1; SA, salicylic acid; NPR1,
non-expressor of pathogenesis-related genes1; TFs, transcription factors; HR, hypersensitive response; PR-1, pathogenesis-related 1; Pip, pipecolic acid; SAR,
systemic acquired resistance; ROS, reactive oxygen species.
acid showed that it was highly susceptible to larvae of the water weevil Lissorhoptrus oryzophilus (Lu et al., 2015); in
saprophagous fungal gnat, Bradysia impatiens (McConn maize, mutants of OPR7 and OPR8, two close homologs of
et al., 1997). Loss of function of the COI1 homolog in OPR3, were more susceptibile to S. exigua (Yan et al.,
tomato increased susceptibility to the two-spotted spider 2012); the tomato jasmonate biosynthesis mutant def-1
mite T. urticae (Li et al., 2004b), and to the lepidopteran that is impaired in volatile emission did not attract preda-
herbivores M. sexta (Chen et al., 2005) and T. ni (Herde tory mites when infested with T. urticae, indicating that the
and Howe, 2014). Silencing COI1 in N. attenuata improved JA pathway is also essential for indirect defense (Ament
performance of M. sexta and the stem weevil Trichobaris et al., 2004). For aphids, Ellis et al. (2002) showed that Ara-
mucorea (Paschold et al., 2007; Diezel et al., 2011); the sil- bidopsis mutants with constitutive activation of JA-signal-
verleaf whitefly Bemisia tabaci accelerated nymphal devel- ing were more resistant to M. persicae.
opment on Arabidopsis coi1-1 (Zarate et al., 2007); the
Other hormones
isopod crustacean Porcellio scaber completely devoured
Arabidopsis aos, whereas wild-type plants remained intact The SA pathway is generally important to fend off
(Farmer and Dubugnon, 2009); silencing LOX and AOC in biotrophic pathogens, and plays a major role in PTI/effec-
rice plants increased root herbivory by the generalist tor-triggered immunity (ETI; Pieterse et al., 2012). SA is a
cucumber beetle Diabrotica balteata and the specialist rice phenolic compound that is mainly synthesized from the
© 2017 The Authors

precursor chorismate by ISOCHORISMATE SYNTHASE 1 require a functional SA pathway (Gouhier-Darimont et al.,

(ICS1/SID2). Activation of the lipase-like protein 2013; Figure 2).
ENHANCED DISEASE SUSCEPTIBILITY 1 (EDS1) and its Ethylene is a modulator of SA and JA pathways. For
related interacting partner PHYTOALEXIN DEFICIENT 4 instance, the ET pathway has a synergistic effect on the JA
(PAD4) by biotrophic pathogens trigger SA accumulation pathway to fight necrotrophic pathogens, or acts with
(Vlot et al., 2009). Consequently, change in the redox state NPR1 to enable SA antagonistic action on the JA pathway
of the cell redirects the transcriptional coactivator NON (for review, see Pieterse et al., 2012). Information on the
EXPRESSOR OF PR GENES 1 (NPR1) from the cytosol to role of ET against arthropods is, however, incomplete or
the nucleus, where it regulates expression of numerous inconclusive. The ET-insensitive Arabidopsis mutant ein2-1
defense genes, including the SA marker gene PR-1 (Vlot is more resistant to S. littoralis feeding (Stotz et al., 2000;
et al., 2009; Pieterse et al., 2012). Bodenhausen and Reymond, 2007). On the contrary, inhibi-
The role of the SA pathway in resistance to arthropods tion of ET perception in maize enhances feeding by S. fru-
has received some attention. Aphid feeding induced giperda (Harfouche et al., 2006). Treatment with HAMPs
expression of SA-marker genes, but no SA accumulation induced ET production in different plant species (Schmelz
was observed and studies with SA-pathway mutants in et al., 2009). Similarly, FACs elicited ET burst in N. attenu-
Arabidopsis generated contrasting data on arthropod per- ata and this prevented SA accumulation, hence reducing a
formance (for review, see Jaouannet et al., 2014). For potential inhibitory effect of SA on the JA pathway (Diezel
example, in one study (Mewis et al., 2005), npr1 and NahG et al., 2009). Whitefly-induced interference of parasitoid
were less susceptible to the green peach aphid M. persi- attraction triggered by Plutella xylostella feeding was abol-
cae, whereas this difference was not found by Pegadaraju ished in ein2-1 (Zhang et al., 2013). Finally, inhibition of
et al. (2005). However, pad4 showed increased perfor- the JA pathway after P. brassicae oviposition-induced SA
mance to M. persicae, but this effect was independent on accumulation in Arabidopsis is dependent on both NPR1
EDS1 (Pegadaraju et al., 2005, 2007). By suppressing PAD4 and EIN2 (Schmiesing et al., 2016).
expression, BOTRYTIS-INDUCED KINASE1 (BIK1) was also Involvement of abscisic acid (ABA), auxin, gibberellins,
shown to confer enhanced susceptibility to M. persicae, brassinosteroids and cytokinins in response to herbivory
indicating that this PTI modulator and target of BAK1 acted has been adressed in several studies (for review, see Erb
as a negative regulator of the plant defense to aphids (Lei et al., 2012). The emerging picture is that these hormones
et al., 2014). Finally, M. persicae infestation triggered a primarily act as modulators of the JA pathway and thus do
transient trehalose accumulation in Arabidopsis, which not play a direct role in defense (for review, see Erb et al.,
was shown to enhance PAD4 expression (Singh et al., 2012).
2011). PAD4 seems thus to constitute an important compo-
Systemic responses
nent mediating defense against aphids, but its connection
to the SA pathway remains elusive (Louis and Shah, 2015). Evidence for a long-distance activation of defenses in
For chewing herbivores, S. littoralis larvae were smaller response to herbivory has accumulated over years. It
when feeding on ics1 and npr1-1, implying a negative role requires activation of the JA pathway in local and distal tis-
of SA (Stotz et al., 2002; Bodenhausen and Reymond, 2007). sues, but the nature of the systemic signal (hydraulic,
Because the SA pathway is known to antagonize the JA chemical or electrical) has been the subject of controversy
pathway (Pieterse et al., 2012), these findings suggest that (for review, see Farmer et al., 2014; Huber and Bauerle,
the enhanced resistance of the mutants is due to a lack of 2016). That JA or a precursor is the mobile signal was pos-
inhibition of the JA pathway rather than a direct effect of SA tulated but not demonstrated (Li et al., 2002a; Stratmann,
(Koornneef and Pieterse, 2008). Spider mite performance 2003; Koo et al., 2009). On the other hand, rapid voltage
was higher on SA-deficient tomato line NahG than on wild- changes in local and distal Arabidopsis leaves in response
type (Villarroel et al., 2016). When the BPH Nilaparvata to S. littoralis feeding were recently reported, and
lugens infested a rice line that overexpresses the resistance depended on GLUTAMATE RECEPTOR-LIKE (GLR) genes
gene Bph14, there was an induced expression of SA-related GLR3.3 and GLR3.6 (Mousavi et al., 2013; Salvador-
genes (Du et al., 2009). Finally, SA accumulated in resistant Recatala et al., 2014). Implanting platinum wires in the
willow genotypes when attacked by the gall midge Dasi- petiole of a leaf and injecting current triggered JA and JA-
neura marginemtorquens (Ollerstam and Larsson, 2003). Ile accumulation, and defense gene expression in the leaf
Pieris brassicae oviposition on Arabidopsis triggered SA lamina distal to the treatment site, providing strong evi-
accumulation and expression of SA-responsive genes (Lit- dence for the role of electrical signaling in systemic
tle et al., 2007). Follow-up studies using SA-signaling response to herbivory (Mousavi et al., 2013). Similar elec-
mutants indicated that Arabidopsis responses to egg trophysiological changes were further observed in mono-
extract, including defense gene expression, ROS accumula- cotyledonous and dicotyledonous species after challenge
tion and local cell death, share similarities with PTI and with S. littoralis and M. sexta (Zimmermann et al., 2016).
© 2017 The Authors

Interestingly, aphid-induced Ca2+ accumulation in Ara- Indeed, pipecolic acid accumulated in local and distal
bidopsis was shown to depend on GLR3.3 and GLR3.6, but leaves after oviposition and mutation in the biosynthesis
here a role in long-distance signaling is unlikely (Vincent gene ALD1 abolished egg-induced SAR (Hilfiker et al.,
et al., 2017). In contrast, systemic responses from 2014). For all these examples, the nature of the systemic
wounded Arabidopsis cotyledons to roots was shown to signal is, however, unknown (Figure 3).
be independent of GLRs and electrical signaling, but more
Open questions
probably due to JA transport (Gasperini et al., 2015). Simi-
larly, JA but not JA-Ile was identified as a long-distance The precise connection between detection of herbivory or
transmissible signal in N. attenuata response to M. sexta egg deposition and the following activation of different sig-
using stem-to-stem grafted plants (Bozorov et al., 2017). In naling pathways is currently unknown. Although the JA
tomato, application of isotope-labeled precursors in pathway is crucial to fend off a majority of herbivores,
wounded leaves indicated that JA-Ile may be a mobile sig- which downstream defenses genes are critical for resis-
nal (Matsuura et al., 2012). It thus appears that a combina- tance is still unresolved in most plant species. The SA path-
tion of electrical signaling and hormone transport may be way may be important in some plant–arthropod
responsible for systemic induction of JA-related defenses, interactions, but further experiments should demonstrate
but that the contribution of each signal may depend on the SA accumulation and altered performance on SA mutants.
organ or plant species considered (Figure 3). Similarly, more work will be necessary to understand the
Oviposition also triggers changes in distal leaves. Egg exact molecular contribution of the ET pathway. Modula-
deposition by the elm leaf beetle Xanthogaleruca luteola, tion of defenses against herbivory by other plant hormones
the sawfly D. pini and the stemborer moth Chilo partellus will also have to be better explored (Erb et al., 2012). Finally,
induced the release of volatiles in local and distal leaves of a better knowledge on the nature of systemic signals that
Ulmus minor, Pinus sylvestris and maize, respectively activate defenses in distal tissues is needed.
(Meiners and Hilker, 2000; Hilker et al., 2002; Tamiru et al.,
2011). Recently, P. brassicae oviposition on Arabidopsis DEFENSE COMPOUNDS
leaves inhibited infection by the bacterial pathogen Pseu-
Metabolites
domonas syringae, both in local and distal leaves (Hilfiker
et al., 2014). This systemic acquired resistance (SAR) The plant multilayered immune system is accompanied by
depended on the metabolic SAR signal pipecolic acid. the endogenous production of metabolites with direct
(a) (b)
EIPVs
al
gn ?
si
al
JA/JA-Ile ?
ic
r
GLR E l e c t JA/JA-Ile ALD1 ALD1
channels Pip Pip
Defenses SAR
Figure 3. Systemic responses to herbivory. (a) Current model of long-distance signaling in response to herbivory. Both GLR-dependent electrical signaling and
JA/JA-Ile movement have been shown to trigger JA-dependent defenses in systemic leaves in response to local feeding. (b) Oviposition triggers release of
HIPVs in local and systemic leaves from several plant species, although the nature of the systemic signal is unknown. ALD1-dependent Pip accumulation in local
and systemic leaves triggers a SAR against plant pathogens. Whether Pip is the mobile SAR signal has not been demonstrated. JA, jasmonic acid; JA-Ile, JA-iso-
leucine; GLR, glutamate receptor-like; ALD1, AGD2-like defense response protein 1; Pip, pipecolic acid; SAR, systemic acquired resistance; HIPVs, herbivore-
induced plant volatiles.
© 2017 The Authors

antimicrobial and/or insecticidal activity, whereas some Canavanine is integrated in proteins, which results in the
metabolites act as signals and contribute to plant immu- synthesis of dysfunctional proteins and poor larval devel-
nity by regulatory means (Mitho € fer and Boland, 2012). opment (Rosenthal et al., 1976; Rosenthal, 2001). Tobacco
Examples of plant-derived metabolites with a direct insecti- and soybean plants respond rapidly to herbivore attack
cidal activity are given in Table 2. with a production of c-aminobutyric acid (GABA; Bown
Plants produce non-protein amino acids that function in et al., 2002). Larvae of the oblique-banded leafroller Chori-
response to herbivory (for review, see Huang et al., 2011). stoneura rosaceana raised on GABA-containing artificial
One of the best-studied examples is L-canavanine, a major diets showed decreased growth and survival rates, indicat-
nitrogen storage compound in seeds of many species of ing that GABA possess direct insecticidal activity (Bown
Leguminosae and a structural analog of L-arginine. L- et al., 2006). This insecticidal activity could result from
Table 2 Plant-derived metabolites with direct insecticidal activity
Metabolite Plant species Arthropod species Mode of action (mutant lines) Reference
Glucosinolates Brassicaceae Mamestra brassicae, Myrosinase-dependent hydrolysis Beekwilder et al. (2008)

Trichoplusia ni, generates nitriles, thiocyanates, Barth and Jander (2006)
Manduca sexta, and ITCs that react with Brown and Hampton (2011)
Spodoptera littoralis biological nucleophiles and
modify proteins and nucleic acids Schweizer et al. (2013b)
(tgg1/tgg2, quadGS, myc234)
Azadirachtina Azadirachta indica Spodoptera littoralis, Disruption of the endocrine system Mordue Luntz et al. (1998)
Spodoptera frugiperda, and inhibition of cell division
Schistocerca gregaria
Benzoxazinoidsg Zea mays Rhopalosiphum maidis Unknown (Bx13NIL-Oh43) Handrick et al. (2016)
Benzyl benzoate Oryza sativa Sogatella furcifera Egg-killing substance Seino et al. (1996)
Calcium oxalate Medicago truncatula Spodoptera exigua Physical abrasion of mandibles Korth et al. (2006)
Ingested calcium oxalate interferes
with larval development (cod5, cod6)
Camalexinc Arabidopsis thaliana Myzus persicae Unknown (pad3, cyp79b2/cyp79b3) Kettles et al. (2013)
GABAb All plant species Choristoneura Suppression of neurotransmission Hosie et al. (1997)
rosaceana, Bown et al. (2002, 2006)
Meloidogyne hapla,
Heliothis virescens
Hydrogen cyanide Trifolium repens, Capnodis tenebrionis, Inhibition of mitochondrial Vetter (2000)
(HCN) Lotus corniculatus Heterobostrychus respiration
Hypera postica brunneus,
Kaempferold Arabidopsis thaliana Pieris brsassicae Unknown (oxMYB75) Onkokesung et al. (2014)
Nicotiana tabacum
Kauralexinsa Zea mays Ostrinia nubilalis Unknown Schmelz et al. (2011)
Lactone taraxinic acida Taraxacum officinale Melolontha melolontha Unknown (ToGAS1) Huber et al. (2016)
b
L-Canavanine Fabaceae Manduca sexta Integration of D-canavanine Rosenthal et al. (1976)
into proteins Rosenthal (2001)
Nicotinee Nicotiana tabacum Spodoptera exigua, Agonist for acetylcholine receptors, Gepner et al. (1978)
Nicotiana attenuata Trimerotropis spp., disruption of nervous system Steppuhn et al. (2004)
Diabrotica (IRpmt, nic1, nic2, nic1/nic2) Katoh et al. (2005)
undecimpunctata
Pyrethrina Chrysanthemum Tetranychidae, Inactivation of sodium channels Casida et al. (1983)
cinerariifolium Pseudococcidae, along nerve cells
Auchenorrhyncha,
Coleoptera, Caelifera,
Aleyrodidae
Rotenoned Derris eliptica, Brought spectrum Inhibition of mitochondrial Dayan et al. (2009)
Pachyrrhizus erosus insecticide respiration
Scopoletinf Artemisia annua Spilartia obliqua Unknown Tripathi et al. (2011)
Teucreina Teucrium marum Monomorium Unknown Eisner et al. (2000)
pharaonis,
Phormia regina,
Periplaneta americana
a
Terpenoid; bamino acid; cindole; dflavonoid; ealkaloid; fcoumarin; ghydroxamic acid.
GABA, c-aminobutyric acid; ITC, isothiocyanate.
© 2017 The Authors

inhibition of neurotransmission via GABA-regulated fast- in roots of tropical legumes, such as Derris eliptica and
acting chloride channels (Hosie et al., 1997; Bown et al., Lonchocarpus, and is a mitochondrial poison that blocks
2006). the electron transport chain and disrupts energy produc-
Terpenoid-based compounds with insecticidal properties tion (Isman, 2006). Kaempferol-3,7-dirhamnoside (KRR)
are widely spread in the plant kingdom. Azadirachtin is syn- accumulates in Arabidopsis in response to P. brassicae
thesized by the neem tree Azadirachta indica, and reduces feeding (Onkokesung et al., 2016). Overexpression of
growth of S. littoralis, S. frugiperda and Schistocerca gre- MYB75, a transcription factor that activates the antho-
garia by negatively influencing cell division and disruption cyanin pathway, resulted in decreased KRR levels in Ara-
of the endocrine system (Mordue Luntz et al., 1998). Pyre- bidopsis plants and increased susceptibility to P. brassicae.
thrin from Chrysanthemum cinerariifolium inactivates Furthermore, P. brassicae gained less weight when reared
sodium channels along nerve cells and thereby harms on an artificial diet containing KRR (Onkokesung et al.,
insects from different orders and families, including 2014).
Tetranychidae, Pseudococcidae, Auchenorrhyncha, Coleop- Aliphatic- and indole-glucosinolates (GS) belong to the
tera, Caelifera and Aleyrodidae (Casida et al., 1983). In best-studied insecticidal metabolites in Brassicaceae,
response to JA, ET and attack by the European corn borer including the model plant Arabidopsis. Aliphatic-GS and
Ostrinia nubilalis, Zea mays produces ent-kaurane-related indole-GS are derived from methionine and tryptophan,
diterpenoids, collectively termed kauralexins, which exhibit respectively. They are produced in leaves constitutively
antifeedant activity on O. nubilalis (Schmelz et al., 2011). and act as phytoanticipins in basal immunity against
Moreover, the lactone taraxinic acid b-D-glucopyranosyl arthropods, but their synthesis can also be induced in
ester (TA-G) in latex protects the dandelion Taraxacum response to various pathogen attacks. Thereby, GS biosyn-
officinale against its major root herbivore, the cockchafer thesis relies on a complex regulatory network, controlled
Melolontha melolontha. Silencing of the germacrene A syn- by several MYB and MYC transcription factors (Schweizer
thase ToGAS1 resulted in decreased levels of TA-G in T. et al., 2013b; Frerigmann, 2016). Upon plant-tissue disrup-
officinale and in increased M. melolontha feeding (Huber tion, b-thioglucoside glucohydrolase-dependent GS hydrol-
et al., 2016). ysis leads to the generation of chemically unstable
Nicotine is one of the best-studied plant-derived alkaloids aglycones, such as toxic nitriles, thiocyanates and isothio-
with insecticidal activity and is produced by native tobacco cyanates (ITCs). These aglycones can react spontaneously
species, such as N. attenuata and Nicotiana sylvestris. It is with biological nucleophiles, and modify proteins and
structurally related to acetylcholine and can thereby target nucleic acids (for review, see Pastorczyk and Bednarek,
acetylcholine receptors in the nervous system of insects 2016). Strikingly, GS-deficient Arabidopsis mutants are
(Gepner et al., 1978). Silencing putrescine N-methyltrans- highly susceptible to arthropod feeding, including chewing
ferase (PMT), which is involved in nicotine biosynthesis, larvae, spider mites and aphids (Mewis et al., 2005; Beek-
results in decreased constitutive and inducible nicotine wilder et al., 2008; Schlaeppi et al., 2008; Schweizer et al.,
levels in N. attenuata. Consequently, IRpmt plants grown in 2013b; Zhurov et al., 2014; Madsen et al., 2015). Trypto-
field experiments were more frequently attacked by the S. phan can also serve as a precursor for several indolic alka-
exigua and Trimerotropis spp. grasshoppers (Steppuhn loids, which act as defense-related metabolites in
et al., 2004). The medicinal plant Catharanthus roseus pro- Arabidopsis. Camalexin is produced in Arabidopsis upon
duces more than 100 different monoterpene indole alka- infestation by the phloem-feeding green peach aphid M.
loids (MIAs), which are well described as anticancer drugs persicae. Consequently, M. persicae grows more success-
in chemotherapy. Catharanthine accumulates in leaf wax fully on camalexin-deficient pad3 mutant, indicating that
exudates and exhibits insect toxicity on Bombyx mori lar- camalexin functions in defense against phloem sap suck-
vae when included in artificial diet (Roepke et al., 2010). Fur- ing insects (Kettles et al., 2013). Similarly, camalexin accu-
thermore, transcriptomic and metabolic analysis showed mulated in response to infestation by the cabbage aphid
that C. roseus respond to M. sexta feeding with the biosyn- Brevicoryne brassicae and aphid performance was aug-
thesis of specific MIAs. Interestingly, C. roseus leaf con- mented on pad3 (Kusnierczyk et al., 2008).
sumption resulted in a rapid death of M. sexta larvae, which Many defense compounds are stored in developmental
could be linked to MIA generation and dimerization (Duge structures, including glandular trichomes, laticifers, resin
Bernonville et al., 2017). Other examples of insecticidal ducts, and specialized cell types or tissues (Mitho € fer and
alkaloids include caffeine, colchicine, strychnine and swain- Boland, 2012). Genetic evidence for the role of trichomes
sonine (Wink et al., 1998; Mitho € fer and Boland, 2012). as a source of defense against herbivores was provided for
Flavonoids, derived from the phenylpropanoid metabo- tomato (Kang et al., 2010; Bleeker et al., 2012), Arabidopis
lism, are a diverse group of plant secondary metabolites (Mauricio, 1998), Arabidopsis lyrata (Kivima€ki et al., 2007)
found in all plant species and they display some antiherbi- and N. attenuata (Luu et al., 2017). Induction of terpene-
vore effects (Ververidis et al., 2007). Rotenone is produced containing traumatic resin ducts by JA in Norway spruce
© 2017 The Authors

provides support for a defensive role of these structures amylase inhibitors have been reported that inhibit diges-
against conifer pests (Martin et al., 2002). tive enzymes and thereby interfere with larval develop-
In addition to ingested defense metabolites that target ment. For instance, expression of an Arabidopsis cysteine
physiological processes in arthropods, plants produce protease inhibitor (Atcys) in transgenic white poplar plants
metabolites that harm feeding herbivores physically. In the is sufficient to inhibit most of the digestive proteinase
barrel medic Medicago truncatula, calcium oxalate crystals activity of the leaf beetle Chrysomela populi and confers
accumulate around secondary veins and act as physical resistance to this insect (Delledonne et al., 2001).
abrasive of S. exigua mandibles. Consistent with this, lar-
Open questions
vae showed a feeding preference for the calcium oxalate-
defective mutants cod5 and cod6 (Korth et al., 2006). Silica Numerous plant-derived insecticides have been identified
constitutes another important physical defense compound, and some of them are of great interest in agriculture for
particularly in grasses (for review, see Hartley and DeGab- plant protection. However, the activity of most of them has
riel, 2016). For example, Spodoptera exempta larvae just been studied in artificial diets. We need better knowl-
exposed to a silica-rich diet displayed mandible wear and edge of biosynthetic pathways and generation of knockout
reduced growth (Massey and Hartley, 2009). mutants to test their role in vivo. Moreover, target sites for
many of the known insecticides are poorly characterized.
Proteins and peptides
SUPPRESSION OF DEFENSES
Besides toxic metabolites, plants produce numerous pro-
teins and peptides with direct insecticidal activity (Table 3). Effective plant PTI exerts strong selection pressure on
Acrelin-1 is a 60-kDa dimeric glycoprotein found in seeds aggressors. Bacterial and fungal pathogens have thus
of the wild kidney bean Phaseolus vulgaris. Acrelin-1 is evolved numerous effectors to interfere with PTI (Dodds
highly resistant to proteolytic degradation and binds to et al., 2009; Deslandes and Rivas, 2012). These effectors
complex glycans, which leads to disruption of the epithe- are secreted and transferred or directly injected into plant
lial structure in the mid-gut of the Mexican bean weevil cells. In return, plants have developed strategies to directly
Zabrotes subfasciatus (Fabre et al., 1998). Plant-derived or indirectly detect effectors by intracellular nucleotide-
lectins are a heterogenous group of proteins found in binding, leucine-rich-repeat receptors (NB-LRRs) that trig-
many members of Leguminosae. They can bind to specific ger an enhanced defense response called ETI (Jones and
carbohydrate structures in the insect digestive tract, which Dangl, 2006). This process illustrates the ongoing arms
leads to harmful effects in the whole insect body. Insectici- race that has been the driving force for generating a multi-
dal activity of lectins was reported against members of tude of effectors and defense proteins during plant–patho-
Coleoptera, Lepidoptera and Homoptera (Vandenborre gen co-evolution. Similarly, plant defense suppression by
et al., 2011). arthropods has been reported in several studies (Table 1).
Cyclotides represent a group of small peptides found in
Arthropod-derived effectors
Rubiaceae and Violaceae. A cyclic peptide backbone in
combination with a cysteine knot confers strong chemical A seminal discovery by Musser et al. (2002) reported that
and biological stability. Cyclotides inhibit larval growth and glucose oxidase (GOX) in Helicoverpa zea salivary glands
development of the native budworm Helicoverpa punctig- inhibited nicotine production in tobacco. Elegant experi-
era, and lead to disruption of microvilli and cellular rupture ments using ablation of the secretory apparatus, the spin-
in the gut epithelium of Helicoverpa armigera larvae (Jen- neret and ectopic application of active or inactive GOX
nings et al., 2001; Barbeta et al., 2008). Canatoxin (CNTX) is demonstrated that this enzyme is responsible for a lower
an urease found in seeds of the jack bean Canavalia ensi- accumulation of nicotine upon feeding. Because GOX gen-
formis. Proteolytic activation of CNTX releases a 10-kDa erates H2O2 from D-glucose, it was further shown that this
peptide that interferes with serotine-related processes in ROS may interfere with plant defense signaling (Bede
Callosobruchus maculatus and Rhodnius prolixus (Sta- et al., 2006; Diezel et al., 2009). An ATP-hydrolyzing apyr-
niscßuaski and Carlini, 2012). In tomato, threonine deami- ase activity was found in H. zea saliva. Tomato plants trea-
nase TD2 has insecticidal properties by depriving ted with this enzyme showed reduced defense gene
herbivores from the essential Thr. Proteolytic activation of expression (Wu et al., 2012). Because ATP can be per-
TD2 is catalyzed by chymotrypsin in the gut of lepidopteran ceived as a DAMP by plant PRRs, it is tempting to specu-
herbivores, such as S. exigua, but not in coleopteran herbi- late that some insects have evolved a way to reduce ATP
vores. Consequently, S. exigua larvae performed better on levels in their host. Unknown proteins or peptides from
TD2-deficient tomato plants (Gonzales-Vigil et al., 2011). lepidopteran OS inhibited wound-induced defense gene
Arthropod digestion and nutrient acquisition relies on expression in Arabidopsis and tomato, and this was corre-
enzymes such as a-amylases, cysteine proteases and ser- lated with enhanced insect performance in the case of Ara-
ine proteases. So far, numerous plant protease and bidopsis (Lawrence et al., 2007; Consales et al., 2012).
© 2017 The Authors

Table 3 Plant-derived proteins with direct insecticidal activity
Protein Plant species Arthropod species Mode of action (mutant lines) Reference
a-Amylase inhibitors Fabaceae, Poaceae, Coloptera, Hemiptera, Inhibition of digestive a-amylases Franco et al. (2002)
Caryophyllales Blattidae
Acrelins Phaseolus vulgaris Zabrotes subfasciatus Binding to complex glycans disrupts Fabre et al. (1998)
mid-gut epithelial structure
Canatoxins Canavalia ensifonnis Callosobruchus chinensis, Interfere with serotonin processes Carlini et al. (1997)
Rhodnius prolixus, and disrupt fluid transport across Staniscßuaski and Carlini (2012)
Nezara viridula, anterior mid-gut epithelium
Dysdercus peruvianus
Cyclotides Oldenlandia affinis Helicoverpa punctigera, Disrupt larval mid-gut membranes Jennings et al. (2001)
Rubiaceae, Violaceae Helicoverpa armigera Barbeta et al. (2008)
Cysteine protease Zea mays L. Spodoptera frugiperda Disrupts caterpillar peritrophic matrix Pechan et al. (2002)
Cysteine protease Oryza sativa Coleoptera, Inhibition of digestive gut proteases Kuroda et al. (1996)
inhibitors Glycine max Hemiptera Koiwa et al. (1998)
Arabidopsis thaliana Delledonne et al. (2001)
Lectins Leguminosae Coleoptera, Binding to glycosyl groups attached Vandenborre et al. (2011)
Lepidoptera, to digestive tract
Homoptera
Ribosome-inactivating Fabaceae, Anthomonus grandis Inactivation of 60S ribosomal subunit Olsnes et al. (1974)
proteins (RIPs) Asparagaceae. Callosobruchus maculatus Carlini and
Passifloraceae Anthomonus grandis Carlini and Grossi-de-Sa (2002)
Serine protease Solanaceae Spodoptera exigua Inhibition of digestive gut proteases Green and Ryan (1972)
inhibitors Hartl et al. (2010)
Threonine deaminase Solanum lycopersicum Spodoptera exigua Deprivation of essential Thr Gonzales-Vigil et al. (2011)
(TDAs15, TDAs7)
Vegetative storage Arabidopsis thaliana Diabrotica Insecticidal activity correlated Liu et al. (2005)
protein 2 (VSP2) undecimpunctata howardi with acid phosphatase activity (vsp2)
Callosobruchus maculatus,
Drosophila melanogaster
© 2017 The Authors

Although they act as HAMPs in several insects, FACs aphid effectors revealed that they act in a plant-specific
may have dual roles. Emission of some volatiles was way and that sequences displayed high non-synonymous
reduced when M. sexta FACs were applied to N. attenuata substitution rates, indicative of positive selection (Pitino
plants. Whether this interfered with parasitoid attraction and Hogenhout, 2013).
was, however, not tested (Gaquerel et al., 2009). Heat- The Hessian fly Mayetiola destructor is an economically
stable components of M. sexta OS suppressed wound- important pest of wheat and a well-studied member of the
induced accumulation of N. attenuata transcripts, but their plant parasitic gall midges (Stuart et al., 2012). The Hessian
chemical nature was not studied (Schittko et al., 2001). fly genome revealed a large family of secreted proteins
Another striking example of a modified HAMP activity is (SSGP-71) that resemble ubiquitin E3 ligases in plants
found in the legume-specialist velvetbean caterpillar Anti- (Zhao et al., 2015). They contain a F-box domain and vari-
carsia gemmatalis. OS of this insect contain a modified able leucine-rich repeats (LRR). In plants, the F-box inter-
inceptin that does not induce plant defenses and further- acts with Skp, a component of the SCF-E3-ubiquitin-ligase
more acts as an antagonist of the normally active inceptin, complex that targets proteins for degradation. Interest-
probably by competing with inceptin–PRR binding ingly, two Hessian fly F-box-LRR effectors were shown to
(Schmelz et al., 2012). directly bind to wheat Skp proteins, suggesting that the
For spider mites and aphids, examples of effective sup- role of these effectors is to highjack the plant proteasome
pression of defenses exist. In the spider-mite T. urticae, in order to block defenses (Zhao et al., 2015). As further
two proteins of unknown function suppressed defenses evidence that F-box-LRRs are true effectors that can be rec-
and increased mite performance when expressed in Nico- ognized by NB-LRRs and trigger ETI, mutations in two
tiana benthamiana (Villarroel et al., 2016). A salivary com- SSGP-71 genes were associated with regained virulence
ponent with high homology to human macrophage on wheat cultivars containing the respective H resistance
migration inhibitory factor (MIF) was identified in the pea genes (Zhao et al., 2015).
aphid Acyrthosiphon pisum (Naessens et al., 2015). MIFs As discussed above, JA and SA signaling pathways gen-
are important pro-inflammatory cytokines modulating erally modulate plant defenses against arthropods and
immunity and inflammation in vertebrates. Interestingly, pathogens, respectively. These pathways are antagonistic
RNAi of ApMIF1 reduced survival and fecundity of A. to each other, and this property has been highjacked by
pisum. In addition, ectopic expression of MIF1 reduced bacterial effectors to effectively suppress SA-dependent
plant defenses in N. benthamiana (Naessens et al., 2015). defenses (Pieterse et al., 2012; Zheng et al., 2012; Gimenez-
Because 1) MIFs form heterocomplexes and 2) MIF homo- Ibanez et al., 2014). Interestingly, effectors from arthropods
logs have been recently identified in plant genomes also exploit antagonism between SA and JA pathways. In
(Panstruga et al., 2015), aphid MIF may interfere with Arabidopsis, defense gene expression and JA levels were
endogenous MIFs to alter plant defenses (Naessens et al., lower in response to S. exigua larvae with intact salivary
2015; Reymond and Calandra, 2015). A salivary calcium- glands compared with larvae with ablated spinneret. This
binding protein from Megoura viciae prevented sieve plate effect was lost in a mutant that does not accumulate SA,
occlusion, a known defense mechanism against phloem implying a role for SA in inhibiting JA accumulation
feeding that is triggered by calcium release (Will and van (Weech et al., 2008). Silverleaf whitefly induced SA
Bel, 2006; Will et al., 2007). Acyrthosiphon pisum, in which defenses while suppressing JA defenses in Arabidopsis
expression of the salivary protein C002 was reduced by and lima bean (Zarate et al., 2007; Zhang et al., 2009). Simi-
RNAi, was impaired in phloem feeding (Mutti et al., 2008). larly, the mealybug Phenacoccus solenopsis inhibited JA
Attempts to identify more aphid effectors have relied on accumulation and JA-dependent defenses in tomato, and
the same proteomic and genomic approaches that sucess- this suppression was due to SA accumulation (Zhang et al.,
fully isolated secreted HAMPs. A series of proteins of 2015). A somewhat twisted example comes from the Color-
unknown function have been tested, and were shown to ado potato beetle (CPB) Leptinotarsa decemlineata that
suppress PTI responses and increase aphid performance uses microbe-derived flagellin to trigger SA-dependent
when expressed in planta (Bos et al., 2010; Atamian et al., inhibition of the JA pathway in tomato. Indeed, bacteria in
2013; Elzinga et al., 2014). For example, the M. persicae CPB OS decreased JA-responsive defenses and increased
Mp10 effector suppressed flg22-induced but not chitin- SA and SA-related gene expression. These responses were
induced ROS production (Bos et al., 2010). Furthermore, lost when using antibiotic-treated larvae and a SA-mutant
Mp10 was shown to act in the BAK1 pathway (Drurey (Chung et al., 2013). The observation that chitinase in larval
et al., 2017). Myzus persicae Mp1 promoted aphid viru- frass of the fall armyworm S. frugiperda suppress maize
lence by targeting a vacuolar sorting protein (VSP52) from defenses through induction of the SA-dependent gene
its preferred host plants Arabidopis and potato, but not expression provides another intriguing evidence of indirect
with VSP52 from poor-host barley and M. truncaluta effector-like activity. Finally, P. brassicae oviposition or egg
(Rodriguez et al., 2017). Similarly, a comparative study on extract-treatment triggered SA accumulation, suppressed
© 2017 The Authors

larval-induced JA-dependent gene expression, and expressing SP11- or AY-WB-infected plants produced less
enhanced larval performance in Arabidopsis (Little et al., JA and allowed enhanced performance of the leafhopper
2007; Bruessow et al., 2010). This egg-induced inhibition of vector Macrosteles quadrilineatus (Sugio et al., 2011).
the JA pathway is achieved through SA-dependent destruc-
Arthropod resistance genes
tion of MYC2, MYC3 and MYC4 transcription factors that
control JA defense gene expression (Schmiesing et al., Effector-triggered immunity triggered by pathogen or
2016). Intriguingly, P. brassicae oviposition also triggers a fungal effectors is driven by NB-LRRs. These resistance pro-
SAR against bacterial pathogens, a response that may ben- teins usually contain a Toll-Interleukin-1 receptor-Resis-
efit hatching larvae (Hilfiker et al., 2014). This latter phe- tance protein (TIR) or a coiled-coil (CC) domain at the amino
nomenon does not seem to be strictly related to terminus. They are encoded by numerous resistance (R)
suppression of defenses but illustrates a manipulation of genes usually clustered in plant genomes, allowing recom-
plant signaling pathways by an egg-derived effector, to the bination-based diversification to respond to the evolution
potential benefit of the attacker. of pathogen effectors (Jones and Dangl, 2006; McHale
et al., 2006). In contrast to R genes associated with bacterial
Defense suppression by insect-vectored viruses and
and fungal pathogens, only a few arthropod-directed R
phytoplasma
genes have been cloned and characterized (Gururani et al.,
Plant pathogens like viruses and phytoplasma are often 2012). Mi-1.2 from tomato encodes a CC-NB-LRR and con-
transmitted by arthropods and thus engage in mutualistic fers resistance to the potato aphid, the whitefly B. tabaci,
interactions with their vector to ensure dispersal and sur- the psyllid Bactericerca cockerelli, and the root-knot nema-
vival. Improved performance and reproduction of the car- tode Meloidogyne incognita, illustrating the first example
rier is thus crucial for the pathogen, and consequently of a resistance gene acting against distantly related pests
compromising plant defenses has obvious advantages. (Milligan et al., 1998; Rossi et al., 1998; Nombela et al.,
The pathogenesis protein bC1 of Tomato yellow leaf curl 2003; Casteel et al., 2006). In the presence of potato aphid
China virus (TYLCCNV), a begomovirus transmitted by the saliva Mi-1.2 was shown to interact with SlSERK1, a recep-
whitefly B. tabaci, binds to the plant transcription factor tor kinase related to Arabidopsis BAK1, and this complex
AS1, triggering a reduced expression of JA-responsive formation is suggested to confer aphid resistance (Peng
genes (Yang et al., 2008). bC1 interacted with MYC2 and et al., 2016). Vat from melon is also a CC-NB-LRR and, inter-
interfered with expression of TPS genes, which are respon- estingly, provides dual resistance against the aphid Aphis
sible for biosynthesis of defensive terpenoids (Li et al., gossypii and viruses transmitted by this vector (Dogimont
2014). Consequently, virus-infected whiteflies displayed a et al., 2014). Resistance to the BPH N. lugens, a sucking
significantly higher survival and reproduction on tobacco insect attacking rice plants, is conferred by two CC-NB-LRR
plants than non-infected ones (Luan et al., 2013). The C2 genes, Bph14 and Bph16 (Du et al., 2009; Tamura et al.,
protein from the Tomato yellow leaf curl Sardinia virus 2014). In lettuce, Ra is part of a large CC-NB-LRR gene clus-
(TYLCSV) and Tomato yellow leaf curl virus (TYLCV) was ter and provides resistance against the root aphid Pemphi-
shown to interfere with the activity of COP9 signalosome gus bursarius (Wroblewski et al., 2007). The AIN locus in M.
complex, which subsequently compromised the function truncatula is associated with resistance against the blue-
of several CUL1-based SCF ubiquitin E3 ligases. Jasmonate green aphid Acyrthosiphon kondoi and resides in a cluster
responses were altered in Arabidopsis expressing C2 from of CC-NB-LRR genes (Klingler et al., 2009). Similarly, Hdic is
TYLCSV or TYLCV, suggesting that SCFCOI1 is one target of embedded in a family of NB-LRR H resistance genes that
this virulence factor (Lozano-Duran et al., 2011; Rosas-Dıaz are active against the Hessian fly M. destructor (Stuart
et al., 2016). The 2b protein of aphid-transmitted Cucumber et al., 2012).
mosaic virus inhibited expression of JA-regulated genes
Open questions
downstream of JA production (Lewsey et al., 2010). Myzus
persicae aphid fecundity was enhanced by Turnip mosaic Chemical identity, mode of action and molecular target(s)
virus infection of Arabidopsis, which showed increased of several effectors are poorly characterized. Whether each
callose deposition. This effect depended on ET-signaling type of effector represents an evolutionary response to PTI
and was caused by the Nuclear Inclusion a-Protease and appears in only a subset of related arthropod species
domain (Casteel et al., 2015). or biotypes, similar to bacterial or fungal effectors, remains
Phytoplasma are obligate bacterial pathogens that an open question. When effectors inhibit defenses via SA-
develop in plant phloem. The Aster Yellows phytoplasma dependent inhibition of the JA pathway, it is unclear
strain Witches’ Broom (AY-WB) secretes the SAP11 protein whether activation of the SA pathway by arthropod-
that destabilizes class II CIN-TCP transcription factors, derived cues illustrates a strategy evolved by the attacker
some of which are positive regulators of the JA-biosynth- to indirectly target the JA pathway or whether this is a
esis enzyme LOX2. As a consequence, Arabidopsis lines trade-off, as the SA pathway may be needed for defense.
© 2017 The Authors

Strikingly, all examples of cloned resistance genes are larvae moved away from elicited and closely connected
CC-NB-LRRs that target phloem-feeding insects. Whether leaves, suggesting that they are capable of detecting a sig-
there is a mechanistic reason for such specificity or nal that triggers this response. The nature of the warning
whether this is explained by a lack of success in cloning signal is unknown but depends on activation of the JA
resistance genes against members of other feeding guilds pathway (Perkins et al., 2013). There are also examples of
will await future experiments. Indeed, many loci providing behaviors that reduce attraction of parasitoids. Larvae of
resistance against different orders of arthropods have been Heliothis subflexa have specialized on their host plant Phy-
identified in different crop species and need to be charac- salis angulata by feeding exclusively on fruits, which lack
terized (Smith and Clement, 2011; Gururani et al., 2012). linolenic acid. As a consequence, no volicitin is produced
Alternatively, other feeding guilds that rapidly consume in H. subflexa OS and feeding does not trigger volatile
leaf material may avoid recognition by ‘eating the evi- emission (De Moraes and Mescher, 2004). Because linole-
dence’. Also, besides F-box-LRR effectors and H resistance nic acid is required for development of most insect larvae,
proteins in Hessian fly/wheat interaction, information this physiological adaptation is remarkable, and provides
about the nature of effectors interacting with known arthro- both a protection against parasitoids and an exclusive
pod NB-LRRs is currently lacking. access to a food source. Interestingly, linolenic acid is also
a precursor for JA, and there is the possibility that P. angu-
PLANT–ARTHROPOD CO-EVOLUTION
lata fruits are unable to trigger JA-dependent defenses
Plants and herbivores are engaged in a continuous battle against herbivores. This hypothesis was, however, not
for survival, and rely on different strategies to counteract tested in the study. Recently, the first evidence of insect
the evolution of resistance or adaptation to defense com- resistance against an introduced parasitoid wasp was
pounds. In addition to PTI and ETI immunity responses, reported (Tomasetto et al., 2017). The Argentine stem wee-
which are based on HAMP recognition and inhibition of vil Listronotus bonariensis was discovered in New Zealand
HAMP-triggered defenses by arthropod effectors (see pre- in 1927, and causes intensive damage to pasture grass.
vious sections), there are numerous examples of behav- Since the introduction of a natural parasitoid of the stem
ioral or metabolic responses that overcome plant defenses weevil in the 1990s, there has been a gradual decline in
(Table 4). In a few cases, a successive appearance of parasitism rate from 80–90% to 10–20%. This sharp reduc-
defense and counterdefense mechanisms can be observed tion is attributed to a host shift from Lolium multiflorum to
and nicely illustrates co-evolutionary processes that under- the more widely cultivated Lolium perenne, which is
lie plant–arthropod interactions. potentially impaired in herbivore-induced volatile emission
(Tomasetto et al., 2017).
Behavioral adaptations
Metabolic resistance
The capability of arthropods to circumvent plant defenses
by specialized feeding behavior has been documented (for Target modification and metabolism of plant toxins are the
review, see Dussourd, 2017). Cardenolides are toxic cardiac main strategies to overcome plant defenses and have been
glycosides that inhibit Na/K-ATPase and are stored in latex the subject of numerous studies, which in some instances
from several plant families. Larvae of the queen butterfly have revealed the molecular mechanism (for review, see
Danaus gilippus cut trenches on leaves of the milkweed Despres et al., 2007; Li et al., 2007; Heidel-Fischer and
Asclepias syriaca, releasing a flow of cardenolide-contain- Vogel, 2015).
ing latex and thus rendering the plant more palatable Insensitivity of the monarch butterfly Danaus plexxipus
(Dussourd and Eisner, 1987). In some Bursera species, to cardenolides was attributed to an amino acid substitu-
terpene-containing resin is stored under pressure in leaf tion in the binding site of a Na/K-ATPase (Holzinger and
canals. Upon feeding, the toxic resin is ejected and solidi- Wink, 1996). The same substitution was found in four
fies around small herbivores. Adapted members of chry- species that span four insect orders and 300 million years
somelid beetles of the genus Blepharida puncture leaf of divergence, providing a stunning example of conver-
veins to stop the flow before feeding (Becerra, 2003). Leaf gent evolution (Dobler et al., 2012). Helicoverpa zea
vein severing or trench cutting is frequent and found in evolved a structural modification in the binding site of a
several arthropod families (Dussourd, 2017). carboxypeptidase to evade inhibition of the potato car-
To avoid defensive trichomes in Solanum sp., larvae of boxypeptidase inhibitor (Bayes et al., 2005). Similarly, a
the ithomiid butterfly Mechanitis isthmia spin a fine silk single amino acid substitution in chymotrypsin from Heli-
fabric over spines, allowing them to move and feed safely coverpa larvae removes a binding contact to a tobacco
(Rathcke and Poole, 1975). Another behavioral adaptation proteinase inhibitor (Dunse et al., 2010). As described
is to minimize contact with induced plant defenses. When above, L-canavanine from legumes is a L-Arg analog with
carefully studying movement of H. armigera caterpillars insecticidal properties. Larvae of the bruchid beetle Car-
feeding on Arabidopsis, Perkins et al. (2013) noticed that yedes brasiliensis have evolved a discriminating arginyl-
© 2017 The Authors

Table 4 Co-evolution between plants and arthropods
Plant defense Arthropod adaptation Plant counterdefense Reference
Cardenolides Leaf vein cutting

Asclepias syriaca Danaus gilippus and others Dussourd and Eisner (1987)
High-pressure resin Leaf vein severing
Bursera sp. Blepharida sp. Becerra (2003)
JA-dependent defenses Avoiding induced tissue
Arabidopsis Helicoverpa armigera Perkins et al. (2013)
Trichomes Silk threads over spines
Solanum hirtum Mechanitis isthmia Rathcke and Poole (1975)
Attraction of parasitoids Host shift, escape behavior (?)
Lolium multiflorum Listronotus bonariensis Tomasetto et al. (2017)
Attraction of parasitoids Eating fruit, no volicitin in OS
Physalis angulata Heliothis subflexa De Moraes and Mescher (2004)
Cardenolides ATPase N122H substitution
Apocynaceae Danaus plexxipus and others Dobler et al. (2012)
Protease inhibitors (PI) PI-insensitive protease
potato Helicoverpa zea Bayes et al. (2005)
L-Canavanine (Arg analog) Discriminating tRNA synthetase
Dioglea megacarpa Caryedes brasiliensis Rosenthal et al. (1976)
Cyanogenic glycoside Detoxification Egg mimicry
Passiflora sp. Heliconius cydno Passiflora cyanea Williams and Gilbert (1981)
Cyanogenic glycoside Bacterial -cyanoalanine synthase
Phaseolus lunatus Tetranychus urticae Wybouw et al. (2014)
Alkaloid Nicotine excretion and metabolism Altered flower phenology
Nicotiana attenuata Manduca sexta Nicotiana attenuata Kessler et al. (2010)
Glucosinolates Nitrile-specifier proteins GS diversification
Brassicales Pieris rapae and other Pierinae Brassicales Edger et al. (2015)
Glucosinolates Nitrile-specifier protein (?) Egg mimicry
Brassicales Pieris sysimbrii Streptanthus brewerii Shapiro (1981)
Glucosinolates Induction of detoxification genes
Arabidopsis Heliothis virescens Schweizer et al. (2017)
Furanocoumarins Detoxification by CYP6B1
Apiaceae Papilio polyxenes Hung et al. (1997)
HAMP detection (inceptin) Inceptin modification
Vigna unguiculata Anticarsia gemmatalis Schmelz et al. (2012)
Defense signaling Induction of CYP450s by JA, SA
Apium graveolens Helicoverpa zea Li et al. (2002b)
Arg, arginine; GS, glucosinolates; HAMP, herbivore-associated molecular pattern; JA, jasmonic acid; OS, oral secretions; SA, salicylic acid.
Question marks indicate no experimental evidence for the adaptation.
tRNA synthetase that does not accept L-canavanine as Excretion of the alkaloid nicotine by the specialist tobacco
substrate and thus are protected against the toxic effect hornworm M. sexta is thought to be the main method by
of this analog (Rosenthal et al., 1976). which this insect can thrive on Solanaceae (Self et al.,
Detoxification of cyanogenic glycosides from Passiflora 1964; Maddrell and Gardiner, 1976). Interestingly, it was
sp. by larvae of the butterfly Heliconius is carried out by recently shown that part of the ingested nicotine is trans-
sequestration and replacement of a nitrile by a thiol ported from M. sexta mid-gut to the hemolymph, from
group that prevents cyanide release (Engler et al., 2000). where it is actively exhaled and used as a defensive sig-
However, the enzyme responsible for this reaction has not nal against the spider predator Camptocosa parallela
been identified yet. Another way to avoid cyanide poison- (Kumar et al., 2014).
ing is to metabolize HCN. Remarkably, the spider mite T. Arthropod adaptation to the GS-myrosinase system of
urticae has acquired a bacterial gene encoding a b-cya- Brassicaceae has been extensively studied (Winde and
noalanine synthase (CAS) that can detoxify HCN to b-cya- Wittstock, 2011). In larvae of P. rapae and P. brassicae,
noalanine (Wybouw et al., 2014). The same activity was mid-gut nitrile-specifier proteins (NSPs) favor GS hydrol-
found in the lepidopteran herbivore P. rapae where CAS ysis to less toxic nitriles, instead of ITC (Wittstock et al.,
genes are also predicted to originate from bacteria 2004). In contrast, the diamondback moth P. xylostella
through horizontal gene transfer (van Ohlen et al., 2016). and the desert locust S. gregaria detoxify intact GS with
© 2017 The Authors

a sulfatase, preventing formation of hydrolysis products allelochemicals. In different strains of the gypsy moth
(Ratzka et al., 2002; Falk and Gershenzon, 2007). Remark- Lymantrya dispar, larval survival on an artificial diet con-
ably, the cabbage aphid B. brassicae sequesters intact taining phenolic glycosides was positively correlated with
GS from its host plants in the hemolymph and produces CCE activity (Lindroth and Weisbrod, 1991). Similarly,
a myrosinase in microbodies. Upon attack by predators, ABC transporters have been associated with insecticide
aphids use this ‘mustard-oil bomb’ to generate bioactive resistance, including Bacillus thuringiensis insecticidal
compounds and defend themselves (Bridges et al., 2007; toxins (Bt). There is an expansion of ABC genes in the T.
Kazana et al., 2007). Similarly, the crucifer specialist urticae genome, and expression of ABC genes is
flea beetle Phyllotreta striolata accumulates GS when enhanced upon switching to a different host plant or
feeding and has acquired a myrosinase gene (Beran feeding on artificial diet containing plant secondary
et al., 2014). metabolites (Grbic et al., 2011; Dermauw et al., 2013a,b;
Major detoxification gene families from arthropods Dermauw and Van Leeuwen, 2014; Tay et al., 2015;
include cytochrome P450 monooxygenases (CYP450s), glu- Bretschneider et al., 2016). However, direct evidence for a
tathione-S-transferases (GSTs), UDP-glycosyltransferases role of ABCs in resistance to plant allelochemicals is
(UGTs), carboxyl/cholinesterases (CCEs) and ABC trans- scarce. In the only known example, the CpMRP trans-
porters (ABCs; Li et al., 2007; Heidel-Fischer and Vogel, porter of the Chrysomelid leaf beetle Chrysomela populi
2015). These enzymes have relatively broad substrate is involved in the sequestration of salicin, a toxic phenolic
specificity and are generally important for generalist herbi- glucoside found in willow and poplar leaves. CpMRP
vores that face a variety of plant toxins. Using the polypha- shuttles salicin from the hemolymph into specialized
gous T. ni and defense or signaling mutants, Herde and defensive glands, which play a role against predators.
Howe (2014) were the first to demonstrate transcriptional Reduction of CpRMP expression by RNAi abolished sali-
reprogramming and altered expression of detoxification cin excretion and rendered leaf beetles defenseless
genes in response to GS in Arabidopsis. Similarly, a com- (Strauss et al., 2013).
parative transcriptomic analysis of larvae of the generalist
Escaping detection or anticipating defenses
Heliothis virescens and the specialist P. brassicae feeding
on Arabidopsis genotypes with contrasting GS levels As a striking example of adaptation, larvae of the vel-
revealed a significant upregulation of detoxification genes vetbean caterpillar produce a modified form of the cyclic
from all the above-mentioned families in the generalist, peptide inceptin, a HAMP found in OS of the generalist
whereas there was a much-reduced transcriptional activa- Fall armyworm (see section on HAMPs). Through yet
tion in the specialist (Schweizer et al., 2017). Fura- unknown modification of a gut protease, digestion of
nocoumarins are DNA-interfering agents primarily found in chloroplastic ATP synthase of the host plant cowpea gen-
Apiaceae and Rutaceae. Species of the genus Papilio, erates a peptide lacking the C-terminal amino acid, Vu-In-
A
including the black swallowtail Papilio polyxenes, induce (Schmelz et al., 2012). Velvetbean OS induced a signifi-
the expression of CYP450s from the CYP6B class upon cantly weaker ET production and volatile emission in
feeding on furanocoumarin-containing plants. CYP6B pro- cowpea leaves, suggesting that the truncated inceptin
teins were shown to metabolize furanocoumarins and were evades recognition by a (unknown) plant receptor (Sch-
more active in the specialist P. polyxenes than in the gen- melz et al., 2012).
eralist H. zea (Hung et al., 1997; Li et al., 2004a, 2007). The A lag phase between ingestion/perception of plant tox-
fly genus Scaptomyza is closely related to the genus Dro- ins and transcriptional activation of detoxification genes
sophila and has acquired the ability to feed on Brassi- may be detrimental to optimal larval development. An
caceae. A duplication in the GST gene GstD1 in Sambucus interesting study reported that treatment of H. zea larvae
nigra is responsible for an enhanced detoxification activity with the plant defense signals JA and SA induced the
against ITCs, toxic breakdown products of GS, and is pos- expression of four CYP450s that metabolize fura-
tulated to be linked to the evolutionary transition to her- nocoumarins and other toxins (Li et al., 2002b). This induc-
bivory in Drosophilidae (Gloss et al., 2014). Gossypol is a tion was shown to provide an advantage to larvae, which
major sesquiterpene defensive compound in cotton. Lar- performed better on furanocoumarin-containing plants or
vae of the generalist Heliothine moth H. armigera can diets. ‘Eavesdropping’ on defense signals seems thus an
develop on cotton plants and are equipped with two UGTs, effective way of anticipating the production of defense
UGT41B3 and UGT40D1, which are capable of glycosylat- compounds, but the generality of this phenomenon
ing gossypol (Krempl et al., 2016). amongst arthropods has yet to be established.
Although CCEs have been clearly associated with resis-
Co-evolution
tance to synthetic insecticides and CCE gene expression
is induced after feeding (Li et al., 2007; Teese et al., 2010), The seminal publication by Ehrlich and Raven (1964)
there is limited information on their role against plant stressed the importance of a reciprocal relationship between
© 2017 The Authors

butterflies and plant hosts in shaping the evolution and host species of Sapindaceae from North America (Carroll,
diversification of each group, and by extension supported 1992).
the notion that plant–enemy interactions are responsible for Although adaptation of specialist arthropods to plant
much of the global biological diversity. This has stimulated defenses is well documented, evidence for plant resistance
decades of research to test these predictions and provide to specialists is less frequent. Interestingly, some Brassi-
experimental data for such a scenario. Evidence is, how- caceae contain other defense compounds besides GS,
ever, scarce, because evolution is such a slow process that including alkaloids (camalexin in Arabidopsis and cochlear-
it is difficult to catch it in action, and because several envi- ine in Cochlera sp.) and the steroid cucurbitacin in Iberis
ronmental, biogeographical and ecological factors may con- amara (Tsuji et al., 1992; Sachdev-Gupta et al., 1993; Brock
found interpretations (for review, see Futuyma and et al., 2006). Cucurbitacin has some antifeedant activity on
Agrawal, 2009). For example, removal of herbivore pressure P. rapae (Sachdev-Gupta et al., 1993), and a study on natu-
in replicate fields of the evening primrose Oenothera ral variation in resistance to P. brassicae in Arabidopsis
biennis caused a rapid evolutionary divergence (Agrawal accessions identified QTLs that are not linked to GS biosyn-
et al., 2012). Phylogenetic reconstructions of plant and thesis (Pfalz et al., 2007). In a beautiful example of co-evolu-
arthropods lineages have, however, generated useful hints tion, some cyanogenic glycoside-containing species of
that evolution of defense chemistry responds to herbivore Passiflora have counteradapted to the specialist Heliconius
pressure and that counteradaptation drives arthropod diver- butterfly by the development of egg mimics that repel
sity. A convincing example is the stepwise evolution of GS oviposition (Williams and Gilbert, 1981). Egg mimics have
complexity in Brassicales, mirrored with the radiation of also evolved in the GS-containing crucifer Strepthanthus
Pierinae butterfly species (Wheat et al., 2007; Edger et al., breweri to fend off the specialist Pieris sisymbrii (Shapiro,
2015). A robust phylogenetic analysis of 14 families from 1981). Many plants face the problem of attracting pollina-
the Brassicales revealed that this order originated tors without being a target for herbivory. Nicotiana attenu-
~90 million years ago (Ma) and that plants only synthesized ata is a night-flowering tobacco whose flowers emit benzyl
aromatic Phe-GS. Indole-GS appeared after a whole-gen- acetone that attracts pollinators, including the adapted her-
ome duplication (WGD) ~77 Ma, followed by the occurrence bivore moth M. sexta. In response to M. sexta feeding, N.
and diversification of aliphatic-GS-containing families attenuata shows a striking change of phenology by gener-
~60 Ma. Finally, after a second WGD, Brassicaceae ating flowers that produce low levels of benzyl acetone and
appeared ~30 Ma and coincided with the greatest GS and open during the day, attracting hummingbird as novel pol-
species diversification (Edger et al., 2015). Pierinae colo- linators (Kessler et al., 2010).
nized Brassicales 68 Ma, approximately 10 million years
Open questions
after indole-GS appearance, and radiated through the
acquisition of NSPs. Again, shortly after the occurrence of Although many assumptions still rely on correlative evi-
Brassicaceae, new lineages of Pierinae evolved and dence, progress has been made in the understanding of
diversified. Strikingly, independent nitrile-specifier gene evolutionary forces that drive escalation of chemical
lineages could be associated with independent colonization defenses and arthropod adaptations to these chemicals. A
of Brassicaceae by two Pierinae lineages (Edger et al., recurring issue is to know the exact chain of events and
2015). causative agents that result in apparent defense–adapta-
Comparative phylogenies of Bursera sp. and Blepharida tion–counterdefense scenarios. Improved and additional
sp. indicated that both groups diversified synchronously, plant/arthropod phylogenies are needed as well as experi-
showing that plant lineages possessing the defensive trait mental evolution experiments.
(resin under high pressure) co-evolved with beetles lin-
PLANT–ARTHROPOD COLLABORATIONS
eages equipped with vein-severing ability (Becerra, 2003).
In addition, escalation of species and chemical diversity Interactions between plants and arthropods are not always
through time was observed in Bursera, providing support antagonistic. Insects pollinate about two-thirds of flower-
for the herbivore–plant co-evolution theory (Becerra et al., ing plant species. In reward of nutrient-rich pollen and nec-
2009). Similarly, diversification of milkweeds was corre- tar, insects offer this service as a mutualistic engagement
lated with increased phenolic production (Agrawal et al., (Schoonhoven et al., 2005). Seed dispersal by arthropods,
2009). For evolution of herbivores, a phylogenetic study of mainly ants, helps colonization while providing food for
the leaf miner fly Phytomyza provided evidence that the carrier (Howe and Smallwood, 1982). However, the
repeated shifts to host plants with different chemistry dur- most sophisticated collaboration is the association of
ing 40 million years of evolution led to elevated diversifica- plants with beneficial arthropods to fend off herbivores.
tion (Winkler et al., 2009). Remarkably, beak length of the Plants have evolved exquisite ways to ‘cry for help’, which
seed-eater soapberry bug Jadera haemotoloma has rely on offering refuge or food for guarding predatory
adapted within 40–150 generations after shifting to novel mites and ants, or emitting complex volatiles to attract
© 2017 The Authors

carnivores (for review, see Romero and Benson, 2005; Heil, analyses of biosynthesis pathways across plant taxa and
2008, 2015; Stam et al., 2014; Hilker and Fatouros, 2015). their correlation with associated parasitoids will be neces-
Leaf domatia are cavities or hair tufts on the lower sur- sary to have a better understanding of how indirect
face of leaves, and create shelter for mites that are preda- defense appeared and was maintained. Whether roots
tors of phytophagous mites. Several studies have proven attract beneficial arthropods is another unsolved question.
that these structures benefit plants by decreasing herbi- On the parasitoid side, the advent of more sequenced gen-
vore pressure (for review, see Romero and Benson, 2005). omes may offer a resource for identifying genes important
Extrafloral nectar, food bodies on leaflets and hollow for volatile recognition and association with the host.
thorns are attributes found in certain acacia trees that host Finally, the contribution of parasitoids to plant–arthropod
ants, providing nutrition and housing (Heil, 2008). This inti- co-evolution is also a question that deserves more
mate association is maintained because ants constantly research.
patrol trees and aggressively remove unwanted herbi-
CONCLUSIONS AND OUTLOOK
vores. Extrafloral nectar production is induced in response
to herbivory, showing that plants keep control of this Decades of research on plant–arthropod interactions have
energy-demanding process. In an elegant and long-term revealed that these organisms are engaged in a battle for
experiment in an African savanna, removing large herbi- survival that relys on sophisticated mechanisms of percep-
vores for 10 years reduced nectar production and thorns tion, signaling and defense activation on the plant side,
by Acacia drepanolobium, and increased antagonistic and on effective suppression of defenses and chemical/be-
behavior of the ant mutualist Crematogaster mimosae, havioral adaptations on the arthropod side. Although it
which ultimately led to a decreased tree defense and appears that nature has reached an equilibrium, as both
growth (Palmer et al., 2008). plants and arthropods are abundant, evidence has accumu-
Upon herbivory and detection of HAMPs in OS, plants lated that there is constant innovation to generate novel
emit a complex blend of volatiles that attract parasitic plant defenses strategies and that this exerts a selection
wasps or predators (for review, see Dicke and Loon, 2000; pressure on arthropods to evolve novel effectors or detoxi-
Stam et al., 2014). Volatiles generally consist of terpenes, fication solutions. This arms race has thus no winner and
phenylpropanoids/benzenoids and fatty acid derivatives the co-evolution process may continue for millions of
(green leaf volatiles; Pare and Tumlinson, 1999; Dudareva years.
et al., 2004). This tritrophic interaction is an efficient Although substantial progress has been made in identi-
defense mechanism as carnivores either kill their prey fying genes and molecules involved in the molecular dia-
directly or parasitize them, therefore dramatically reducing log between plants and arthropods, as well as some
feeding activity (Dicke and Loon, 2000). Qualitative and evolutionary processes that underlie their co-evolution, we
quantitative differences in volatile emission explain the have identified open questions that deserve further
specific attraction of parasitoids to their host. For instance, research. In addition, root herbivory (Johnson and Ras-
the specialist parasitic wasp Cardiochiles nigriceps was sig- mann, 2015), insect galls (Stone, 2003), the role of leaf and
nificantly more attracted by the volatile blend produced by arthropod microbiomes (Pineda et al., 2010; Sugio et al.,
tobacco and cotton plants infested with his host H. vires- 2015), and the outcome of multiple biotic interactions (Pie-
cens than by volatiles produced by plants infested with H. terse and Dicke, 2007) are clearly understudied. In times
zea (De Moraes et al., 1998). Similarly, oviposition triggers when stability of ecosystems, emergence of invasive spe-
volatile release and attraction of egg parasitoids, illustrat- cies and sustainable control of insect pests in agriculture
ing the specificity of the emitted blend (Hilker and Fatouros, provide challenges to a growing human population, future
2015). Strikingly, indirect defense was also discovered research on plant–arthropod interactions may contribute
belowground. Upon feeding by the rootworm Diabrotica viable solutions to these problems.
virgifera virgifera, maize roots emit the sesquiterperne (E)-
ACKNOWLEDGEMENTS
b-caryophyllene. However, this response does not attract
arthropods but entomopathogenic nematodes (Figure 1; The authors thank Dr Fabian Schweizer for critically reading the
manuscript. The authors apologize to scientists whose work was
Rasmann et al., 2005).
not mentioned in this review owing to text size limits. The Swiss
Open questions National Science Foundation SNF (grant 31003A_169278 to P.R.)
and the Herbette Foundation (University of Lausanne) supported
One of the fascinating yet poorly studied questions about this work.
plant–arthropod mutualism is how indirect defense
AUTHOR CONTRIBUTIONS
evolved. Evidence that plants benefit from attraction of
parasitoids suggests that genes involved in volatile biosyn- E.S. and P.R. wrote the paper. O.H. provided feedback on
thesis are under positive selection. Comparative genomic the text and designed the figures.
© 2017 The Authors

CONFLICT OF INTEREST Bonaventure, G., VanDoorn, A. and Baldwin, I.T. (2011) Herbivore-asso-
ciated elicitors: FAC signaling and metabolism. Trends Plant Sci., 16,
The authors declare that they have no conflict of interest. 294–299.
Bos, J.I.B., Prince, D., Pitino, M., Maffei, M.E., Win, J. and Hogenhout, S.A.
(2010) A functional genomics approach identifies candidate effectors
from the aphid species Myzus persicae (green peach aphid). PLoS
REFERENCES
Genet., 6, e1001216.
Abe, H., Ohnishi, J., Narusaka, M., Seo, S., Narusaka, Y., Tsuda, S. and Bown, A.W., Hall, D.E. and MacGregor, K.B. (2002) Insect footsteps on
Kobayashi, M. (2008) Function of jasmonate in response and tolerance of leaves stimulate the accumulation of 4-aminobutyrate and can be visual-
Arabidopsis to thrip feeding. Plant Cell Physiol., 49, 68–80. ized through increased chlorophyll fluorescence and superoxide produc-
Acevedo, F.E., Rivera-Vega, L.J., Chung, S.H., Ray, S. and Felton, G.W. tion. Plant Physiol., 129, 1430–1434.
(2015) Cues from chewing insects – the intersection of DAMPs, HAMPs, Bown, A.W., MacGregor, K.B. and Shelp, B.J. (2006) Gamma-aminobuty-
MAMPs and effectors. Curr. Opin. Plant Biol., 26, 80–86. rate: defense against invertebrate pests? Trends Plant Sci., 11, 424–
Acosta, I.F. and Farmer, E.E. (2010) Jasmonates. Arabidopsis Book, 1–13. 427.
Agrawal, A.A., Salminen, J.-P. and Fishbein, M. (2009) Phylogenetic trends Bozorov, T.A., Dinh, S.T. and Baldwin, I.T. (2017) JA but not JA-Ile is the
in phenolic metabolism of milkweeds (Asclepias): evidence for escala- cell-nonautonomous signal activating JA mediated systemic defenses to
tion. Evolution, 63, 663–673. herbivory in Nicotiana attenuata. J. Integr. Plant Biol., 59, 552–571.
Agrawal, A.A., Hastings, A.P., Johnson, M.T.J., Maron, J.L. and Salminen, Bretschneider, A., Heckel, D.G. and Vogel, H. (2016) Know your ABCs: char-
J.-P. (2012) Insect herbivores drive real-time ecological and evolutionary acterization and gene expression dynamics of ABC transporters in the
change in plant populations. Science, 338, 113–116. polyphagous herbivore Helicoverpa armigera. Insect Biochem. Mol. Biol.,
Alborn, H.T., Turlings, T.C.J., Jones, T., Stenhagen, G., Loughrin, J.H. and 72, 1–9.
Tumlinson, J.H. (1997) An elicitor of plant volatiles from beet armyworm Bricchi, I., Leitner, M., Foti, M., Mitho€ fer, A., Boland, W., Massimo, E. and
oral secretion. Science, 276, 945–949. Maffei, M.E. (2010) Robotic mechanical wounding (MecWorm) versus
Alborn, H.T., Hansen, T.V., Jones, T.H., Bennett, D.C., Tumlinson, J.H., Sch- herbivore-induced responses: early signaling and volatile emission in
melz, E.A. and Teal, P.E.A. (2007) Disulfooxy fatty acids from the Ameri- Lima bean (Phaseolus lunatus L.). Planta, 232, 719–729.
can bird grasshopper Schistocerca americana, elicitors of plant volatiles. Bricchi, I., Occhipinti, A., Bertea, C.M. et al. (2013) Separation of early and
Proc. Natl Acad. Sci. USA, 104, 12 976–12 981. late responses to herbivory in Arabidopsis by changing plasmodesmal
Ament, K., Kant, M.R., Sabelis, M.W., Haring, M.A. and Schuurink, R.C. function. Plant J., 73, 14–25.
(2004) Jasmonic acid is a key regulator of spider mite-induced volatile Bridges, M., Jones, A.M.E., Bones, A.M., Hodgson, C., Cole, R., Bartlet, E.,
terpenoid and methyl salicylate emission in tomato. Plant Physiol., 135, Wallsgrove, R., Karapapa, V.K., Watts, N. and Rossiter, J.T. (2002) Spatial
2025–2037. organization of the glucosinolate-myrosinase system in brassica specia-
Atamian, H.S., Chaudhary, R., Cin, V.D., Bao, E., Girke, T. and Kaloshian, I. lists aphids is similar to that of the host plant. Proc. R. Soc. Lond., B 269,
(2013) In planta expression or delivery of potato aphid Macrosiphum 187–191.
euphorbiae effectors Me10 and Me23 enhances aphid fecundity. Mol. Brock, A., Herzfeld, T., Paschke, R., Koch, M. and Dra€ger, B. (2006) Brassi-
Plant Microbe Interact., 26, 67–74. caceae contain nortropane alkaloids. Phytochemistry, 67, 2050–2057.
Barbeta, B.L., Marshall, A.T., Gillon, A.D., Craik, D.J. and Anderson, M.A. Brown, K.K. and Hampton, M.B. (2011) Biological targets of isothiocyanates.
(2008) Plant cyclotides disrupt epithelial cells in the midgut of lepi- Biochem. Biophys. Acta., 1810, 888–894.
dopteran larvae. Proc. Natl Acad. Sci. USA, 105, 1221–1225. Browse, J. (2009) Jasmonate passes muster: a receptor and targets for the
Barth, C. and Jander, G. (2006) Arabidopsis myrosinases TGG1 and TGG2 defense hormone. Annu. Rev. Plant Biol., 60, 183–205.
have redundant function in glucosinolate breakdown and insect defense. Bruessow, F., Gouhier-Darimont, C., Buchala, A., Metraux, J.-P. and Rey-
Plant J., 46, 549–562. mond, P. (2010) Insect eggs suppress plant defence against chewing her-
Bayes, A., Comellas-Bigler, M., deRodrıguez la Vega, M., Maskos, K., Bode, bivores. Plant J., 62, 876–885.
W., Aviles, F.X., Jongsma, M.A., Beekwilder, J. and Vendrell, J. (2005) Carlini, C.R. and Grossi-de-Sa, M.F. (2002) Plant toxic proteins with insectici-
Structural basis of the resistance of an insect carboxypeptidase to plant dal properties. A review on their potentialities as bioinsecticides. Toxi-
protease inhibitors. Proc. Natl Acad. Sci. USA, 102, 16 602–16 607. con, 40, 1515–1539.
Becerra, J.X. (2003) Synchronous coadaptation in an ancient case of her- Carlini, C.R., Oliveira, A.E., Azambuja, P., Xavier-Filho, J. and Wells, M.A.
bivory. Proc. Natl Acad. Sci. USA, 100, 12 804–12 807. (1997) Biological effects of canatoxin in different insect models: evidence
Becerra, J.X., Noge, K. and Venable, D.L. (2009) Macroevolutionary chemi- for a proteolytic activation of the toxin by insect cathepsinlike enzymes.
cal escalation in an ancient plant-herbivore arms race. Proc. Natl Acad. J. Econ. Entomol., 90, 340–348.
Sci. USA, 106, 18 062–18 066. Carroll, S. (1992) Host race radiation in the soapberry bug: natural history
Bede, J.C., Musser, R.O., Felton, G.W. and Korth, K.L. (2006) Caterpillar her- with the history. Evolution, 46, 1053–1069.
bivory and salivary enzymes decrease transcript levels of Medicago trun- Casida, J.E., Gammon, D.W., Glickman, A.H. and Lawrence, L.J. (1983)
catula genes encoding early enzymes in terpenoid biosynthesis. Plant Mechanism of pyrethroid insecticides. Annu. Rev. Pharmacol. Toxicol.,
Mol. Biol., 60, 519–531. 23, 413–418.
Beekwilder, J., van Leeuwen, W., van Dam, N.M. et al. (2008) The impact of Casteel, C.L., Walling, L.L. and Paine, T.D. (2006) Behavior and biology of
the absence of aliphatic glucosinolates on insect herbivory in Arabidop- the tomato psyllid, Bactericerca cockerelli, in response to the Mi-1.2
sis. PLoS ONE, 3, e2068. gene. Entomol. Exp. Appl., 121, 67–72.
Beran, F., Pauchet, Y., Kunert, G. et al. (2014) Phyllotreta striolata flea bee- Casteel, C.L., De Alwis, M., Bak, A., Dong, H., Whitham, S.A. and Jander, G.
tles use host plant defense compounds to create their own glucosino- (2015) Disruption of ethylene responses by turnip mosaic virus mediates
late-myrosinase system. Proc. Natl Acad. Sci. USA, 111, 7349–7354. suppression of plant defense against the green peach aphid vector. Plant
Bleeker, P.M., Mirabella, R., Diergaarde, P.J., VanDoorn, A., Tissier, A., Kant, Physiol., 169, 209–218.
M.R., Prins, M., deVos, M., Haring, M.A. and Schuurink, R.C. (2012) Chaudhary, R., Atamian, H.S., Shen, Z., Briggs, S.P. and Kaloshian, I.
Improved herbivore resistance in cultivated tomato with the sesquiter- (2014) GroEL from the endosymbiont Buchnera aphidicola betrays the
pene biosynthetic pathway from a wild relative. Proc. Natl Acad. Sci. aphid by triggering plant defense. Proc. Natl Acad. Sci. USA, 111,
USA, 109, 20 124–20 129. 8919–8924.
Bodenhausen, N. and Reymond, P. (2007) Signaling pathways controlling Chen, H., Wilkerson, C.G., Kuchar, J.A., Phinney, B.S. and Howe, G.A.
induced resistance to insect herbivores in Arabidopsis. Mol. Plant (2005) Jasmonate-inducible plant enzymes degrade essential amino
Microbe Interact., 20, 1406–1420. acids in the herbivore midgut. Proc. Natl Acad. Sci. USA, 101, 19 237–
Boller, T. and Felix, G. (2009) A renaissance of elicitors: perception of 19 242.
microbe-associated molecular patterns and danger signals by pattern- Chini, A., Fonseca, S., Fernandez, G. et al. (2007) The JAZ family of repres-
recognition receptors. Annu. Rev. Plant Biol., 60, 379–406. sors is the missing link in jasmonate signalling. Nature, 448, 666–671.
© 2017 The Authors

Choi, J., Tanaka, K., Cao, Y., Qi, Y., Qiu, J., Liang, Y., Lee, S.Y. and Stacey, Dudareva, N., Pichersky, E. and Gershenzon, J. (2004) Biochemistry of plant
G. (2014) Identification of a plant receptor for extracellular ATP. Science, volatiles. Plant Physiol., 135, 1893–1902.
343, 290–294. deDuge Bernonville, T., Carqueijeiro, I., Lanoue, A. et al. (2017) Folivory elic-
Chung, S.H., Rosa, C., Scully, E.D., Peiffer, M., Tooker, J.F., Hoover, K., its a strong defense reaction in Catharanthus roseus: metabolomic and
Luthe, D.S. and Felton, G.W. (2013) Herbivore exploits orally secreted transcriptomic analyses reveal distinct local and systemic responses. Sci.
bacteria to suppress plant defenses. Proc. Natl Acad. Sci. USA, 110, 15 Rep., 7, 40 453.
728–15 733. Dunse, K.M., Kaas, Q., Guarino, R.F., Barton, P.A., Craik, D.J. and Anderson,
Consales, F., Schweizer, F., Erb, M., Gouhier-Darimont, C., Bodenhausen, N., M.A. (2010) Molecular basis for the resistance of an insect chymotrypsin
Bruessow, F., Sobhy, I. and Reymond, P. (2012) Insect oral secretions sup- to a potato type II proteinase inhibitor. Proc. Natl Acad. Sci. USA, 107,
press wound-induced responses in Arabidopsis. J. Exp. Bot., 63, 727–737. 15 016–15 021.
Couto, D. and Zipfel, C. (2016) Regulation of pattern recognition receptor Dussourd, D.E. (2017) Behavioral sabotage of plant defenses by insect foli-
signalling in plants. Nat. Rev. Immunol., 16, 537–552. vores. Annu. Rev. Entomol., 62, 15–34.
Dayan, F.E., Cantrell, C.L. and Duke, S.O. (2009) Natural products in crop Dussourd, D. and Eisner, T. (1987) Vein-cutting behavior: insect counterploy
protection. Bioorg. Med. Chem., 17, 4022–4034. to the latex defense of plants. Science, 237, 898–901.
De Moraes, C.M. and Mescher, M.C. (2004) Biochemical crypsis in the avoid- Edger, P.P., Heidel-Fischer, H.M., Bekaert, M. et al. (2015) The butterfly plant
ance of natural enemies by an insect herbivore. Proc. Natl Acad. Sci. arms-race escalated by gene and genome duplications. Proc. Natl Acad.
USA, 101, 8993–8997. Sci. USA, 112, 8362–8366.
De Moraes, C.M., Lewis, W.J., Pare, P.W., Alborn, H.T. and Tumlinson, J.H. Ehrlich, P. and Raven, P.H. (1964) Butterflies and plants: a study in coevolu-
(1998) Herbivore-infested plants selectively attract parasitoids. Nature, tion. Evolution, 18, 586–608.
393, 570–573. Eisner, T., Eisner, M., Aneshansley, D.J., Wu, C. and Meinwald, J. (2000)
Delledonne, M., Allegro, G., Belenghi, B., Balestrazzi, A., Picco, F., Levine, A., Chemical defense of the mint plant, Teucrium marum (Labiatae). Che-
Zelasco, S., Calligari, P. and Confalonieri, M. (2001) Transformation of white moecology, 4, 211–216.
poplar (Populus alba L.) with a novel Arabidopsis thaliana cysteine pro- Ellis, C., Karafyllidis, L. and Turner, J.G. (2002) Constitutive activation of jas-
teinase inhibitor and analysis of insect pest resistance. Mol. Breed., 7, 35–42. monate signaling in an Arabidopsis mutant correlates with enhanced
Dermauw, W. and Van Leeuwen, T. (2014) The ABC gene family in arthro- resistance to Erysiphe cichoracearum, Pseudomonas syringae, and
pods: comparative genomics and role in insecticide transport and resis- Myzus persicae. Mol. Plant Microbe Interact., 15, 1025–1030.
tance. Insect Biochem. Mol. Biol., 45, 89–110. Elzinga, D.A., de Vos, M. and Jander, G. (2014) Suppression of plant
Dermauw, W., Osborne, E.J., Clark, R.M., Grbic, M., Tirry, L. and Van Leeu- defenses by a Myzus persicae (green peach aphid) salivary effector pro-
wen, T. (2013a) A burst of ABC genes in the genome of the polyphagous tein. Mol. Plant Microbe Interact., 27, 747–756.
spider mite Tetranychus urticae. BMC Genom., 14, 317. Engler, H.S., Spencer, K.C. and Gilbert, L.E. (2000) Preventing cyanide
Dermauw, W., Wybouw, N., Rombauts, S., Menten, B., Vontas, J., Grbic, M., release from leaves. Nature, 406, 144–145.
Clark, R.M., Feyereisen, R. and Van Leeuwen, T. (2013b) A link between Erb, M., Meldau, S. and Howe, G.A. (2012) Role of phytohormones in
host plant adaptation and pesticide resistance in the polyphagous spider insect-specific plant reactions. Trends Plant Sci., 17, 250–259.
mite Tetranychus urticae. Proc. Natl Acad. Sci. USA, 110, E113–E122. Fabre, C., Causse, H., Mourey, L., Koninkx, J., Riviere, M., Hendriks, H.,
Deslandes, L. and Rivas, S. (2012) Catch me if you can: bacterial effectors Puzo, G., Samama, J.P. and Rouge, P. (1998) Characterization and sugar
and plant targets. Trends Plant Sci., 17, 644–655. binding properties of arcelin-1, an insecticidal lectin-like protein isolated
Despres, L., David, J.-P. and Gallet, C. (2007) The evolutionary ecology of from kidney bean (Phaseolus vulgaris L. cv RAZ-2) seeds. Biochem. J.,
insect resistance to plant chemicals. Trends Ecol. Evol., 22, 298–307. 329, 551–560.
Dicke, M. and Loon, J.J.A. (2000) Multitrophic effects of herbivore-induced Falk, K.L. and Gershenzon, J. (2007) The desert locust, Schistocerca gre-
plant volatiles in an evolutionary context. Entomol. Exp. Appl., 97, 237– garia, detoxifies the glucosinolates of Schouwia purpurea by desulfation.
249. J. Chem. Ecol., 33, 1542–1555.
Diezel, C., Von Dahl, C.C., Gaquerel, E. and Baldwin, I.T. (2009) Different Farmer, E.E. (2014) Leaf Defence. Oxford: OUP.
lepidopteran elicitors account for cross-talk in herbivory-induced phyto- Farmer, E.E. and Dubugnon, L. (2009) Detritivorous crustaceans become
hormone signaling. Plant Physiol., 150, 1576–1586. herbivores on jasmonate-deficient plants. Proc. Natl Acad. Sci. USA, 106,
Diezel, C., Kessler, D. and Baldwin, I.T. (2011) Pithy protection: Nicotiana 935–940.
attenuata’s jasmonic acid-mediated defenses are required to resist stem- Farmer, E.E., Gasperini, D. and Acosta, I.F. (2014) The squeeze cell hypothe-
boring weevil larvae. Plant Physiol., 155, 1936–1946. sis for the activation of jasmonate synthesis in response to wounding.
Dobler, S., Dalla, S., Wagschal, V. and Agrawal, A.A. (2012) Community- New Phytol., 204, 282–288.
wide convergent evolution in insect adaptation to toxic cardenolides by Fatouros, N.E., Broekgaarden, C., Bukovinszkine’kiss, G., vanLoon, J.J.A.,
substitutions in the Na,K-ATPase. Proc. Natl Acad. Sci. USA, 109, 13 040– Mumm, R., Huigens, M.E., Dicke, M. and Hilker, M. (2008) Male-derived
13 045. butterfly anti-aphrodisiac mediates induced indirect plant defense. Proc.
Dodds, P.N., Rafiqi, M., Gan, P.H.P., Hardham, A.R., Jones, D.A. and Ellis, Natl Acad. Sci. USA, 105, 10 033–10 038.
J.G. (2009) Effectors of biotrophic fungi and oomycetes: pathogenicity Fatouros, N.E., Pashalidou, F.G., Cordero, W.V.A., Loon, J.J.A., Mumm,
factors and triggers of host resistance. New Phytol., 183, 993–1000. R., Dicke, M., Hilker, M. and Huigens, M.E. (2009) Anti-aphrodisiac
Dogimont, C., Chovelon, V., Pauquet, J., Boualem, A. and Bendahmane, A. compounds of male butterflies increase the risk of egg parasitoid
(2014) The Vat locus encodes for a CC-NBS-LRR protein that confers attack by inducing plant synomone production. J. Chem. Ecol., 35,
resistance to Aphis gossypii infestation and A. gossypii-mediated virus 1373–1381.
resistance. Plant J., 80, 993–1004. Fernandez-Calvo, P., Chini, A., Fernandez-Barbero, G. et al. (2011) The Ara-
Doss, R.P., Oliver, J.E., Proebsting, W.M., Potter, S.W., Kuy, S., Clement, bidopsis bHLH transcription factors MYC3 and MYC4 are targets of JAZ
S.L., Williamson, R.T., Carney, J.R. and DeVilbiss, E.D. (2000) Bruchins: repressors and act additively with MYC2 in the activation of jasmonate
insect-derived plant regulators that stimulate neoplasm formation. Proc. responses. Plant Cell, 23, 701–715.
Natl Acad. Sci. USA, 97, 6218–6223. Fonseca, S., Chini, A., Hamberg, M., Adie, B.A.T., Porzel, A., Kramell, R.,
Drurey, C., Mathers, T.C., Prince, D.C., Wilson, C., Caceres-Moreno, C., Mug- Miersch, O., Wasternack, C. and Solano, R. (2009) (+)-7-iso-Jasmonoyl-L-
ford, S.T. and Hogenhout, S.A. (2017) Chemosensory proteins in the isoleucine is the endogenous bioactive jasmonate. Nat. Chem. Biol., 5,
CSP4 clade evolved as plant immunity suppressors before two suborders 344–350.
of plant-feeding hemipteran insects diverged. BioRxiv, https://doi.org/10. Franco, O.L., Rigden, D.J., Melo, F.R. and Grossi-De-Sa, M.F. (2002) Plant
1101/173278. alpha-amylase inhibitors and their interaction with insect alpha-amy-
Du, B., Zhang, W., Liu, B. et al. (2009) Identification and characterization of lases. Eur. J. Biochem., 269, 397–412.
Bph14, a gene conferring resistance to brown planthopper in rice. Proc. Frerigmann, H. (2016) Glucosinolate regulation in a complex relationship – MYC
Natl Acad. Sci. USA, 106, 22 163–22 168. and MYB – no one can act without each other. Adv. Bot. Res., 80, 57–97.
© 2017 The Authors

Futuyma, D.J. and Agrawal, A.A. (2009) Macroevolution and the biological Hilfiker, O., Groux, R., Bruessow, F., Kiefer, K., Zeier, J. and Reymond, P.
diversity of plants and herbivores. Proc. Natl Acad. Sci. USA, 106, 18 (2014) Insect eggs induce a systemic acquired resistance in Arabidopsis.
054–18 061. Plant J., 80, 1085–1094.
Gaquerel, E., Weinhold, A. and Baldwin, I.T. (2009) Molecular interactions Hilker, M. and Fatouros, N.E. (2015) Plant responses to insect egg deposi-
between the specialist herbivore Manduca sexta (Lepidoptera, Sphigi- tion. Annu. Rev. Entomol., 60, 493–515.
dae) and its natural host Nicotiana attenuata. VIII. An unbiased GCxGC- Hilker, M., Kobs, C., Varama, M. and Schrank, K. (2002) Insect egg deposi-
ToFMS analysis of the plant’s elicited volatile emissions. Plant Physiol., tion induces Pinus sylvestris to attract egg parasitoids. J. Exp. Biol., 205,
149, 1408–1423. 455–461.
Gasperini, D., Chauvin, A., Acosta, I.F., Kurenda, A., Stolz, S., Chetelat, A., Hilker, M., Stein, C., Schro € der, R., Varama, M. and Mumm, R. (2005) Insect
Wolfender, J.-L. and Farmer, E.E. (2015) Axial and radial oxylipin trans- egg deposition induces defence responses in Pinus sylvestris: characteri-
port. Plant Physiol., 169, 2244–2254. sation of the elicitor. J. Exp. Biol., 208, 1849–1854.
Gepner, J.I., Hall, L.M. and Sattelle, D.B. (1978) Insect acetylcholine recep- Hogenhout, S.A. and Bos, J.I.B. (2011) Effector proteins that modulate
tors as a site of insecticide action. Nature, 276, 188–190. plant–insect interactions. Curr. Opin. Plant Biol., 14, 422–428.
Gimenez-Ibanez, S., Boter, M., Fernandez-Barbero, G., Chini, A., Rathjen, Holzinger, F. and Wink, M. (1996) Mediation of cardiac glycoside insensitiv-
J.P. and Solano, R. (2014) The bacterial effector HopX1 targets JAZ tran- ity in the monarch butterfly (Danaus plexippus): role of an amino acid
scriptional repressors to activate jasmonate signaling and promote infec- substitution in the ouabain binding site of Na+, K+-ATPase. J. Chem.
tion in Arabidopsis. PLoS Biol., 12, e1001792. Ecol., 22, 1921–1937.
Glauser, G., Grata, E., Dubugnon, L., Rudaz, S., Farmer, E.E. and Wolfender, Hosie, A.M., Aronstein, K., Sattelle, D.B. and ffrench-Constant, R.H. (1997)
J.L. (2008) Spatial and temporal dynamics of jasmonate synthesis and Molecular biology of insect neuronal GABA receptors. Trends Neurosci.,
accumulation in Arabidopsis in response to wounding. J. Biol. Chem., 20, 578–589.
283, 16 400–16 407. Howe, G.A. and Jander, G. (2008) Plant immunity to insect herbivores.
Gloss, A.D., Vassa~o, D.G., Hailey, A.L. et al. (2014) Evolution in an ancient Annu. Rev. Plant Biol., 59, 41–66.
detoxification pathway is coupled with a transition to herbivory in the Howe, H.F. and Smallwood, J. (1982) Ecology of seed dispersal. Annu. Rev.
drosophilidae. Mol. Biol. Evol., 31, 2441–2456. Ecol. Syst., 13, 201–228.
Gonzales-Vigil, E., Bianchetti, C.M., Phillips, G.N. Jr and Howe, G.A. (2011) Huang, T., Jander, G. and de Vos, M. (2011) Non-protein amino acids in
Adaptive evolution of threonine deaminase in plant defense against plant defense against insect herbivores: representative cases and
insect herbivores. Proc. Natl Acad. Sci. USA, 108, 5897–5902. opportunities for further functional analysis. Phytochemistry, 72, 1531–
Gouhier-Darimont, C., Schmiesing, A., Bonnet, C., Lassueur, S. and Rey- 1537.
mond, P. (2013) Signalling of Arabidopsis thaliana response to Pieris Huber, A.E. and Bauerle, T.L. (2016) Long-distance plant signaling pathways
brassicae eggs shares similarities with PAMP-triggered immunity. J. Exp. in response to multiple stressors: the gap in knowledge. J. Exp. Bot., 67,
Bot., 64, 665–674. 2063–2079.
Grbic, M., Van Leeuwen, T., Clark, R.M. et al. (2011) The genome of Huber, M., Epping, J., Schulze Gronover, C. et al. (2016) A latex metabolite
Tetranychus urticae reveals herbivorous pest adaptations. Nature, 479, benefits plant fitness under root herbivore attack. PLoS Biol., 14,
487–492. e1002332.
Green, T.R. and Ryan, C.A. (1972) Wound-induced proteinase inhibitor in Hung, C.F., Berenbaum, M.R. and Schuler, M.A. (1997) Isolation and charac-
plant leaves: a possible defense mechanism against insects. Science, terization of CYP6B4, a furanocoumarin-inducible cytochrome P450 from
175, 776–777. a polyphagous caterpillar (Lepidoptera:papilionidae). Insect Biochem.
Guo, H., Wielsch, N., Hafke, J.B., Svatos, A., Mitho € fer, A. and Boland, W. Mol. Biol., 27, 377–385.
(2013) A porin-like protein from oral secretions of Spodoptera littoralis Isman, M.B. (2006) Botanical insecticides, deterrents, and repellents in mod-
larvae induces defense-related early events in plant leaves. Insect Bio- ern agriculture and an increasingly regulated world. Annu. Rev. Ento-
chem. Mol. Biol., 43, 849–858. mol., 51, 45–66.
Gururani, M.A., Venkatesh, J., Upadhyaya, C.P., Nookaraju, A., Pandey, S.K. Jaouannet, M., Rodriguez, P.A., Thorpe, P., Lenoir, C.J.G., MacLeod, R.,
and Park, S.W. (2012) Plant disease resistance genes: current status and Escudero-Martinez, C. and Bos, J.I.B. (2014) Plant immunity in plant-
future directions. Physiol. Mol. Plant Pathol., 78, 51–65. aphid interactions. Front. Plant-Microbe Interact., 5, 663.
Halitschke, R., Schittko, U., Pohnert, G., Boland, W. and Baldwin, I.T. (2001) Jennings, C., West, J., Waine, C., Craik, D. and Anderson, M. (2001) Biosyn-
Molecular interactions between the specialist herbivore Manduca sexta thesis and insecticidal properties of plant cyclotides: the cyclic knotted
(Lepidoptera, Sphingidae) and its natural host Nicotiana attenuata. III. proteins from Oldenlandia affinis. Proc. Natl Acad. Sci. USA, 98, 10 614–
Fatty acid-amino acid conjugates in herbivore oral secretions are neces- 10 619.
sary and sufficient for herbivore-specific plant responses. Plant Physiol., Johnson, S.N. and Rasmann, S. (2015) Root-feeding insects and their inter-
125, 711–717. actions with organisms in the rhizosphere. Annu. Rev. Entomol., 60, 517–
Handrick, V., Robert, C.A., Ahern, K.R. et al. (2016) Biosynthesis of 8-o- 535.
methylated benzoxazinoid defense compounds in maize. Plant Cell, 28, Jones, J.D.G. and Dangl, J.L. (2006) The plant immune system. Nature, 444,
1682–1700. 323–329.
Harfouche, A.L., Shivaji, R., Stocker, R., Williams, P.W. and Luthe, D.S. Kang, J.-H., Liu, G., FShi, F., Jones, A.D., Beaudry, R.M. and Howe, G.A.
(2006) Ethylene signaling mediates a maize defense response to insect (2010) The tomato odorless-2 mutant is defective in trichome-based pro-
herbivory. Mol. Plant Microbe Interact., 19, 189–199. duction of diverse specialized metabolites and broad-spectrum resis-
Hartl, M., Giri, A.P., Kaur, H. and Baldwin, I.T. (2010) Serine protease inhibi- tance to insect herbivores. Plant Physiol., 154, 262–272.
tors specifically defend Solanum nigrum against generalist herbivores but Kant, M.R., Sabelis, M.W., Haring, M.A. and Schuurink, R.C. (2008) Intraspeci-
do not influence plant growth and development. Plant Cell, 22, 4158–4175. fic variation in a generalist herbivore accounts for differential induction
Hartley, S.E. and DeGabriel, J.L. (2016) The ecology of herbivore-induced and impact of host plant defences. Proc. R. Soc. B, 275, 443–452.
silicon defences in grasses. Funct. Ecol., 30, 1311–1322. Katoh, A., Ohki, H., Inai, K. and Hashimoto, T. (2005) Molecular regulation
Heidel-Fischer, H.M. and Vogel, H. (2015) Molecular mechanisms of insect of nicotine biosynthesis. Plant Biotechnol., 22, 389–392.
adaptation to plant secondary compounds. Curr. Opin. Insect Sci., 8, 8–14. Kazana, E., Pope, T.W., Tibbles, L., Bridges, M., Pickett, J.A., Bones, A.M.,
Heil, M. (2008) Indirect defence via tritrophic interactions. New Phytol., 178, Powell, G. and Rossiter, J.T. (2007) The cabbage aphid: a walking mus-
41–61. tard oil bomb. Proc. Biol. Sci. B, 274, 2271–2277.
Heil, M. (2015) Extrafloral nectar at the plant-insect interface: a spotlight on Kessler, D., Diezel, C. and Baldwin, I.T. (2010) Changing pollinators as a
chemical ecology, phenotypic plasticity, and food webs. Annu. Rev. means of escaping herbivores. Curr. Biol., 20, 237–242.
Entomol., 60, 213–232. Kettles, G.J., Drurey, C., Schoonbeek, H.J., Maule, A.J. and Hogenhout, S.A.
Herde, M. and Howe, G.A. (2014) Host plant-specific remodeling of midgut (2013) Resistance of Arabidopsis thaliana to the green peach aphid,
physiology in the generalist insect herbivore Trichoplusia ni. Insect Bio- Myzus persicae, involves camalexin and is regulated by microRNAs.
chem. Mol. Biol., 50, 58–67. New Phytol., 198, 1178–1190.
© 2017 The Authors

Kivima€ki, M., Ka€ rkka€inen, K., Gaudeul, M., Løe, G. and Agren, J. (2007) Li, R., Weldegergis, B.T., Li, J. et al. (2014) Virulence factors of geminivirus
Gene, phenotype and function: GLABROUS1 and resistance to herbivory interact with MYC2 to subvert plant resistance and promote vector per-
in natural populations of Arabidopsis lyrata. Mol. Ecol., 16, 453–462. formance. Plant Cell, 26, 4991–5008.
Klingler, J.P., Nair, R.M., Edwards, O.R. and Singh, K.B. (2009) A single Li, B., Meng, X., Shan, L. and He, P. (2016) Transcriptional regulation of pat-
gene, AIN, in Medicago truncatula mediates a hypersensitive response tern-triggered immunity in plants. Cell Host Microbe, 19, 641–650.
to both bluegreen aphid and pea aphid, but confers resistance only to Lindroth, R.L. and Weisbrod, A.V. (1991) Genetic variation in response of
bluegreen aphid. J. Exp. Bot., 60, 4115–4127. the gypsy moth to aspen phenolic glycosides. Biochem. Syst. Ecol., 19,
Koiwa, H., Shade, R.E., Zhu-Salzman, K., Subramanian, L., Murdock, L.L., 97–103.
Nielsen, S.S., Bressan, R.A. and Hasegawa, P.M. (1998) Phage display Little, D., Gouhier-Darimont, C., Bruessow, F. and Reymond, P. (2007)
selection can differentiate insecticidal activity of soybean cystatins. Plant Oviposition by pierid butterflies triggers defense responses in Arabidop-
J., 14, 371–379. sis. Plant Physiol., 143, 784–800.
Koo, A.J.K., Gao, X., Jone, A.D. and Howe, G.A. (2009) A rapid wound signal Liu, Y., Ahn, J.E., Datta, S., Salzman, R.A., Moon, J., Huyghues-Despointes,
activates the systemic synthesis of bioactive jasmonates in Arabidopsis. B., Pittendrigh, B., Murdock, L.L., Koiwa, H. and Zhu-Salzman, K. (2005)
Plant J., 59, 974–986. Arabidopsis vegetative storage protein is an anti-insect acid phos-
Koornneef, A. and Pieterse, C.M.J. (2008) Cross talk in defense signaling. phatase. Plant Physiol., 139, 1545–1556.
Plant Physiol., 146, 839–844. Liu, Y., Wu, H., Chen, H. et al. (2015) A gene cluster encoding lectin receptor
Korth, K.L., Doege, S.J., Park, S.H., Goggin, F.L., Wang, Q., Gomez, S.K., kinases confers broad-spectrum and durable insect resistance in rice.
Liu, G., Jia, L. and Nakata, P.A. (2006) Medicago truncatula mutants Nat. Biotechnol., 33, 301–305.
demonstrate the role of plant calcium oxalate crystals as an effective Louis, J. and Shah, J. (2015) Plant defence against aphids: the PAD4 sig-
defense against chewing insects. Plant Physiol., 141, 188–195. nalling nexus. J. Exp. Bot., 66, 449–454.
Krempl, C., Sporer, T., Reichelt, M., Ahn, S.-J., Heidel-Fischer, H., Vogel, H., Lozano-Duran, R., Rosas-Dıaz, T., Gusmaroli, G., Luna, A.P., Taconnat, L.,
Heckel, D.G. and Joußen, N. (2016) Potential detoxification of gossypol Deng, X.W. and Bejarano, E.R. (2011) Geminiviruses subvert ubiquitina-
by UDP-glycosyltransferases in the two Heliothine moth species Helicov- tion by altering CSN-mediated derubylation of SCF E3 ligase complexes
erpa armigera and Heliothis virescens. Insect Biochem. Mol. Biol., 71, and inhibit jasmonate signaling in Arabidopsis thaliana. Plant Cell, 23,
49–57. 1014–1032.
Kumar, P., Pandit, S.S., Steppuhn, A. and Baldwin, I.T. (2014) Natural his- Lu, J., Robert, C.A.M., Riemann, M. et al. (2015) Induced jasmonate signal-
tory-driven, plant-mediated RNAi-based study reveals CYP6B46’s role in ing leads to contrasting effects on root damage and herbivore perfor-
a nicotine-mediated antipredator herbivore defense. Proc. Natl Acad. Sci. mance. Plant Physiol., 167, 1100–1116.
USA, 111, 1245–1252. Luan, J.-B., Yao, D.-M., Zhang, T., Walling, L.L., Yang, M., Wang, Y.-J. and
Kuroda, M., Ishimoto, M., Suzuki, K., Kondo, H., Abe, K., Kitamura, K. and Liu, S.-S. (2013) Suppression of terpenoid synthesis in plants by a virus
Arai, S. (1996) Oryzacystatins exhibit growth-inhibitory and lethal effects promotes its mutualism with vectors. Ecol. Lett., 16, 390–398.
on different species of bean insect pests, Callosobruchus chinensis Luu, V.T., Weinhold, A., Ullah, C., Dressel, S., Schoettner, M., Gase, K.,
(Coleoptera) and Riptortus clavatus (Hemiptera). Biosci. Biotech. Bio- Gaquerel, E., Xu, S. and Baldwin, I.T. (2017) O-Acyl sugars protect a wild
chem., 60, 209–212. tobacco from both native fungal pathogens and a specialist herbivore.
Kusnierczyk, A., Winge, P., Jørstad, T.S., Troczynska, J., Rossiter, J.T. and Plant Physiol., 174, 370–386.
Bones, A.M. (2008) Towards global understanding of plant defence Maddrell, S.H. and Gardiner, B.O. (1976) Excretion of alkaloids by malpigh-
against aphids – timing and dynamics of early Arabidopsis defence ian tubules of insects. J. Exp. Biol., 64, 267–281.
responses to cabbage aphid (Brevicoryne brassicae) attack. Plant, Cell Madsen, S.R., Kunert, G., Reichelt, M., Gershenzon, J. and Halkier, B.A.
Environ., 31, 1097–1115. (2015) Feeding on leaves of the glucosinolate transporter mutant gtr1gtr2
Lait, C.G., Alborn, H.T., Teal, P.E.A. and Tumlinson, J.H. (2003) Rapid reduces fitness of Myzus persicae. J. Chem. Ecol., 41, 975–984.
biosynthesis of N-linolenoyl-L-glutamine, an elicitor of plant volatiles, by Major, I.T. and Constabel, C.P. (2006) Molecular analysis of poplar defense
membrane-associated enzyme(s) in Manduca sexta. Proc. Natl Acad. Sci. against herbivory: comparison of wound- and insect elicitor-induced
USA, 100, 7027–7032. gene expression. New Phytol., 172, 617–635.
Lawrence, S.D., Novak, N.G. and Blackburn, M.B. (2007) Inhibition of pro- Major, I.T., Yoshida, Y., Campos, M.L., Kapali, G., Xin, X.F., Sugimoto, K.,
teinase inhibitor transcripts by Leptinotarsa decemlineata regurgitant in De Oliveira Ferreira, D., He, S.Y. and Howe, G.A. (2017) Regulation of
Solanum lycopersicum. J. Chem. Ecol., 33, 1041–1048. growth–defense balance by the JASMONATE ZIM-DOMAIN (JAZ)-MYC
Lei, J., Finlayson, S.A., Salzman, R.A., Shan, L. and Zhu-Salzman, K. (2014) transcriptional module. New Phytol., 215, 1533–1547.
BOTRYTIS-INDUCED KINASE1 modulates Arabidopsis resistance to Martin, D., Tholl, D., Gershenzon, J. and Bohlmann, J. (2002) Methyl jas-
green peach aphids via PHYTOALEXIN DEFICIENT4. Plant Physiol., 165, monate induces traumatic resin ducts, terpenoid resin biosynthesis, and
1665–1670. terpenoid accumulation in developing xylem of Norway spruce stems.
Lewsey, M.G., Murphy, A.M., Maclean, D. et al. (2010) Disruption of two Plant Physiol., 129, 1003–1018.
defensive signaling pathways by a viral RNA silencing suppressor. Mol. Massey, F.P. and Hartley, S.E. (2009) Physical defences wear you down: pro-
Plant Microbe Interact., 23, 835–845. gressive and irreversible impacts of silica on insect herbivores. J. Animal
Li, L., Li, C., Lee, G.I. and Howe, G.A. (2002a) Distinct roles for jasmonate Ecol., 78, 281–291.
synthesis and action in the systemic wound response of tomato. Proc. Matsuura, H., Takeishi, S., Kiatoka, N., Sato, C., Sueda, K., Masuta, C. and
Natl Acad. Sci. USA, 99, 6416–6421. Nabeta, K. (2012) Transportation of de novo synthesized jasmonoyl iso-
Li, X., Schuler, M.A. and Berenbaum, M.R. (2002b) Jasmonate and salicylate leucine in tomato. Phytochemistry, 83, 25–33.
induce expression of herbivore cytochrome P450 genes. Nature, 419, 712– Mattiacci, L., Dicke, M. and Posthumus, M.A. (1995) beta-Glucosidase: an
715. elicitor of herbivore-induced plant odor that attracts host-searching para-
Li, X., Baudry, J., Berenbaum, M.R. and Schuler, M.A. (2004a) Structural sitic wasps. Proc. Natl Acad. Sci. USA, 92, 2036–2040.
and functional divergence of insect CYP6B proteins: from specialist to Mauricio, R. (1998) Costs of resistance to natural enemies in field populations
generalist cytochrome P450. Proc. Natl Acad. Sci. USA, 101, 2939– of the annual plant Arabidopsis thaliana. Am. Nat., 151, 20–28.
2944. McConn, M., Creelman, R.A., Bel, E., Mullet, J.E. and Browse, J. (1997) Jas-
Li, L., Zhao, Y., McCaig, B.C., Wingerd, B.A., Wang, J., Whalon, M.E., Picher- monate is essential for insect defense in Arabidopsis. Proc. Natl Acad.
sky, E. and Howe, G.A. (2004b) The tomato homolog of CORONATINE- Sci. USA, 94, 5473–5477.
INSENSITIVE1 is required for the maternal control of seed maturation, McHale, L., Tan, X., Koehl, P. and Michelmore, R.W. (2006) Plant NBS-LRR
jasmonate-signaled defense responses, and glandular trichome develop- proteins: adaptable guards. Genome Biol., 7, 212.
ment. Plant Cell, 16, 126–143. Meiners, T. and Hilker, M. (2000) Induction of plant synomones by oviposi-
Li, X., Schuler, M.A. and Berenbaum, M.R. (2007) Molecular mechanisms of tion of a phytophagous insect. J. Chem. Ecol., 26, 221–232.
metabolic resistance to synthetic and natural xenobiotics. Annu. Rev. Mewis, I., Appel, H.M., Hom, A., Raina, R. and Schultz, J.C. (2005) Major sig-
Entomol., 52, 231–253. naling pathways modulate Arabidopsis glucosinolate accumulation and
© 2017 The Authors

response to both phloem-feeding and chewing insects. Plant Physiol., Pechan, T., Cohen, A., Williams, W.P. and Luthe, D.S. (2002) Insect feed-
138, 1149–1162. ing mobilizes a unique plant defense protease that disrupts the per-
Milligan, S.B., Bodeau, J., Yaghoobi, J., Kaloshian, I., Zabel, P. and Wil- itrophic matrix of caterpillars. Proc. Natl Acad. Sci. USA, 99, 13 319–13
liamson, V.M. (1998) The root knot nematode resistance gene Mi from 323.
tomato is a member of the leucine zipper, nucleotide binding, leucine- Pegadaraju, V., Knepper, C., Reese, J.C. and Shah, J. (2005) Premature leaf
rich repeat family of plant genes. Plant Cell, 10, 1307–1319. senescence modulated by the Arabidopsis PHYTOALEXIN DEFICIENT4
Mitho € fer, A. and Boland, W. (2008) Recognition of herbivory-associated gene is associated with defense against the phloem-feeding green peach
molecular patterns. Plant Physiol., 146, 825–831. aphid. Plant Physiol., 139, 1927–1934.
Mitho € fer, A. and Boland, W. (2012) Plant defense against herbivores: chemi- Pegadaraju, V., Louis, J., Singh, V., Reese, J.C., Bautor, J., Feys, B.J., Cook,
cal aspects. Annu. Rev. Plant Biol., 63, 431–450. G., Parker, J.E. and Shah, J. (2007) Phloem-based resistance to green
Mordue Luntz, A.J., Simmonds, M.S.J., Ley, S.V., Blaney, W.M., Mordue, peach aphid is controlled by Arabidopsis PHYTOALEXIN DEFICIENT4
W., Nasiruddin, M. and Nisbet, A.J. (1998) Actions of azadirachtin, a without its signaling partner ENHANCED DISEASE SUSCEPTIBILITY1.
plant allelochemical, against insects. Pestic. Sci., 54, 277–284. Plant J., 52, 332–341.
Mori, N., Yoshinaga, N., Sawada, Y., Fukui, M., Shimoda, M., Fujisaki, K., Peng, H.-C., Mantelin, S., Hicks, G.R., Takken, F.L.W. and Kaloshian, I.
Nishida, R. and Kuwahara, Y. (2003) Identification of volicitin-related (2016) The conformation of a plasma membrane-localized somatic
compounds from the regurgitant of lepidopteran caterpillars. Biosci. embryogenesis receptor kinase complex is altered by a potato aphid-
Biotechnol. Biochem., 67, 1168–1171. derived effector. Plant Physiol., 171, 2211–2222.
Mousavi, S.A.R., Chauvin, A., Pascaud, F., Kellenberger, S. and Farmer, E.E. Perkins, L.E., Cribb, B.W., Brewer, P.B., Hanan, J., Grant, M., de Torres, M.
(2013) GLUTAMATE RECEPTOR-LIKE genes mediate leaf-to-leaf wound and Zalucki, M.P. (2013) Generalist insects behave in a jasmonate-depen-
signalling. Nature, 500, 422–426. dent manner on their host plants, leaving induced areas quickly and
Musser, R.O., Hum-Musser, S.M., Eichenseer, H., Peiffer, M., Ervin, G., Mur- staying longer on distant parts. Proc. Biol. Sci. B, 280, 20122646.
phy, J.B. and Felton, G.W. (2002) Herbivory: caterpillar saliva beats plant Pfalz, M., Vogel, H., Mitchell-Olds, T. and Kroymann, J. (2007) Mapping of
defences. Nature, 416, 599–600. QTL for resistance against the crucifer specialist herbivore Pieris brassi-
Mutti, N.S., Louis, J., Pappan, L.K. et al. (2008) A protein from the salivary cae in a new Arabidopsis inbred line population, Da(1)-12 x Ei-2. PLoS
glands of the pea aphid, Acyrthosiphon pisum, is essential in feeding on ONE, 2, e578.
a host plant. Proc. Natl Acad. Sci. USA, 105, 9965–9969. Pieterse, C.M.J. and Dicke, M. (2007) Plant interactions with microbes and
Naessens, E., Dubreuil, G., Giordanengo, P., Baron, O.L., Minet-Kebdani, N., insects: from molecular mechanisms to ecology. Trends Plant Sci., 12,
Keller, H. and Coustau, C. (2015) A secreted MIF cytokine enables aphid 564–569.
feeding and represses plant immune responses. Curr. Biol., 25, 1898– Pieterse, C.M.J., derDoes Van, D., Zamioudis, C., Leon-Reyes, A. and Van
1903. Wees, S.C.M. (2012) Hormonal modulation of plant immunity. Annu.
Nombela, G., Williamson, V.M. and Mun ~ iz, M. (2003) The root-knot nema- Rev. Cell Dev. Biol., 28, 489–521.
tode resistance gene Mi-1.2 of tomato is responsible for resistance Pineda, A., Zheng, S.-J., van Loon, J.J.A., Pieterse, C.M.J. and Dicke, M.
against the whitefly Bemisia tabaci. Mol. Plant Microbe Interact., 16, 645– (2010) Helping plants to deal with insects: the role of beneficial soil-
649. borne microbes. Trends Plant Sci., 15, 507–514.
van Ohlen, M., Herfurth, A.-M., Kerbstadt, H. and Wittstock, U. (2016) Cya- Pitino, M. and Hogenhout, S.A. (2013) Aphid protein effectors promote
nide detoxification in an insect herbivore: molecular identification of b- aphid colonization in a plant species-specific manner. Mol. Plant-Microbe
cyanoalanine synthases from Pieris rapae. Insect Biochem. Mol. Biol., 70, Interact., 26, 130–139.
99–110. Pohnert, G., Jung, V., Haukioja, E., Lempa, K. and Boland, W. (1999) New
Ollerstam, O. and Larsson, S. (2003) Salicylic acid mediates resistance in fatty acid amides from regurgitant of lepidopteran (Noctuidae, Geometri-
the willow Salix viminalis against the gall midge Dasineura marginem- dae) caterpillars. Tetrahedron, 55, 11 275–11 280.
torquens. J. Chem. Ecol., 29, 163–174. Prince, D.C., Drurey, C., Zipfel, C. and Hogenhout, S.A. (2014) The leucine-
Olsnes, S., Refsnes, K. and Pihl, A. (1974) Mechanism of action of the toxic rich repeat receptor-like kinase BRASSINOSTEROID INSENSITIVE1-
lectins abrin and ricin. Nature, 249, 627–631. ASSOCIATED KINASE1 and the cytochrome P450 PHYTOALEXIN DEFI-
Onkokesung, N., Reichelt, M., van Doorn, A., Schuurink, R.C., van Loon, J.J. CIENT3 contribute to innate immunity to aphids in Arabidopsis. Plant
and Dicke, M. (2014) Modulation of flavonoid metabolites in Arabidopsis Physiol., 164, 2207–2219.
thaliana through overexpression of the MYB75 transcription factor: role Rasmann, S., Ko€ llner, T.G., Degenhardt, J., Hiltpold, I., Toepfer, S., Kuhl-
of kaempferol-3,7-dirhamnoside in resistance to the specialist insect her- mann, U., Gershenzon, J. and Turlings, T.C.J. (2005) Recruitment of
bivore Pieris brassicae. J. Exp. Bot., 65, 2203–2217. entomopathogenic nematodes by insect-damaged maize roots. Nature,
Onkokesung, N., Reichelt, M., van Doorn, A., Schuurink, R.C. and Dicke, M. 434, 732–737.
(2016) Differential costs of two distinct resistance mechanisms induced Rathcke, B. and Poole, R. (1975) Coevolutionary race continues: butterfly lar-
by different herbivore species in Arabidopsis. Plant Physiol., 170, 891– val adaptation to plant trichomes. Science, 187, 175–176.
906. Ratzka, A., Vogel, H., Kliebenstein, D.J., Mitchell-Olds, T. and Kroymann, J.
Palmer, T.M., Stanton, M.L., Young, T.P., Goheen, J.R., Pringle, R.M. and (2002) Disarming the mustard oil bomb. Proc. Natl Acad. Sci. USA, 99,
Karban, R. (2008) Breakdown of an ant-plant mutualism follows the 11 223–11 228.
loss of large herbivores from an African savanna. Science, 319, 192– Ray, S., Alves, P.C., Ahmad, I. et al. (2016) Turnabout is fair play: herbivory-
195. induced plant chitinases excreted in fall armyworm frass suppress herbi-
Panstruga, R., Baumgarten, K. and Bernhagen, J. (2015) Phylogeny and evo- vore defenses in maize. Plant Physiol., 171, 694–706.
lution of plant macrophage migration inhibitory factor/D-dopachrome Reymond, P. (2013) Perception, signaling and molecular basis of oviposi-
tautomerase-like proteins. BMC Evol. Biol., 15, 64. tion-mediated plant responses. Planta, 238, 247–258.
Pare, P.W. and Tumlinson, J.H. (1999) Plant volatiles as a defense against Reymond, P. and Calandra, T. (2015) Plant immune responses: aphids strike
insect herbivores. Plant Physiol., 121, 325–332. back. Curr. Biol., 25, R604–R606.
Pare, P.W., Alborn, H.T. and Tumlinson, J.H. (1998) Concerted biosynthesis Reymond, P., Weber, H., Damond, M. and Farmer, E.E. (2000) Differential
of an insect elicitor of plant volatiles. Proc. Natl Acad. Sci. USA, 95, 13 gene expression in response to mechanical wounding and insect feeding
971–13 975. in Arabidopsis. Plant Cell, 12, 707–720.
Paschold, A., Halitschke, R. and Baldwin, I.T. (2007) Co(i)-ordinating Reymond, P., Bodenhausen, N., Van Poecke, R.M.P., Krishnamurthy, V.,
defenses: NaCOI1 mediates herbivore-induced resistance in Nicotiana Dicke, M. and Farmer, E.E. (2004) A conserved transcript pattern in
attenuata and reveals the role of herbivore movement in avoiding response to a specialist and a generalist herbivore. Plant Cell, 16, 3132–
defenses. Plant J., 51, 79–91. 3147.
Pastorczyk, M. and Bednarek, P. (2016) Chapter seven – the function of glu- Rodriguez, P.A., Escudero-Martinez, C. and Bos, J.I.B. (2017) An aphid effec-
cosinolates and related metabolites in plant innate immunity. Adv. Bot. tor targets trafficking protein VPS52 in a host-specific manner to promote
Res., 80, 171–198. virulence. Plant Physiol., 173, 1893–1903.
© 2017 The Authors

Roepke, J., Salim, V., Wu, M., Thamm, A.M., Murata, J., Ploss, K., Boland, Seino, Y., Suzuki, Y. and Kazushige, S. (1996) An ovicidal substance pro-
W. and De Luca, V. (2010) Vinca drug components accumulate exclu- duced by rice plants in response to oviposition by the whitebacked plan-
sively in leaf exudates of Madagascar periwinkle. Proc. Natl Acad. Sci. thopper, Sogatella furcifera (HORVATH) (Homoptera: Delphacidae). Appl.
USA, 107, 15 287–15 292. Entomol. Zool., 31, 467–473.
Romero, G.Q. and Benson, W.W. (2005) Biotic interactions of mites, plants Self, L.S., Guthrie, F.E. and Hodgson, E. (1964) Adaptation of tobacco horn-
and leaf domatia. Curr. Opin. Plant Biol., 8, 436–440. worms to the ingestion of nicotine. J. Insect Physiol., 10, 907–914.
Rosas-Dıaz, T., Macho, A.P., Beuzo n, C.R., Lozano-Duran, R. and Bejarano, Shapiro, A.M. (1981) Egg-mimics of Streptanthus (Cruciferae) deter
E.R. (2016) The C2 protein from the geminivirus Tomato yellow leaf curl oviposition by Pieris sisymbrii (Lepidoptera: Pieridae). Oecologia, 48,
Sardinia virus decreases sensitivity to jasmonates and suppresses jas- 142–143.
monate-mediated defences. Plants, 5, 8. Singh, V., Louis, J., Ayre, B.G., Reese, J.C. and Shah, J. (2011) TREHALOSE
Rosenthal, G.A. (2001) L-Canavanine: a higher plant insecticidal allelochemi- PHOSPHATE SYNTHASE11-dependent trehalose metabolism promotes
cal. Amino Acids, 21, 319–330. Arabidopsis thaliana defense against the phloem-feeding insect Myzus
Rosenthal, G.A., Dahlman, D.L. and Janzen, D.H. (1976) A novel means for persicae. Plant J., 67, 94–104.
dealing with L-canavanine, a toxic metabolite. Science, 192, 256–258. Smith, C.M.C. and Clement, S.L.S. (2011) Molecular bases of plant resis-
Rossi, M., Goggin, F.L., Milligan, S.B., Kaloshian, I., Ullman, D.E. and Wil- tance to arthropods. Annu. Rev. Entomol., 57, 309–328.
liamson, V.M. (1998) The nematode resistance gene Mi of tomato con- Spiteller, D., Pohnert, G. and Boland, W. (2001) Absolute configuration of
fers resistance against the potato aphid. Proc. Natl Acad. Sci. USA, 95, volicitin, an elicitor of plant volatile biosynthesis from lepidopteran lar-
9750–9754. vae. Tetrahedron Lett., 42, 1483–1485.
Ryan, C.A. and Pearce, G. (1998) Systemin: a polypeptide signal for plant Stam, J.M., Kroes, A., Li, Y., Gols, R., van Loon, J.J.A., Poelman, E.H. and
defensive genes. Annu. Rev. Cell Dev. Biol., 14, 1–17. Dicke, M. (2014) Plant interactions with multiple insect herbivores: from
Sachdev-Gupta, K., Radke, C.D. and Renwick, J.A.A. (1993) Antifeedant community to genes. Annu. Rev. Plant Biol., 65, 689–713.
activity of cucurbitacins from Iberis amara against larvae of Pieris rapae. Staniscßuaski, F. and Carlini, C.R. (2012) Plant ureases and related peptides:
Phytochemistry, 33, 1385–1388. understanding their entomotoxic properties. Toxins, 4, 55–67.
Salvador-Recatala, V., Tjallingii, W.F. and Farmer, E.E. (2014) Real-time, Staswick, P.E. and Tiryaki, I. (2004) The oxylipin signal jasmonic acid is ac-
in vivo intracellular recordings of caterpillar-induced depolarization waves tivated by an enzyme that conjugates it to isoleucine in Arabidopsis.
in sieve elements using aphid electrodes. New Phytol., 203, 674–684. Plant Cell, 16, 2117–2127.
Scha€fer, M., Fischer, C., Meldau, S., Seebald, E., Oelm€uller, R. and Baldwin, Steppuhn, A., Gase, K., Krock, B., Halitschke, R. and Baldwin, I.T. (2004)
I.T. (2011) Lipase activity in insect oral secretions mediates defense Nicotine’s defensive function in nature. PLoS Biol., 2, e217.
responses in Arabidopsis. Plant Physiol., 156, 1520–1534. Stone, G. (2003) The adaptive significance of insect gall morphology.
Schittko, U., Hermsmeier, D. and Baldwin, I.T. (2001) Molecular interactions Trends Ecol. Evol., 18, 512–522.
between the specialist herbivore Manduca sexta (Lepidoptera, Sphingidae) Stotz, H.U., Pittendrigh, B., Kroymann, J., Weniger, K., Fritsche, J., Bauke,
and its natural host Nicotiana attenuata. II. Accumulation of plant mRNAs A. and Mitchell-Olds, T. (2000) Induced plant defense responses against
in response to insect-derived cues. Plant Physiol., 125, 701–710. chewing insects. Ethylene signaling reduces resistance of Arabidopsis
Schlaeppi, K., Bodenhausen, N., Buchala, A., Mauch, F. and Reymond, P. against Egyptian cotton worm but not diamondback moth. Plant Physiol.,
(2008) The glutathione-deficient mutant pad2-1 accumulates lower 124, 1007–1018.
amounts of glucosinolates and is more susceptible to the insect herbi- Stotz, H.U., Koch, T., Biedermann, A., Weniger, K., Boland, W. and Mitchell-
vore Spodoptera littoralis. Plant J., 55, 774–786. Olds, T. (2002) Evidence for regulation of resistance in Arabidopsis to
Schmelz, E.A., Carroll, M.J., LeClere, S., Phipps, S.M., Meredith, J., Egyptian cotton worm by salicylic and jasmonic acid signaling pathways.
Chourey, P.S., Alborn, H.T. and Teal, P.E.A. (2006) Fragments of ATP syn- Planta, 214, 648–652.
thase mediate plant perception of insect attack. Proc. Natl Acad. Sci. Stratmann, J.W. (2003) Long distance run in the wound response – jas-
USA, 103, 8894–8899. monic acid is pulling ahead. Trends Plant Sci., 8, 248–250.
Schmelz, E.A., Engelberth, J., Alborn, H.T., Tumlinson, J.H. and Teal, P.E.A. Strauss, A.S., Peters, S., Boland, W. and Burse, A. (2013) ABC transporter
(2009) Phytohormone-based activity mapping of insect herbivore-pro- functions as a pacemaker for sequestration of plant glucosides in leaf
duced elicitors. Proc. Natl Acad. Sci. USA, 106, 653–657. beetles. Elife, 2, e01096.
Schmelz, E.A., Kaplan, F., Huffaker, A., Dafoe, N.J., Vaughan, M.M., Ni, X., Stuart, J.J., Chen, M.-S., Shukle, R. and Harris, M.O. (2012) Gall midges (Hessian
Rocca, J.R., Alborn, H.T. and Teal, P.E. (2011) Identity, regulation, and flies) as plant pathogens. Annu. Rev. Phytopathol., 50, 339–357.
activity of inducible diterpenoid phytoalexins in maize. Proc. Natl Acad. Sugio, A., Kingdom, H.N., Maclean, A.M., Grieve, V.M. and Hogenhout, S.A.
Sci. USA, 108, 5455–5460. (2011) Phytoplasma protein effector SAP11 enhances insect vector repro-
Schmelz, E.A., Huffaker, A., Carroll, M.J., Alborn, H.T., Ali, J.G. and Teal, duction by manipulating plant development and defense hormone
P.E.A. (2012) An amino acid substitution inhibits specialist herbivore pro- biosynthesis. Proc. Natl Acad. Sci. USA, 108, E1254–E1263.
duction of an antagonist effector and recovers insect-induced plant Sugio, A., Dubreuil, G., Giron, D. and Simon, J.-C. (2015) Plant-insect inter-
defenses. Plant Physiol., 160, 1468–1478. actions under bacterial influence: ecological implications and underlying
Schmiesing, A., Emonet, A., Gouhier-Darimont, C. and Reymond, P. (2016) mechanisms. J. Exp. Bot., 66, 467–478.
Arabidopsis MYC transcription factors are the target of hormonal SA/JA Tamiru, A., Bruce, T.J.A., Woodcock, C.M. et al. (2011) Maize landraces
cross talk in response to Pieris brassicae egg Extract. Plant Physiol., 170, recruit egg and larval parasitoids in response to egg deposition by a her-
2432–2443. bivore. Ecol. Lett., 14, 1075–1083.
Schoonhoven, L.M., van Loon, J.J.A. and Dicke, M. (2005) Insect-Plant Biol- Tamura, Y., Hattori, M., Yoshioka, H., Yoshioka, M., Takahashi, A., Wu, J.,
ogy. USA: Oxford University Press. Sentoku, N. and Yasui, H. (2014) Map-based cloning and characterization
Schuman, M.C. and Baldwin, I.T. (2016) The layers of plant responses to of a brown planthopper resistance gene BPH26 from Oryza sativa L. ssp.
insect herbivores. Annu. Rev. Entomol., 61, 373–394. indica cultivar ADR52. Sci. Rep., 4, 5872.
Schweizer, F., Bodenhausen, N., Lassueur, S., Masclaux, F.G. and Reymond, P. Tay, W.T., Mahon, R.J., Heckel, D.G. et al. (2015) Insect resistance to Bacil-
(2013a) Differential contribution of transcription factors to Arabidopsis thali- lus thuringiensis toxin Cry2Ab is conferred by mutations in an ABC
ana defense against Spodoptera littoralis. Front. Plant-Microbe Interact., 4, 13. transporter subfamily A protein (Malik, H.S., ed.). PLoS Genet., 11,
Schweizer, F., Fernandez-Calvo, P., Zander, M., Diez-Diaz, M., Fonseca, S., e1005534.
Glauser, G., Lewsey, M.G., Ecker, J.R., Solano, R. and Reymond, P. Teese, M.G., Campbell, P.M., Scott, C., Gordon, K.H.J., Southon, A., Hovan,
(2013b) Arabidopsis basic helix-loop-helix transcription factors MYC2, D., Robin, C., Russell, R.J. and Oakeshott, J.G. (2010) Gene identification
MYC3, and MYC4 regulate glucosinolate biosynthesis, insect perfor- and proteomic analysis of the esterases of the cotton bollworm, Helicov-
mance, and feeding behavior. Plant Cell, 25, 3117–3132. erpa armigera. Insect Biochem. Mol. Biol., 40, 1–16.
Schweizer, F., Heidel-Fischer, H., Vogel, H. and Reymond, P. (2017) Arabidop- Thines, B., Katsir, L., Melotto, M. et al. (2007) JAZ repressor proteins are
sis glucosinolates trigger a contrasting transcriptomic response in a gener- targets of the SCF(COI1) complex during jasmonate signalling. Nature,
alist and a specialist herbivore. Insect Biochem. Mol. Biol., 85, 21–31. 448, 661–665.
© 2017 The Authors

Tomasetto, F., Tylianakis, J.M., Reale, M., Wratten, S. and Goldson, S.L. Wroblewski, T., Piskurewicz, U., Tomczak, A., Ochoa, O. and Michelmore,
(2017) Intensified agriculture favors evolved resistance to biological con- R.W. (2007) Silencing of the major family of NBS-LRR-encoding genes in
trol. Proc. Natl Acad. Sci. USA, 114, 3885–3890. lettuce results in the loss of multiple resistance specificities. Plant J., 51,
Tripathi, A.K., Bhakuni, R.S., Upadhayay, S. and Gaur, R. (2011) Insect feed- 803–818.
ing deterrent and growth inhibitory activities in scopoletin isolated from Wu, J. and Baldwin, I.T. (2010) New insights into plant responses to the
Artemisia annua against Spilarctia obliqua (Lepidoptera: Noctuidae). attack from insect herbivores. Annu. Rev. Genet., 44, 1–24.
Insect Sci., 18, 189–194. Wu, S., Peiffer, M., Luthe, D.S. and Felton, G.W. (2012) ATP hydrolyzing sali-
Truitt, C.L., Wei, H.-X. and Pare, P.W. (2004) A plasma membrane protein vary enzymes of caterpillars suppress plant defenses. PLoS ONE, 7,
from Zea mays binds with the herbivore elicitor volicitin. Plant Cell, 16, e41947.
523–532. Wybouw, N., Dermauw, W., Tirry, L., Stevens, C., Grbic, M., Feyereisen, R.
Tsuji, J., Jackson, E.P., Gage, D.A., Hammerschmidt, R. and Somerville, and Van Leeuwen, T. (2014) A gene horizontally transferred from bacte-
S.C. (1992) Phytoalexin accumulation in Arabidopsis thaliana during the ria protects arthropods from host plant cyanide poisoning. Elife, 3,
hypersensitive reaction to Pseudomonas syringae pv syringae. Plant e02365.
Physiol., 98, 1304–1309. Yan, Y., Christensen, S., Isakeit, T., Engelberth, J., Meeley, R., Hayward, A.,
Vandenborre, G., Smagghe, G. and Van Damme, E.J. (2011) Plant lectins as Emery, R.J.N. and Kolomiets, M.V. (2012) Disruption of OPR7 and OPR8
defense proteins against phytophagous insects. Phytochemistry, 72, reveals the versatile functions of jasmonic acid in maize development
1538–1550. and defense. Plant Cell, 24, 1420–1436.
Ververidis, F., Trantas, E., Douglas, C., Vollmer, G., Kretzschmar, G. and Yang, J.-Y., Iwasaki, M., Machida, C., Machida, Y., Zhou, X. and Chua, N.-H.
Panopoulos, N. (2007) Biotechnology of flavonoids and other phenyl- (2008) betaC1, the pathogenicity factor of TYLCCNV, interacts with AS1
propanoid-derived natural products. Part I: chemical diversity, impacts to alter leaf development and suppress selective jasmonic acid
on plant biology and human health. Biotechnol. J., 2, 1214–1234. responses. Genes Dev., 22, 2564–2577.
Vetter, J. (2000) Plant cyanogenic glycosides. Toxicon, 38, 11–36. Yang, J.-O., Nakayama, N., Toda, K., Tebayashi, S. and Kim, C.-S. (2014)
Villarroel, C.A., Jonckheere, W., Alba, J.M., Glas, J.J., Dermauw, W., Haring, Structural determination of elicitors in Sogatella furcifera (Horvath) that
M.A., Van Leeuwen, T., Schuurink, R.C. and Kant, M.R. (2016) Salivary induce Japonica rice plant varieties (Oryza sativa L.) to produce an ovici-
proteins of spider mites suppress defenses in Nicotiana benthamiana dal substance against S. furcifera eggs. Biosci. Biotechnol. Biochem., 78,
and promote mite reproduction. Plant J., 86, 119–131. 937–942.
Vincent, T.R., Avramova, M., Canham, J. et al. (2017) Interplay of plasma Yoshinaga, N., Aboshi, T., Ishikawa, C., Fukui, M., Shimoda, M., Nishida, R.,
membrane and vacuolar ion channels, together with BAK1, elicits rapid Lait, C.G., Tumlinson, J.H. and Mori, N. (2007) Fatty acid amides, previ-
cytosolic calcium elevations in Arabidopsis during aphid feeding. Plant ously identified in caterpillars, found in the cricket Teleogryllus tai-
Cell, 29, 1460–1479. wanemma and fruit fly Drosophila melanogaster larvae. J. Chem. Ecol.,
Vlot, A.C., Dempsey, D.A. and Klessig, D.F. (2009) Salicylic acid, a multi- 33, 1376–1381.
faceted hormone to combat disease. Annu. Rev. Phytopathol., 47, 177–206. Yoshinaga, N., Aboshi, T., Abe, H., Nishida, R., Alborn, H.T., Tumlinson, J.H.
de Vos, M. and Jander, G. (2009) Myzus persicae (green peach aphid) sali- and Mori, N. (2008) Active role of fatty acid amino acid conjugates in
vary components induce defence responses in Arabidopsis thaliana. nitrogen metabolism in Spodoptera litura larvae. Proc. Natl Acad. Sci.
Plant, Cell Environ., 32, 1548–1560. USA, 105, 18 058–18 063.
de Vos, M., Van Oosten, V.R., Van Poecke, R.M.P. et al. (2005) Signal signa- Zarate, S.I., Kempema, L.A. and Walling, L.L. (2007) Silverleaf whitefly
ture and transcriptome changes of Arabidopsis during pathogen and induces salicylic acid defenses and suppresses effectual jasmonic acid
insect attack. Mol. Plant Microbe Interact., 18, 923–937. defenses. Plant Physiol., 143, 866–875.
Weech, M.-H., Chapleau, M., Pan, L., Ide, C. and Bede, J.C. (2008) Caterpillar Zhang, P.-J., Zheng, S.-J., vanLoon, J.J.A., Boland, W., David, A., Mumm, R.
saliva interferes with induced Arabidopsis thaliana defence responses via and Dicke, M. (2009) Whiteflies interfere with indirect plant defense
the systemic acquired resistance pathway. J. Exp. Bot., 59, 2437–2448. against spider mites in Lima bean. Proc. Natl Acad. Sci. USA, 106, 21
Wheat, C.W., Vogel, H., Wittstock, U., Braby, M.F., Underwood, D. and 202–21 207.
Mitchell-Olds, T. (2007) The genetic basis of a plant-insect coevolutionary Zhang, P.-J., Broekgaarden, C., Zheng, S.-J., Snoeren, T.A.L., van Loon,
key innovation. Proc. Natl Acad. Sci. USA, 104, 20 427–20 431. J.J.A., Gols, R. and Dicke, M. (2013) Jasmonate and ethylene
Will, T. and van Bel, A.J.E. (2006) Physical and chemical interactions signaling mediate whitefly-induced interference with indirect plant
between aphids and plants. J. Exp. Bot., 57, 729–737. defense in Arabidopsis thaliana. New Phytol., 197, 1291–1299.
€ nnessen, A. and van Bel, A.J.E. (2007) Molecular
Will, T., Tjallingii, W.F., Tho Zhang, P.-J., Huang, F., Zhang, J.-M., Wei, J.-N. and Lu, Y.-B. (2015) The
sabotage of plant defense by aphid saliva. Proc. Natl Acad. Sci. USA, mealybug Phenacoccus solenopsis suppresses plant defense responses
104, 10 536–10 541. by manipulating JA-SA crosstalk. Sci. Rep., 5, 9354.
Williams, K.S. and Gilbert, L.E. (1981) Insects as selective agents on plant Zhao, C., Escalante, L.N., Chen, H. et al. (2015) A massive expansion of
vegetative morphology: egg mimicry reduces egg laying by butterflies. effector genes underlies gall-formation in the wheat pest Mayetiola
Science, 212, 467–469. destructor. Curr. Biol., 25, 613–620.
Winde, I. and Wittstock, U. (2011) Insect herbivore counteradaptations to Zheng, X.-Y., Spivey, N.W., Zeng, W., Liu, P.-P., Fu, Z.Q., Klessig, D.F., He,
the plant glucosinolate-myrosinase system. Phytochemistry, 72, 1566– S.Y. and Dong, X. (2012) Coronatine promotes Pseudomonas syringae
1575. virulence in plants by activating a signaling cascade that inhibits salicylic
Wink, M., Schmeller, T. and Latz-Bruning, B. (1998) Modes of action of alle- acid accumulation. Cell Host Microbe, 11, 587–596.
lochemical alkaloids: interaction with neuroreceptors, DNA, and other Zhurov, V., Navarro, M., Bruinsma, K.A. et al. (2014) Reciprocal responses
molecular targets. J. Chem. Ecol., 24, 1881–1893. in the interaction between Arabidopsis and the cell-content-feeding che-
Winkler, I.S., Mitter, C. and Scheffer, S.J. (2009) Repeated climate-linked licerate herbivore spider mite. Plant Physiol., 164, 384–399.
host shifts have promoted diversification in a temperate clade of leaf- Zhu-Salzman, K., Bi, J.-L. and Liu, T.-X. (2005) Molecular strategies of plant
mining flies. Proc. Natl Acad. Sci. USA, 106, 18 103–18 108. defense and insect counter-defense. Insect Sci., 12, 3–15.
Wittstock, U., Agerbirk, N., Stauber, E.J., Olsen, C.E., Hippler, M., Mitchell- Zimmermann, M.R., Mitho € fer, A., Will, T., Felle, H.H. and Furch, A.C.U.
Olds, T., Gershenzon, J. and Vogel, H. (2004) Successful herbivore attack (2016) Herbivore-triggered electrophysiological reactions: candidates for
due to metabolic diversion of a plant chemical defense. Proc. Natl Acad. systemic signals in higher plants and the challenge of their identification.
Sci. USA, 101, 4859–4864. Plant Physiol., 170, 2407–2419.
© 2017 The Authors


Stahl Et Al., 2018 Agroecología Interacciones Plantas Artrópodos Herbivoría MIP

Uploaded by

Copyright:

Available Formats

Stahl Et Al., 2018 Agroecología Interacciones Plantas Artrópodos Herbivoría MIP

Uploaded by

Document Information

Copyright

Available Formats

Share this document

Share or Embed Document

Sharing Options

Did you find this document useful?

Is this content inappropriate?

Copyright:

Available Formats

Stahl Et Al., 2018 Agroecología Interacciones Plantas Artrópodos Herbivoría MIP

Uploaded by

Copyright:

Available Formats

The Plant Journal (2018) 93, 703–728 doi: 10.1111/tpj.

SI PLANT BIOTIC INTERACTIONS

Plant–arthropod interactions: who is the winner?

© 2017 The Authors 703

Figure 1. Overview of plant responses to herbivory.

© 2017 The Authors

Table 1 HAMPs and effectors from arthropods

Name Origin Response Reference

© 2017 The Authors

© 2017 The Authors

© 2017 The Authors

Cell death SAR

© 2017 The Authors

precursor chorismate by ISOCHORISMATE SYNTHASE 1 require a functional SA pathway (Gouhier-Darimont et al.,

© 2017 The Authors

© 2017 The Authors

Table 2 Plant-derived metabolites with direct insecticidal activity

Glucosinolates Brassicaceae Mamestra brassicae, Myrosinase-dependent hydrolysis Beekwilder et al. (2008)

© 2017 The Authors

© 2017 The Authors

© 2017 The Authors

Table 3 Plant-derived proteins with direct insecticidal activity

© 2017 The Authors

© 2017 The Authors

© 2017 The Authors

© 2017 The Authors

Table 4 Co-evolution between plants and arthropods

Plant defense Arthropod adaptation Plant counterdefense Reference

Cardenolides Leaf vein cutting

© 2017 The Authors

© 2017 The Authors

© 2017 The Authors

© 2017 The Authors

© 2017 The Authors

© 2017 The Authors

© 2017 The Authors

© 2017 The Authors

© 2017 The Authors

© 2017 The Authors

© 2017 The Authors

You might also like