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Annual Review of Plant Biology

Molecular Interactions Between
Plants and Insect Herbivores
Matthias Erb1 and Philippe Reymond2
Annu. Rev. Plant Biol. 2019.70:527-557. Downloaded from [Link]
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1
Institute of Plant Sciences, University of Bern, 3000 Bern, Switzerland;
email: [Link]@[Link]
2
Department of Plant Molecular Biology, University of Lausanne, 1015 Lausanne,
Switzerland; email: [Link]@[Link]

Annu. Rev. Plant Biol. 2019. 70:527–57 Keywords

First published as a Review in Advance on
herbivore-associated molecular pattern, HAMP, damage-associated
February 20, 2019
molecular pattern, DAMP, insect herbivory, jasmonate, plant defense
The Annual Review of Plant Biology is online at
signaling, secondary metabolites
[Link]

[Link] Abstract
095910
Diverse molecular processes regulate the interactions between plants and
Copyright © 2019 by Annual Reviews.
insect herbivores. Here, we review genes and proteins that are involved in
All rights reserved
plant–herbivore interactions and discuss how their discovery has structured
the current standard model of plant–herbivore interactions. Plants perceive
damage-associated and, possibly, herbivore-associated molecular patterns
via receptors that activate early signaling components such as Ca2+ , reactive
oxygen species, and MAP kinases. Specific defense reprogramming proceeds
via signaling networks that include phytohormones, secondary metabolites,
and transcription factors. Local and systemic regulation of toxins, defense
proteins, physical barriers, and tolerance traits protect plants against her-
bivores. Herbivores counteract plant defenses through biochemical defense
deactivation, effector-mediated suppression of defense signaling, and chem-
ically controlled behavioral changes. The molecular basis of plant–herbivore
interactions is now well established for model systems. Expanding molecular
approaches to unexplored dimensions of plant–insect interactions should be
a future priority.

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Contents
INTRODUCTION . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 528
PLANT PERCEPTION AND SIGNALING . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 528
Recognition of Herbivore- and Damage-Associated Molecular Patterns
by Pattern Recognition Receptors . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 529
Early Signaling Events Triggered by Herbivory . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 530
Jasmonate Signaling as a Conserved Core Pathway in Herbivory-Induced
Responses . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 532
Signaling Networks Mediated by Small Metabolites . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 534
Transcription Factors as Major Players in Early and Late Defense Signaling . . . . . . . . 538
Systemic Regulation of Defenses . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 539
Spatiotemporal Control of Plant Defense Deployment . . . . . . . . . . . . . . . . . . . . . . . . . . . . 539
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PLANT DEFENSE TRAITS . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 541

Toxic Secondary Metabolites . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 541
Defense Proteins . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 541
Volatiles as Attractants of Herbivore Natural Enemies . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 542
Physical Barriers . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 542
Tolerance Strategies . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 543
Progress with Genomics Approaches . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 543
HERBIVORE ADAPTATIONS TO PLANT DEFENSES . . . . . . . . . . . . . . . . . . . . . . . . . 543
Detoxification and Neutralization of Plant Defenses . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 544
Plant Defense Suppression . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 544
Behavioral Adaptations . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 545
FASCINATING BUT UNEXPLORED INTERACTIONS . . . . . . . . . . . . . . . . . . . . . . . . 545
CONCLUSIONS . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 547

INTRODUCTION
Plants face numerous abiotic and biotic stresses in nature. Insects are among the most important
threats to plant survival, owing to their abundance and diversity. Millions of years of selection
pressure generated by insect herbivores has resulted in the evolution of sophisticated plant de-
fenses. The ecology and evolution of plant–insect interactions have been studied extensively (150).
With the development and application of molecular biology techniques, scientists have also begun
to unravel the molecular mechanisms underpinning these interactions. Seventeen years after the
acclaimed review “Plant Responses to Insect Herbivory: The Emerging Molecular Analysis” by
Kessler & Baldwin (75), this review evaluates how the development of genomic tools and gene
manipulation strategies has propelled the field forward and has resulted in a detailed mechanistic
understanding of plant–herbivore interactions. We focus primarily on examples that demonstrate
the functional role of plant and insect herbivore genes and molecules using molecular manipu-
lative approaches and place the resulting insights into a general conceptual framework of plant
defense. This approach complements a series of recent reviews on the mechanisms, ecology, and
evolution of plant–herbivore interactions (1, 41, 171, 199).

PLANT PERCEPTION AND SIGNALING

An efficient defense response requires specific recognition of the herbivore and translation into
defense signaling to reprogram cellular functions. Following the identification of numerous
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molecules that plants can use to detect herbivore attack, recent studies have unraveled down-
stream elements and their role in defense signaling. Substantial progress has also been made in
identifying receptors that are involved in the recognition of damage- and, albeit to a lesser extent,
Herbivore-associated
herbivore-associated cues. molecular pattern
(HAMP):
insect-derived
Recognition of Herbivore- and Damage-Associated Molecular Patterns metabolites or proteins
by Pattern Recognition Receptors detected by a plant cell
surface receptor and
According to the canonical model of plant herbivore perception, plants perceive herbivory through inducing defense
the binding of herbivore- and damage-associated molecular patterns (HAMPs and DAMPs) to responses
pattern recognition receptors (PRRs). Many HAMPs have been isolated from insect herbivores
Damage-associated
(for reviews, see 1, 163), and information regarding their interactions with PRRs is emerging. molecular pattern
Radiolabeled volicitin (17-hydroxylinolenoyl-L-Gln) from Spodoptera exigua oral secretions (OSs) (DAMP): plant
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binds with high affinity to an unidentified potential PRR on the maize plasma membrane (170). cytosolic or apoplastic
Inceptin, a peptide fragment from a chloroplastic ATP synthase that is present in Spodoptera molecule freely
released upon tissue
frugiperda OSs, is a highly potent defense inducer in maize and cowpea (146). The discovery of
injury, perceived by
a truncated form of inceptin that inhibits defenses suggests that it may be recognized by a PRR cell surface receptors,
to which modified inceptin may bind as a competitive antagonist (147). The C-terminal region and inducing defense
of a mucin-like protein that is secreted by the brown planthopper (BPH) Nilaparvata lugens in- responses
duces defense responses in rice (155). Interestingly, a cluster of three G-type lectin receptor ki- Pattern recognition
nases (LecRKs) confers rice resistance against BPH (97), but whether they bind the mucin-like receptor (PRR):
protein or another ligand is unknown. Recently, a leucine-rich repeat receptor kinase (LRR-RK) cell surface receptor
from rice has been shown to be essential for perception and defense against the striped stemborer kinases with a
ligand-binding
(SSB) Chilo suppressalis (64). Future investigation of these cell surface–localized orphan PRRs may
ectodomain,
unveil the nature of their respective ligands. transmembrane
Defense activation by HAMPs may occur independently of PRRs. Glucose oxidase, for in- domain, and
stance, is found in saliva of different caterpillar species (1). It induces defenses in tomato (98) but intracellular kinase
suppresses them in tobacco and Nicotiana attenuata (33, 121). By oxidizing glucose, this enzyme domain; many are
termed receptor-like
produces the signaling molecule hydrogen peroxide (H2 O2 ). Insect-derived H2 O2 modulation of
proteins if they lack a
defenses may occur independently of PRRs because H2 O2 can diffuse through membranes or en- kinase domain
ter the cell via aquaporins. Also, the induction of 12-oxo-phytodienoic acid (OPDA) by OSs from
Oral secretion (OS):
the grasshopper Schistocera gregaria in Arabidopsis is related to lipase activity of the OS, which may
mixture of insect saliva
directly liberate defense hormone precursors from membrane lipids (143). and regurgitant that
Chewing herbivores inflict mechanical damage that strongly modifies the extracellular space can contain
by releasing cell wall fragments and intracellular components. Collectively called DAMPs, these defense-inducing
chemically diverse elicitors induce defense responses. Oligogalacturonides are pectic fragments HAMPs or effectors
perceived by wall-associated kinases in Arabidopsis thaliana (19, 81). Cells can monitor cell Nicotiana attenuata:
wall modifications and respond by activating defense responses, as has been observed in mu- wild relative of tobacco
tants impaired in cellulose synthesis. THESEUS1 is a RK that senses cellulose-related cell that has emerged as an
important model to
wall integrity (57). Similarly, FERONIA contains two extracellular domains that show homol-
identify molecular
ogy to carbohydrate-binding malectin and can bind to pectin to monitor cell wall integrity players of resistance to
in response to salt stress (42, 96, 195). In addition, THESEUS1 and FERONIA bind RAPID insects
ALKALINIZATION FACTOR peptides (48, 55), and the interaction with FERONIA modulates
plant immunity (164). To date, there is no information on the role of cell wall integrity sensors like
WALL-ASSOCIATED KINASE1, THESEUS1, or FERONIA in defense against herbivores.
However, it is tempting to speculate that perception of cell wall perturbation is a key factor in
response to feeding. Testing insect performance on PRR mutants may unveil an additional role
for these important components of the plant surveillance machinery.

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Broken cells release numerous intracellular molecules into the apoplastic space. Exogenous
treatment with ATP induces defense responses in Arabidopsis including an increase in cytoso-
lic Ca2+ (25). A screen for ATP-insensitive mutants has identified DORN1 (DOES NOT RE-
Jasmonate ( JA):
generic term that SPOND TO NUCLEOTIDES 1), a plasma membrane–localized L-type LecRK (LecRK-I.9)
refers to jasmonic acid that binds ATP with high affinity and selectivity (25). DORN1 overexpression increases plant re-
or the bioactive form sponses to wounding, implying a role in perception of mechanical damage (25). Furthermore,
jasmonoyl-L- extracellular ATP induces a set of jasmonate ( JA)-responsive genes, indicating that perception of
isoleucine
ATP stimulates the JA pathway (169). NAD(P) has been identified in the extracellular space of
Secondary danger wounded Arabidopsis leaves. When applied exogenously, NAD(P) induces defense gene expression
signal: peptide derived in a Ca2+ -dependent manner (194). Recently, Wang et al. (176) showed that LecRK-I.8 binds
from a processed
NAD+ and induces immune responses. Intriguingly, LecRK-I.8 is also implicated in Arabidop-
proprotein and
secreted in the sis responses to Pieris brassicae eggs (51). Whether this is linked to NAD+ perception or whether
apoplast upon LecRK-I.8 recognizes another egg-derived ligand remains to be elucidated. It is, however, striking
Annu. Rev. Plant Biol. 2019.70:527-557. Downloaded from [Link]

that two closely related LecRKs bind extracellular nucleotides. A G-type LecRK from N. attenuata
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perception of a
primary danger signal also contributes to resistance against Manduca sexta, but the corresponding ligand is unknown (46).
Wounding or insect feeding triggers the production of plant peptides that are released into
the apoplastic space and considered endogenous secondary danger signals. The best character-
ized of these signals is systemin from tomato, an 18–amino acid polypeptide that is cleaved from
the precursor prosystemin, spreads throughout the plant, and induces JA-dependent accumula-
tion of proteinase inhibitors that can negatively impact chewing herbivores (127). In tomato, the
LRR-RK SYR1 binds systemin with high affinity, and introgression lines that lack SYR1 are more
susceptible to Spodoptera littoralis. However, local and distal induction of proteinase inhibitors is
not affected in these lines, suggesting the involvement of other defense molecules (178). Systemin
is restricted to Solanaceae, but other wound-induced peptides have been identified. In maize, a
family of five related peptides induces emission of herbivore-related volatiles, with the 23–amino
acid ZmPep3 triggering responses similar to those induced by S. exigua (68). ZmPeps are orthol-
ogous to Arabidopsis AtPeps, which were initially discovered as defense signals that amplify innate
immunity (69). AtPep1 and its homologs trigger both JA- and salicylic acid (SA)-responsive genes
and are perceived by two related LRR-RKs, Pep1 RECEPTOR 1 (PEPR1) and PEPR2 (186).
Expression of PEPR1, PEPR2, and PROPEP3 is strongly activated by herbivore feeding, and pepr1
pepr2 double mutants are more susceptible to S. littoralis and the bacterium Pseudomonas syringae pv.
tomato (Pst) infection, consistent with a dual role for the AtPep-PEPR system in danger detection
against microbes and insects (79, 186).
In summary, the first phase of insect feeding triggers the perception of HAMPs and DAMPs
that reach the apoplastic interface (Figure 1). PRRs for HAMPs have not yet been described, but
recent breakthroughs have identified PRRs for DAMPs. Because insect feeding is accompanied
by a mixture of HAMPs and DAMPs, the specific contribution of each molecule to plant defense
response is difficult to assess and has led to controversy (15). Recent identification of DAMP re-
ceptors and receptor mutants such as dorn1 and lecRK-I.8 provides an excellent opportunity to
revisit this issue. Identification of insect genes responsible for HAMP biosynthesis in combina-
tion with physical ablation of secretory structures could shed further light on the importance of
HAMPs in plant–herbivore interactions (121).

Early Signaling Events Triggered by Herbivory

Early signaling steps following insect perception include (a) depolarization of the plasma trans-
membrane potential (Vm ), (b) rise in cytosolic Ca2+ , (c) production of reactive oxygen species
(ROS), and (d) mitogen-activated protein kinase (MAPK) activity. Vm variation and [Ca2+ ]cyt

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OS
Cell wall

Peps Sys Pect Cel OGs In FACs ?

? ? NAD ATP ?
Apoplast

Cytosol

PEPR1/2 SYR1 FER THE1 WAK1 ? ? RLK1 LecRK-I.8 DORN1 LecRK1/2/3

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LRR Malectin HAMPs

EGF-like Lectin Defense responses DAMPs

SDSs
Transmembrane domain
Cytosolic kinase domain

Figure 1
Perception of known or putative ligands associated with insect attack. HAMPs from OSs of attacking insect herbivores are perceived by
as-yet-unknown plant cell surface pattern recognition receptors and trigger downstream defenses against insects. Cell damage releases
DAMPs consisting of cell wall fragments or intracellular metabolites that reach the apoplast. Herbivory also triggers the production
and release of endogenous SDSs, such as Arabidopsis Peps and Sys, that bind to pattern recognition receptors and activate defense. Solid
arrows indicate demonstrated effect on insect performance. Dashed arrows indicate absence of direct evidence for a role in defense
against insects. Abbreviations: ATP, adenosine 5 -triphosphate; Cel, cellulose; DAMP, damage-associated molecular pattern; DORN1,
DOES NOT RESPOND TO NUCLEOTIDES 1; EGF, epidermal growth factor; FAC, fatty-acid amino-acid conjugate; FER,
FERONIA; HAMP, herbivore-associated molecular pattern; In, inceptin; LecRK, lectin receptor kinase; LRR, leucine-rich repeat;
NAD, nicotinamide adenine dinucleotide; OG, oligogalacturonide; OS, oral secretion; Pect, pectin; PEPR1/2, Pep1 RECEPTORS 1
and 2; Peps, peptides 1–6; RLK1, RECEPTOR-LIKE KINASE 1; SDS, secondary danger signal; SYR1, SYSTEMIN RECEPTOR 1;
Sys, systemin; THE1, THESEUS1; WAK1, WALL-ASSOCIATED KINASE 1.

occur within seconds and minutes, respectively, in lima bean and Arabidopsis leaves after wounding,
application of HAMPs and DAMPs, and natural feeding by S. littoralis or the aphid Myzus persicae
(111, 136, 143, 172, 175). Use of Ca2+ channel inhibitors suggests that a membrane channel
drives the increase in [Ca2+ ]cyt (111, 143, 187). The vacuolar cation channel TWO-PORE
CHANNEL1 (TPC1) plays a role in defense against herbivores. Indeed, the Arabidopsis TPC1
gain-of-function mutant fou2 possesses a hyperactive version of this cation channel, displays
strong JA pathway activation, and is more resistant to S. littoralis feeding (12, 88). Interestingly,
local aphid-induced [Ca2+ ]cyt elevation is greatly diminished in tpc1-2 (175). Wound- and insect-
triggered long-distance propagation of membrane depolarizations and [Ca2+ ]cyt were recently
shown to be dependent on glutamate receptor-like (GLR) ion channels (123, 168). Interestingly,
S. littoralis larval growth is enhanced on Arabidopsis glr3.1/3.3 and glr3.3/3.6 double mutants (123).
Finally, AtPep3 activates the plasma membrane CYCLIC NUCLEOTIDE–GATED CATION
CHANNEL 2, whose role in response to herbivory is unknown, and triggers [Ca2+ ]cyt elevation
through the guanylyl cyclase activity of AtPEPR1 (136). The guanylyl cyclase activity of AtPEPR1
is controversial, however, and deserves further evaluation (4). There are at least 57 putative cation
channels in the Arabidopsis genome (174), and a high level of functional redundancy could explain
the paucity of characterized candidates.

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The decoding of Ca2+ signals is mediated by various Ca2+ sensors, including calmodulins
(CaMs), calmodulin-like proteins (CMLs), and calcium-dependent protein kinases (CDPKs). In
a series of experiments, Yan et al. (187) demonstrated that the Arabidopsis JA biosynthesis regu-
WRKY transcription
factors: transcription lator JAV1 ( JASMONATE-ASSOCIATED VQ MOTIF 1) is phosphorylated upon wounding
factors involved in and interacts with CaM1, CaM4, and CaM7 in a Ca2+ -dependent manner. Furthermore, the Ara-
defense against insects bidopsis CML37 positively regulates S. littoralis–induced defense by activating the JA pathway (149),
and targeting JA whereas CML42 acts as a negative regulator and cml42 displays enhanced resistance to S. littoralis
biosynthesis genes
and higher [Ca2+ ]cyt accumulation (172). In N. attenuata , the Ca2+ -sensor homologs NaCDPK4
and NaCDPK5 suppress JA biosynthesis and promote M. sexta herbivory through an unknown
mechanism (188). Thus, available studies suggest that different sensors that are part of a larger
regulatory network decode [Ca2+ ]cyt elevation after wounding/feeding.
ROS are induced by herbivory and have been associated with plant defense regulation. Apoplas-
tic plant-derived ROS are primarily produced by plasma membrane NADPH oxidases [respiratory
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burst oxidase homologs (RBOHs)]. Wounding causes a rapid local and systemic ROS burst that
depends on RBOH protein D (RBOHD) in Arabidopsis (116). The rbohD mutant is more suscep-
tible to M. persicae infestation (116), and a silenced rbohD line in N. attenuata is more susceptible
to S. littoralis (184). By contrast, the rbohD/F mutant in Arabidopsis is more resistant to S. exigua
and Trichoplusia ni feeding (10). Thus, ROS can act as both positive and negative regulators of
plant resistance. As RBOHs are activated by ROS-dependent Ca2+ influx and CDPKs, they likely
interact closely with Ca2+ in early defense signaling.
Herbivory and wounding rapidly activate MAPKs (62). Silencing genes encoding WOUND-
INDUCED PROTEIN KINASE (WIPK/MPK3) and SA-INDUCED PROTEIN KINASE
(SIPK/MPK6) in N. attenuata inhibits JA biosynthesis, expression of WRKY transcription fac-
tors, and accumulation of defense compounds (183). Silencing tomato MPK6 orthologs MPK1
and MPK2 renders plants more susceptible to M. sexta and the potato aphid Macrosiphum euphor-
biae (72, 90). In rice, SSB activates MPK3 and MPK6, which positively regulate JA accumulation.
Consequently, the inverted repeat mpk3 line is more susceptible to SSB feeding (65, 93, 179). In
contrast, N. attenuata MPK4 suppresses JA-dependent defenses, and silencing MPK4 increases
resistance to the specialist M. sexta but not to the generalist S. littoralis (56).
In summary, molecular studies have provided clear evidence for the involvement of Ca2+ , ROS,
and MAPKs in plant responses to DAMPs and HAMPs, thus supporting current models of early
defense signaling. However, major open questions remain. It is, for instance, unclear how poten-
tial PRRs are connected to these early signaling events, how Vm variation is connected to Ca2+
influx, if there is a hierarchical or independent organization of the signaling network, how positive
and negative regulatory steps are modulated, and to what extent the network topology is species
dependent (Figure 2). Thus, understanding the topology of early signaling networks of plant re-
sponses to herbivory remains a major challenge, and integrating quantitative genetics and systems
biology approaches may be necessary to overcome it.

Jasmonate Signaling as a Conserved Core Pathway in Herbivory-Induced

Responses
Hormonal signaling networks connect perception and early signaling to broad transcriptional re-
organization and defense induction. JA signaling is well established as the core pathway that regu-
lates plant defense responses against herbivores, and intense research over the past two decades has
revealed essential molecular components of the JA pathway (63). In brief, upon injury, acyl-lipid
hydrolases release α-linolenic acid (18:3) from galactolipids in plastid membranes. Oxygenation by
13-lipoxygenases is followed by epoxidation and cyclization reactions to generate OPDA. OPDA

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Activation
Activation through unknown mechanisms
Negative regulation
GOX
HAMPs
DAMPs Ca2+ channel H2O2
Apoplast SDSs O2 O2–

Vm RBOHD/F

Cytosol PRRs Membrane ROS signaling

depolarization

Ca2+ Ca2+ signaling

CML37 CaM1/4/7 H2O2
MAPK signaling
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WRKY53 MAPKs
JAV1, JAZ8
WRKY51
Transcription MPK4
factors
WRKYs
JA
JA-Ile signaling

WRKY70 CDPK4/5
SCFCOI1
CML42 JAZs
EREB58
Sesquiterpenes
WRKYs
MYC2
MYBs Nicotine
MYCs Sesquiterpenes
MYBs Threonine deaminase
Phenylpropanoids JAMs Proteinase inhibitors

Glucosinolates

Figure 2
Current model of plant defense signaling network in response to herbivory. HAMPs from oral secretions, DAMPs from damaged cells,
or SDSs (e.g., systemin, Arabidopsis peptides) are perceived by PRRs at the plasma membrane. Membrane depolarization (Vm ) (magenta),
Ca2+ signaling (yellow), ROS signaling (green), and downstream MAPK signaling (orange) steps are activated and trigger the biosynthesis
of JA-Ile, the bioactive form of JA. Chloroplast- and peroxisome-located enzymes (not shown) are rapidly activated to generate the
primary JA burst through unknown mechanisms (dashed arrow). Binding of JA-Ile to the SCFCOI1 complex leads to degradation of JAZ
repressors (blue), resulting in activation of transcription factors (blue-green) that regulate the production of defense metabolites and
proteins. H2 O2 accumulation can be stimulated by Ca2+ -activated NADPH oxidases (RBOHD and RBOHF) or by GOX in oral
secretions. Several negative regulators have been identified and contribute to the fine-tuning of the JA pathway (red lines). Higher level
of regulation by other hormonal pathways and plant secondary metabolites is not shown. MYBs involved are MYB8, MYB12, MYB28,
MYB29, MYB34, MYB51, MYB75, MYB76, and MYB122; MYCs are MYC2, MYC3, MYC4, and MYC5; and WRKYs are WRKY3,
WRKY6, WRKY18, WRKY40, WRKY53, WRKY70, WRKY72, and WRKY89. Abbreviations: CaM, calmodulin; CDPK,
calcium-dependent protein kinase; CML, calmodulin-like; DAMP, damage-associated molecular pattern; EREB58, APETALA
2/ethylene responsive factor; GOX, glucose oxidase; HAMP, herbivore-associated molecular pattern; JA, jasmonate; JA-Ile,
jasmonoyl-L-isoleucine; JAM, JASMONATE-ASSOCIATED MYC2-LIKE; JAV1, jasmonate-associated VQ motif 1; JAZ,
JASMONATE-ZIM DOMAIN; MAPK/MPK, mitogen-activated protein kinase; PRR, pattern recognition receptor; RBOH,
respiratory burst oxidase homolog; ROS, reactive oxygen species; SCFCOI1 , SKP1–CUL1–F-box protein E3 ubiquitin ligase; SDS,
secondary danger signal.

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is transported into the peroxisome, where it is reduced and undergoes three cycles of β-oxidation
to form (+)-7-iso-JA, which is transported into the cytosol, where it is conjugated to isoleucine
by the jasmonoyl amino acid conjugate synthase JAR1. Jasmonoyl-L-isoleucine ( JA-Ile) is the
CORONATINE-
INSENSITIVE1 canonical bioactive JA and is transported into the nucleus by the ABC transporter JAT1. JA-Ile
(COI1): F-box protein binds to its nuclear receptor, which is a complex consisting of CORONATINE-INSENSITIVE1
that is the receptor of (COI1), JASMONATE-ZIM DOMAIN ( JAZ), and an inositol-polyphosphate cofactor. COI1 is
JA-Ile and the major a component of a SKP1–CUL1–F-box protein E3 ubiquitin ligase (SCFCOI1 ) complex and, upon
regulator of plant
binding JA-Ile, interacts with JAZ repressors and triggers their degradation by the 26S protea-
defense against insects
some. JAZ degradation releases repression of MYC transcription factors, resulting in expression
JASMONATE-ZIM of defense genes and resistance against a wide variety of herbivores (Table 1 and Supplemental
DOMAIN ( JAZ):
Table 1). The JA signaling pathway was likely already present in early land plants such as liv-
family of repressors
that inhibit erwort. As recently shown, COI1 of Marchantia polymorpha is a functional protein that regulates
transcription of resistance to herbivory (118). Strikingly, MpCOI1 harbors a single amino acid substitution that
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allows it to bind to two isomeric forms of dinor-OPDA but not to JA-Ile, which is absent from
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defense genes,
including basic M. polymorpha (118).
helix-loop-helix
Although the JA pathway has been extensively studied, there are still some open questions.
(bHLH) MYC factors
The connection between early defense signaling and the activation of acyl-lipid hydrolases in
MYC transcription chloroplasts to initiate JA biosynthesis, for instance, remains largely unknown. A recent Arabidopsis
factors: basic
study by Yan et al. (187) showed that Ca2+ /CaM-dependent phosphorylation of JAV1 leads to its
helix-loop-helix
(bHLH) transcription degradation by the proteasome, disrupting a nuclear JAV1-JAZ8-WRKY51 repressing complex
factors; Arabidopsis that inhibits expression of JA biosynthesis genes. This work provides the first coherent model
MYC2–MYC5 are that links herbivore-induced [Ca2+ ]cyt accumulation with JA biosynthesis. Of note, JA accumulates
targets of JAZs and within 30 s in wounded Arabidopsis tissues (47), suggesting that the first JA burst does not require
regulate transcription
transcriptional activation of JA biosynthesis genes and that JAV1-mediated regulation may instead
of defense genes
be a secondary amplification step (Figure 2).

Signaling Networks Mediated by Small Metabolites

Plant responses to herbivory display a great deal of specificity, which is incompatible with the no-
tion of a single hormonal pathway controlling all responses. Indeed, numerous other hormones
influence JA-dependent and JA-independent responses through hormonal crosstalk. Furthermore,
inducible plant secondary metabolites are emerging as defense regulators that can modulate de-
fense deployment, thereby increasing the specificity of the signaling networks underlying plant
defense responses.
SA, ethylene (ET), and abscisic acid (ABA) are stress-related phytohormones that are induced
upon herbivory and are well-established modulators of plant resistance to herbivores. The im-
pact of these hormones on resistance seems to be highly context dependent. SA-deficient tomato
plants, for instance, are more susceptible to the potato aphid, whereas SA-signaling mutants in
Arabidopsis are not affected in their resistance to M. persicae (31, 90). Furthermore, Arabidopsis mu-
tants deficient in SA biosynthesis (sid2-1) or signaling (npr1) are more resistant to S. littoralis and
Bemisia tabaci (11, 191). The SA pathway antagonizes JA signaling and can therefore act as a nega-
tive regulator of JA-dependent defenses in plants (133). Silencing a rice 1-aminocyclopropane-1-
carboxylic acid synthase reduces rice ET production and resistance to the chewing herbivore SSB
but increases resistance to the phloem feeder BPH (100). By contrast, Arabidopsis ET-insensitive
mutants ein2-1 and ein3 eil1 are more resistant to S. littoralis and S. exigua (11, 160). ET-stabilized
transcription factors ETHYLENE-INSENSITIVE 3 (EIN3) and EIN3-LIKE1 interact with
JA-activated MYC2 and inhibit JA-regulated defenses against herbivores, providing a molec-
ular mechanism for such ET/JA antagonism (160). ABA-deficient Arabidopsis plants are more

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Table 1 Examples of plant genes with a demonstrated role in plant–insect interactions

Insect performance on
Gene Description Plant Genotype altered genotypea Reference(s)
Perception
LecRK1–3 Lectin-like RK Rice, Nicotiana OE lecRK1–3, IR Nilaparvata lugens ↓, 46, 96
attenuata lecRK1 Manduca sexta ↑
LRR-RLK1 LRR-RK Rice IR LRR-RLK1 Chilo suppressalis ↑ 64
PEPR1/2 LRR-RK, Pep Arabidopsis pepr1/2 Spodoptera littoralis ↑ 79
receptor
Prosystemin Systemin precursor Tomato AS prosystemin M. sexta ↑ 127
SYR1 LRR-RK, systemin Tomato syr1 S. littoralis ↑ 178
receptor
Ca2+ , ROS, MAPK signaling
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Vacuolar cation S. littoralis ↓, Myzus 88, 175

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TPC1 Arabidopsis fou2

channel persicae ↓
JAV1 JA-associated VQ Arabidopsis RNAi JAV1 Spodoptera exigua ↓, 66
motif M. persicae ↓
CML37/42 CaM-like protein Arabidopsis cml37, cml42 S. littoralis ↑, S. littoralis ↓ 149, 172
CDPK4/5 Ca2+ -dependent N. attenuata IR CDPK4/5 M. sexta ↓ 188
protein kinase
RBOHD/F NADPH oxidase Arabidopsis rbohD/F S. exigua ↓, M. persicae ↑ 10, 116
MPK1/2/3 MAPK Tomato, rice mpk1/2, IR MPK3 M. sexta ↑, C. suppressalis ↑ 72, 179
MPK4 MAPK N. attenuata IR MPK4 M. sexta ↓ 56
JA pathway
LOX2/3/4/6 13-Lipoxygenase Arabidopsis, rice lox2/3/4/6, AS S. littoralis ↑, N. lugens ↓ 22, 197
HI-LOX
AOS Allene oxide synthase Arabidopsis aos Trichoplusia ni ↑ 50
AOC Allene oxide cyclase Rice, hebiba, IR AOC Diabrotica balteata ↑, 44, 101
N. attenuata M. sexta ↑
OPR3 OPDA reductase Arabidopsis opr3-3 S. littoralis ↑ 24
ACX1 Acyl-CoA oxidase Arabidopsis acx1/5 T. ni ↑ 144
JAR1 JA-Ile synthase Arabidopsis jar1 T. ni ↑ 50
COI1 F-box protein Arabidopsis, coi1-1 S. littoralis ↑, Bemisia 11, 44, 191
N. attenuata tabaci ↑, M. sexta ↑
JAZ Jasmonate ZIM Arabidopsis jaz1/3/4/9/10 T. ni ↓ 112
domain
Transcription factors
MYC2/3/4/5 bHLH TF Arabidopsis myc2/3/4, myc2/3/4/5 S. littoralis ↑ 154, 161
JAMs bHLH TF Arabidopsis bhlh3/13/14/17 S. exigua ↓ 162
WRKY18/40 WRKY TF Arabidopsis wrky18/40 S. littoralis ↑ 153
WRKY53 WRKY TF Rice, wheat IR WRKY53 C. suppressalis ↓ 65
WRKY70 WRKY TF Rice, IR WRKY70, wrky70 N. lugens ↓, Pieris 93, 125
Arabidopsis brassicae ↓
MYB28/29 MYB TF (aliphatic Arabidopsis myb28/29 M. sexta ↑, S. exigua ↑ 122
GS)
MYB75 MYB TF Arabidopsis OE MYB75 P. brassicae ↑ 126
(phenylpropanoids)
(Continued)

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Table 1 (Continued)
Insect performance on
Gene Description Plant Genotype altered genotypea Reference(s)
Defense regulators (hormones and secondary metabolites)
ICS1 Isochorismate Arabidopsis sid2-1 S. littoralis ↓, P. brassicae ↓ 11, 125
synthase (SA)
NPR1 Nonexpressor of PR-1 Arabidopsis npr1 S. littoralis ↓, B. tabaci ↓ 11, 191
(SA)
ACS2 Ethylene biosynthesis Rice AS ACS2 C. suppressalis ↑, 100
N. lugens ↓
EIN2 Ethylene insensitive Arabidopsis ein2-1 S. littoralis ↓ 11
EIN3/EIL1 TF, ethylene signaling Arabidopsis ein3 eil1 S. exigua ↓ 160
ABA1 Zeaxanthin epoxidase Arabidopsis aba1-1 M. persicae ↓ 60
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ABA2 Xanthoxin Arabidopsis aba2-1 S. littoralis ↑ 11

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dehydrogenase
HER1 Inhibitor of ABA N. attenuata IR HER1 M. sexta ↑ 34
catabolism
CYP714D1 CYP450 (GA Rice eui N. lugens ↓ 93
catabolism)
BX1 Indole-3-glycerol P Maize bx1 Rhopalosiphum padi ↑ 3
lyase
Direct defense traits
CYP79B2/B3 CYP450 (indole GS) Arabidopsis cyp79b2/b3 S. exigua ↑ 122
TGG1/2 Myrosinase (GS Arabidopsis tgg1/2 M. sexta ↑, T. ni ↑ 6
activation)
CYP81F2 CYP450 (indole GS) Arabidopsis cyp81F2 M. persicae ↑ 132
PAD3 Camalexin Arabidopsis pad3-1 B. brassicae ↑ 86
biosynthesis
F5H Ferulate hydroxylase Arabidopsis fah1-7 P. brassicae ↑ 125
BX1/13 Benzoxazinoid Maize bx1, bx13 S. littoralis ↑, R. maidis ↑ 54, 105
biosynthesis
PMT Nicotine biosynthesis N. attenuata IR PMT M. sexta ↑ 165
TPS08 Terpene synthase Arabidopsis tps08-1 Bradysia sp. ↑ 173
ShZIS Sesquiterpene Tomato OE ShZIS M. sexta ↓ 9
synthase
GAS1 Germacrene synthase Taraxacum RNAi GAS1 Melolontha melolontha ↑ 67
officinale
PIN I/II Proteinase inhibitors Tobacco OE PIN I/II M. sexta ↓ 71
Mir1-CP Cysteine protease Maize OE Mir1-CP Spodoptera frugiperda ↓ 130
TD Threonine deaminase Tomato AS TD2 S. exigua ↑, T. ni ↑ 49
ARG2 Arginase Tomato OE ARG2 M. sexta ↓ 23
PP2-A1 Phloem protein Arabidopsis OE PP2-A1 M. persicae ↓ 192
SLI1 Chaperone Arabidopsis sli1-1 M. persicae ↑ 80
GL1 Trichome formation Arabidopsis gl1 S. littoralis ↑ 137
ATL2 Wax and cutin Arabidopsis eca S. littoralis ↓ 8
formation
(Continued)

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Table 1 (Continued)
Insect performance on
Gene Description Plant Genotype altered genotypea Reference(s)
Putative indirect defense traits
HPL Hydroperoxide lyase N. attenuata AS HPL Geocoris punctipes ↓↓ 53
TPS10 Terpene synthase Arabidopsis OE TPS10 Cotesia marginiventris ↑↑ 148
TPS23 (E)-β-caryophyllene Maize OE E-βC Heterorhabditis megidis ↑↑, 32
synthase Diabrotica virgifera ↓
LIS S-linalool synthase Rice IR LIS N. lugens ↑, Anagrus 185
nilaparvatae ↓↓
Others
ZTL Zeitlupe, clock N. attenuata IR ZTL S. littoralis ↑ 91
component
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N. lugens ↓, Sogatella
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BPH6 Unknown, binds Rice Bph6-carrying lines 52

EXO70E1 furcifera ↓

Abbreviations: ABA, abscisic acid; Acy-CoA, acetyl coenzyme A; AS, antisense; bHLH, basic helix-loop-helix; CaM, calmodulin; GA, gibberellin; GS, glucosi-
nolate; IR, inverted repeat; JA, jasmonate; JA-Ile, jasmonoyl-L-isoleucine; LRR-RK, leucine-rich-repeat receptor kinase; MAPK, mitogen-activated protein
kinase; OE, overexpression; OPDA, 12-oxo-phytodienoic acid; RLK, receptor-like kinase; RNAi, RNA interference; SA, salicylic acid; TF, transcription
factor.
a
↑, enhanced insect performance; ↓, reduced insect performance; ↑↑, enhanced attraction of natural enemy; ↓↓, reduced attraction of natural enemy. For a
more complete list of genes and a description of insect and nematode species, see Supplemental Tables 1 and 2.

susceptible to S. littoralis (11). In N. attenuata, HERBIVORE ELICITOR REGULATED 1

(HER1) inhibits ABA catabolism. Lines with reduced HER1 expression are more susceptible to
M. sexta and accumulate fewer JA and defense metabolites (34). Because ABA is involved in drought
stress, a response that often occurs after leaf damage, it is not surprising that ABA contributes and
may even reinforce plant resistance to chewing herbivores. The recent finding that expression of
Arabidopsis chloroplast-localized glycerolipid A1 lipases PLIP2 and PLIP3 is induced by ABA and
leads to JA accumulation provides an attractive mechanistic link between ABA accumulation and
downstream JA-defense responses. Herbivore performance on plip2/3 mutants has, however, not
been tested (177). Furthermore, pea aphid performance is decreased on the ABA biosynthesis mu-
tant aba1-1 in Arabidopsis (60). In summary, SA, ET, and ABA are well-established modulators of
Feeding guild: group
plant defense and resistance, but their impact varies among plant species and herbivore feeding of unrelated insect
guilds. species with a similar
Growth hormones such as gibberellins (GAs), auxin, and cytokinins (CKs) may also be involved feeding behavior
in the regulation of antiherbivore defenses. GAs regulate growth via proteasome-mediated degra- Glucosinolate (GS):
dation of DELLA repressors. DELLAs modulate the JA pathway by physically interacting with sulfated secondary
JAZs, thereby preventing the negative effect of JAZs on MYC2-related defense expression. Thus, metabolite essential
activation of the GA pathway leads to DELLA degradation and inhibition of JA responses. How- for defense against
insects in Brassicaceae
ever, the Arabidopsis quad della mutant does not display dramatic changes in defense metabolite
accumulation upon S. exigua feeding, and insect performance has not been tested (87). In con- Benzoxazinoids:
trast, a rice GA-accumulating mutant increases resistance to BPH, suggesting that GAs positively indole-derived defense
compounds in grasses
regulate defense against phloem-feeding insects (93). Auxins and CKs have been explored in the
that are effective
context of systemic defense regulation and are discussed in more detail below (see the section against insects and
titled Systemic Regulation of Defenses). plant pathogens
Apart from hormones, induced plant secondary metabolites are increasingly recognized as reg-
ulators of plant defense deployment. Glucosinolate (GS) breakdown products in Arabidopsis and
benzoxazinoids in maize act as positive regulators of callose accumulation (27, 114), and various

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plant volatiles prime JA signaling and plant defense (104). Flavonols and the GS breakdown prod-
uct indole-3-carbinol inhibit auxin transport and perception signaling and may thereby influence
plant responses to herbivores (74). These recent findings blur the dichotomy between defense
hormones and defense metabolites and suggest that plants can use a wide variety of molecules to
specifically regulate their defenses. Understanding the evolutionary and ecological implications of
this phenomenon will be greatly facilitated by the availability of secondary metabolite biosynthesis
mutants in various plant species.
In addition, studies in N. attenuata suggest that small RNAs can modulate the JA pathway
during herbivory. Insect feeding induces a significant change in the small-RNA transcriptome
(128), and N. attenuata mutants in components of the small-RNA machinery are more susceptible
to insects (Supplemental Table 1). However, how small RNAs modulate the reprogramming of
plant defenses and whether this regulation occurs in other plants need further research.
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Transcription Factors as Major Players in Early and Late Defense Signaling

Transcription factors play a key role in regulating defenses both up- and downstream of phyto-
hormone signaling. Basic helix-loop-helix (bHLH) MYCs form a transcriptional complex that
regulates defense against herbivores in Arabidopsis. In absence of insect feeding, JAZs bind and re-
press MYCs. Activation of the JA pathway leads to JAZ degradation, subsequent binding of MYCs
to MED25 of the mediator complex, and recruitment of RNA polymerase II (for a review, see 63).
Four closely related MYCs from the IIIe subgroup of bHLH factors act synergistically to con-
trol JA-dependent defenses. Indeed, single and higher-order mutants of MYC2, MYC3, MYC4,
and MYC5 display increasing susceptibility to S. littoralis and S. exigua feeding (43, 161). Fur-
thermore, myc2/3/4 is as susceptible as coi1-1 to S. littoralis, and both mutants show a similarly
altered transcriptome in response to feeding, indicating that MYCs are the main contributors of
defense against chewing herbivores in Arabidopsis (153). MYCs bind to the G-box on promoters
of target genes, including GS biosynthesis genes (43, 154). In addition to MYCs, GS biosynthe-
sis requires coordinated activity of six MYB transcription factors. MYB28, MYB29, and MYB76
regulate synthesis of methionine-derived aliphatic GS, and MYB34, MYB51, and MYB122 reg-
ulate synthesis of tryptophan-derived indole GS (45). These MYBs interact directly with MYC2,
MYC3, and MYC4, but not with JAZs, and are also necessary for GS biosynthesis and defense
(154). For instance, myb28/29 lacks aliphatic GS and is susceptible to several lepidopteran her-
bivores (122). Thus, MYCs and MYBs together constitute a functional regulatory module that
controls expression of GS genes in Arabidopsis.
In addition, MYCs regulate expression of other antiherbivore genes. In Arabidopsis, MYC2
binds to the promoter of TPS11 and TPS21 to regulate sesquiterpene biosynthesis (61). In N. at-
tenuata, MYC2 homologs directly control nicotine biosynthesis (182). In tomato, MYC2 regulates
the expression of many defense genes, including genes coding for known antiherbivore defense
proteins, such as threonine deaminase and proteinase inhibitor 1 (36). Other transcription factors
with demonstrated antiherbivore effect have also been identified, including WRKY18, WRKY40,
WRKY53, and WRKY70 as well as MYB75 (93, 126, 153) (Figure 2, Table 1, and Supplemental
Table 1). Yet, how these proteins regulate defense is unclear.
Evidence of negative regulation of MYC activity has recently been demonstrated. Four mem-
bers of the IIId subgroup of Arabidopsis bHLHs (bHLH3, bHLH13, bHLH14, and bHLH17)
act additively as transcription repressors. Also known as JA-ASSOCIATED MYC2-LIKE, they
competitively bind to target sequences of MYC2. Consequently, their single or multiple mutants
have enhanced JA-dependent defenses and are more resistant to S. exigua (140, 162). As discussed
above, WRKY51 inhibits JA biosynthesis through association with JAV1 and JAZ8. WRKY51

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binds to a W-motif on the promoter of ALLENE OXIDE SYNTHASE and inhibits its expression,
potentially preventing unnecessary JA biosynthesis in the absence of feeding (187). Rice MPK3
and MPK6 directly phosphorylate WRKY53 (190), which in turn interacts with both MPK3 and
MPK6 and suppresses their activity (65). This creates a negative feedback loop that restricts over-
expression of defense genes. Accordingly, inverted repeat wrky53 is more resistant to the SSB C.
suppressalis (65). These findings illustrate tight regulation of different steps of the JA pathway by
various transcription factors (Figure 2). Future work should elucidate whether and how different
biotic or abiotic stresses interact with these negative regulators.

Systemic Regulation of Defenses

Herbivores are often mobile and move from attacked to nonattacked tissues. Upon herbivore at-
tack, plants can use systemic signals to regulate defenses in systemic tissues in preparation for an
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incoming attack. The important role of JA signaling in the activation of systemic defense regula-
tion is well established. Grafting experiments with N. attenuata show that silencing homologs of JA
biosynthesis and perception genes such as AOC and COI1 in roots reduces the capacity to accu-
mulate nicotine and to deploy it to leaves, leading to enhanced aboveground herbivory by M. sexta
and S. littoralis (44). To what extent JAs are moving between local and systemic tissues to regulate
defenses is still subject to debate. Localized manipulation of JA biosynthesis and perception shows
that the production of JAs in systemic tissues, but not in locally induced tissues, is important for
systemic defense deployment in Arabidopsis and N. attenuata (44, 82). In Arabidopsis, glutamate-like
receptor genes are required for the induction of systemic JA synthesis, and their silencing has been
associated with a reduction in wound-induced, systemic surface potential charges, suggesting that
electrical potentials are important for the systemic induction of JAs (120). Ca2+ and ROS have
also been implicated in rapid systemic signaling, most probably in interaction with membrane
potentials (for a review, see 59).
Recent work demonstrates that, apart from JA, other mobile hormones such as CKs and auxins
may regulate systemic defense responses. Wounded N. attenuata plants silenced in homologs of
the CK receptor CHASE-DOMAIN CONTAINING HIS KINASE 2 accumulate lower levels of
caffeoylputrescine in systemic leaves (142). Furthermore, inhibiting auxin transport through appli-
cation of the indole-3 acetic acid biosynthesis inhibitor L-kynurenine or the transport inhibitor
2,3,5-triiodobenzoic acid abolishes herbivore-induced systemic induction of stem anthocyanins
(109). Further experiments with auxin and CK signaling mutants are required to understand the
impact of these hormones on plant resistance to herbivores.
Plants can also use volatiles to regulate systemic defenses. Several volatile organic compounds
including C6 green-leaf volatiles, terpenes, and indole can be emitted by herbivore-attacked leaves
and can induce and/or prime defenses in systemic leaves (39). Using an igl mutant that does not
produce indole, investigators showed that this volatile is required for the priming of monoter-
penes in systemic maize leaves (40). Arabidopsis genes involved in root response to (E)-2-hexenal
include the gamma-amino butyric acid (GABA) transaminase HER1, which degrades GABA, and
the oxidoreductase HER2, which regulates the redox status in mitochondria (117, 141). Systemic
signaling through plant volatiles may be particularly important when vascular constraints and long
vascular distances between adjacent tissues limit the spread of internal signals.

Spatiotemporal Control of Plant Defense Deployment

Many constitutive and induced defenses show pronounced ontogenetic (i.e., developmental) pat-
terns and vary with the age of plants and organs. Although this variation has been mapped in great

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SECONDARY METABOLITE TRANSPORT

Transport allows plants to partition biosynthesis and accumulation of defensive secondary metabolites and to control
their local and systemic accumulation. Alkaloids are often synthesized in belowground tissues and then transported
to the leaves. In tobacco, NtMATE1 and NTMATE2 transport nicotine from the cytoplasm into the vacuole of
root cells, whereas Nt-JAT1 and Nt-JAT2 have a similar function in leaves (119, 158). Furthermore, the tobacco
permease NUP1 supports uptake of nicotine from the apoplast into root cells (58). In Coptis japonica, two ABC trans-
porters, CjABCB1 and CjABCB2, function as berberine importers from the xylem into the rhizome (157). Finally,
the tonoplast localized nitrate/peptide family transporter CrNPF2.9 from Catharanthus roseus exports strictosidine
from the vacuole to the cytosol (129). Most transporters identified so far function in metabolite uptake or subcel-
lular localization, and much less is known about the molecular basis of systemic secondary metabolite transport. In
Arabidopsis, two proton-dependent transporters, GTR1 and GTR2, transport GS from leaves and silique walls to
the seeds (124). In Petunia hybrida, the ABC transporter PhABCG1 releases benzenoid volatiles from flowers (2).
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These recent discoveries pave a way to understand the contribution of systemic secondary metabolite transport
through the vasculature and the headspace of plant–herbivore interactions.

detail in many different plant species (7), the underlying molecular mechanisms are only beginning
to be unveiled. In addition, secondary metabolite transporters have been identified as important
determinants of defense distribution (see the sidebar titled Secondary Metabolite Transport).
In maize, the decline of benzoxazinoids in older plants has been mapped to the Bx gene cluster
containing major benzoxazinoid biosynthesis genes (196). Expression of Bx1, the gene encoding
for an indole-3-glycerol-phosphate lyase that provides indole as a benzoxazinoid precursor, is as-
sociated with benzoxazinoid levels, and its overexpression enhances benzoxazinoid levels in older
maize plants (196), thus suggesting that a decrease of these metabolites in older plants is the re-
sult of transcriptional regulation of biosynthesis genes (103). Transcriptional regulation may also
regulate tissue-specific production of alkaloids and other secondary metabolites in plants (89).
For instance, a cluster of ethylene responsive factor (ERF) transcription factors regulates the ex-
pression of nicotine biosynthesis genes in tobacco. Although nicotine accumulates specifically in
roots, expression of some of these ERFs is not restricted to roots and is also observed in leaves,
suggesting that another factor is crucial for root-specific biosynthesis or that ERFs are inhibited
in leaves (159). In N. attenuata, CKs covary with caffeoylputrescine inducibility, which is higher
in young versus old leaves. Increasing CK levels through dexamethasone-inducible expression of
the CK biosynthesis isopentenyltransferase is sufficient to restore the inducibility of caffeoylpu-
trescine in old leaves (18). In N. attenuata flowers, only one member of the JAZ family of repressors,
NaJAZi, regulates constitutive accumulation of defense compounds, and silenced NaJAZi lines
show reduced feeding by the florivore Heliothis virescens (92). The capacity to manipulate ontoge-
netic patterns of defense expression will eventually allow for testing of long-standing ecological
hypotheses such as the optimal defense theory, which predicts that ontogenetic patterns reflect
costs and benefits of defense production (115).
Defense metabolites also show diurnal fluctuations that may be tailored to insect feeding be-
havior. For instance, Arabidopsis displays circadian accumulation of JA and GS that correlates with
circadian feeding of T. ni. Consumption of plants exposed to experimentally desynchronized T. ni
larvae is significantly greater than under normal conditions (50). In N. attenuata, many herbivore-
induced metabolites show tissue-specific diurnal rhythmicity (77). Silencing the clock component
ZEITLUPE in N. attenuata renders plants more susceptible to S. littoralis. ZEITLUPE interacts
with JAZs, therefore enhancing MYC2-dependent expression of nicotine biosynthesis genes (91).

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Tobacco plants emit herbivore-induced volatiles during the night to repel oviposition by noctur-
nal female moths of the pest H. virescens (30). Similarly, N. attenuata TPS38 is expressed in flowers
during the night and produces (E)-α-bergamotene that attracts M. sexta moths for pollination,
whereas the same gene is expressed in leaves upon M. sexta feeding and triggers production of
(E)-α-bergamotene during the day to attract predators of M. sexta larvae (198).

PLANT DEFENSE TRAITS

Physical barriers, secondary metabolites, and defense proteins directly determine herbivore resis-
tance by interacting with the feeding, digestive system, and physiology of the attacker (41, 62).
Molecular studies have become instrumental in providing evidence for the functional importance
of multiple putative defense traits in vivo.
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Toxic Secondary Metabolites

Plants produce hundreds of thousands of different specialized metabolites, many of which are as-
sumed to function as defenses by reducing the digestibility of plants. In Arabidopsis, mutations in
genes involved in GS biosynthesis, regulation, or activation render plants highly susceptible to a
wide range of chewing herbivores (Table 1 and Supplemental Table 1). For specialist insects
adapted to GS, metabolites from the phenylpropanoid pathway provide some level of resistance.
Arabidopsis fah1-7 lacks sinapoyl malate and shows increased susceptibility to P. brassicae (125). In
addition, reduced levels of kaempferol 3,7-dirhamnoside in MYB75 overexpression lines correlates
with increased P. brassicae performance (126). In tobacco, reducing nicotine content in silenced
N. attenuata lines increases performance of M. sexta, S. exigua, and other native herbivores, an effect
that can be reversed by applying nicotine (106, 165). In maize, a bx1 mutant devoid of benzoxazi-
noids, 2-(2,4-dihydroxy-7-methoxy-1,4-benzoxazin-3-one)-β-D-glucopyranose (DIMBOA-Glc)
and 2-(2-hydroxy-4,7- dimethoxy-1,4-benzoxazin-3-one)-β-D-glucopyranose (HDMBOA-Glc),
allows increased feeding by S. exigua and S. littoralis (105). In tomato, production of the sesquiter-
pene 7-epizingiberene by expression of a terpene synthase from a wild variety increases resistance
to M. sexta (9). The diterpene rhizathalene A is produced in Arabidopsis roots by terpene synthase
TPS08, and feeding by the root herbivore Bradysia sp. significantly increases in tps08-1 (173). In
dandelion (Taraxacum officinale), silencing the germacrene A synthase ToGAS1, which catalyzes for-
mation of sesquiterpene lactone taraxinic acid β-D-glucopyranosyl ester in root latex, enhances
the attractiveness of roots to the common cockchafer Melolontha melolontha (67).
For phloem-feeding insects, the role of secondary metabolites is less clear. Mutants with altered
indole GS levels, for instance, display contrasting effects on aphid performance (6, 132). The Ara-
bidopsis camalexin-deficient pad3-1, by contrast, is susceptible to aphids (86). In maize, benzoxazi-
noids are directly toxic and regulate callose inducibility, allowing them to operate against chewing
and phloem-feeding insects (114). A bx13 mutant defective in the conversion of DIMBOA-Glc to
DIM2 BOA-Glc and HDM2 BOA-Glc slightly enhances the performance of the corn leaf aphid,
Rhopalosiphum maidis (54).

Defense Proteins
Overexpression of proteinase inhibitor genes in transgenic plants has provided the first evidence
that proteinase inhibitors are efficient antiherbivore proteins (71). Further work with knockout
lines has confirmed the importance of proteinase inhibitors in several plant species against
various herbivores (Supplemental Table 1). Overexpression of a cysteine protease in maize

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disrupts insect peritrophic matrix and severely retards growth of S. frugiperda (130). Depletion
of essential amino acids from insect diets is another efficient defense strategy. Transgenic tomato
lines deficient in the threonine deaminase TD2 are more susceptible to S. exigua and T. ni (49).
Interestingly, proteolytic activation in insect midgut releases feedback inhibition by isoleucine
and enhances TD efficiency (23). Similarly, TD-deficient N. attenuata lines are more susceptible
to M. sexta (73). Finally, overexpression of arginase in tomato significantly reduces arginase in
larval midgut and renders plants more resistant to M. sexta (23).
To our knowledge, there are only three reports demonstrating a role for defense proteins
against phloem-feeding insects. Overexpression of PP2-A1, a member of the multigene family
of Arabidopsis phloem lectins, reduces M. persicae infestation, presumably by clogging sieve pores
(192). SLI1 is a recently identified membrane-anchored chaperone that may prevent a stylet from
piercing the parietal membrane of sieve tubes. Arabidopsis sli1 shows enhanced feeding and infes-
tation by M. persicae (80). In rice, Bph6 is an unknown protein that interacts with exocyst subunit
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EXO70E1. Bph6-carrying cultivars provide resistance to BPH and Sogatella furcifera by increased
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exocytosis and cell wall reinforcement (52).

Volatiles as Attractants of Herbivore Natural Enemies

Plants that are attacked by herbivores release distinct volatile blends, which affect herbivores
and increase the attraction of herbivore natural enemies. Molecular approaches have helped re-
searchers understand how these effects affect plant–herbivore interactions. Overexpressing the
hydroperoxide lyase gene HPL in Arabidopsis enhances the production of green-leaf volatiles, ren-
ders plants more attractive to the Cotesia glomerata parasitoid, and increases Pieris rapae larval mor-
tality (156). Silencing HPL in N. attenuata significantly reduces the attraction of the egg predator
Geocoris punctipes in the field (53), and silencing LOX2, which is involved in green-leaf volatile
biosynthesis, reduces predator recruitment and increases damage by M. sexta (151). Transgenic
Arabidopsis lines that overexpress the maize terpene synthase TPS10 emit more herbivore-induced
sesquiterpenes and are more attractive to Cotesia marginiventris (148). Interestingly, expression of
the maize APETALA 2 (AP2)/ERF EREB58 is induced by JA treatment, and this factor binds
to the promoter of TPS10 to control the production of volatile sesquiterpenes (94). In rice, si-
lencing S-linalool synthase diminishes attraction of the parasitoid Anagrus nilaparvatae, leading to
enhanced BPH performance in laboratory and field conditions (185). In maize, overexpression of
the terpene synthase TPS23 increases the recruitment of entomopathogenic nematodes, the west-
ern corn rootworm, and S. frugiperda in the field (32), resulting in neutral effects on plant yield
(139). Overexpressing the terpene synthase Eβf in wheat repels aphids and increases parasitoid
recruitment in the laboratory, but it has not resulted in clear effects in a 2-year field trial (16).
A recent study with an indole-deficient igl maize mutant demonstrates that indole attracts para-
sitoids to plants but reduces the attractiveness of caterpillars, thereby reducing overall parasitoid
recruitment (189). Together, these manipulative studies reveal that the effects of plant volatiles
on plant–herbivore interactions can be multifaceted and can result in unexpected patterns, which
complicates their use as strengtheners of biological control (171).

Physical Barriers
Physical barriers of plants such as trichomes, cuticle, epidermis, and bark tissues are important
for stopping herbivores from attaining nutritious plant tissues. Arabidopsis lyrata genotypes with
mutation in GLABROUS1 suffer from a higher abundance of leaf-chewing insects in the field
(78), whereas Arabidopsis gl1 is more susceptible to S. littoralis in the laboratory (137). Surprisingly,

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an Arabidopsis mutant with reduced cuticular wax and cutin is more resistant to feeding by the
generalist S. littoralis (8). Apart from these studies, there are surprisingly few reports on the impact
of molecular manipulation of physical defenses on plant–herbivore interactions.

Tolerance Strategies
The capacity to regrow and reproduce after herbivore attack is important for plant survival and
represents a complementary strategy to resistance. However, the molecular basis of plant tolerance
to herbivory remains poorly studied. Herbivore attack depletes carbohydrates in N. attenuata
roots and reduces the regrowth capacity of defoliated plants. Both effects are absent in JA-deficient
inverted repeat AOC plants and can be recovered by JA application (108). Solanaceae species that
display a lower JA burst upon herbivory have greater defoliation tolerance (110), suggesting that JA
signaling regulates both processes in opposite directions, most likely by antagonizing GA signaling
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(107). Furthermore, silencing the SNF1-related kinase SnRK1—which is also downregulated by

herbivory—increases carbon transport to the roots and prolongs flowering in N. attenuata; this
silencing may thus help to buffer root carbohydrate depletion and increase tolerance (152).

Progress with Genomics Approaches

Whole-genome analyses of herbivore-attacked plants have generated an unbiased view on tran-
scriptional investment in defense, associated biological functions, and quantitative contribution of
signaling pathways. Generally, insects from the same feeding guild trigger overlapping transcrip-
tome signatures, which are clearly distinct between chewing larvae and phloem-feeding insects
(86, 137). In all these experiments, the dominant biological functions activated by herbivory are
responses to biotic and abiotic stress, production and response to ROS, calcium signaling, cell
wall modification, secondary metabolism, hormone metabolism, and transcriptional regulation.
Consistent with the prominent role of the JA pathway, induction of a large majority of insect-
responsive genes depends on a functional COI1 (137, 153).
Because forward genetic screens are not easily amenable for plant–insect interactions, genetic
approaches such as quantitative trait locus mapping and genome-wide association studies hold
promise for uncovering novel molecular players. Recording of aphid behavior on 350 Arabidop-
sis accessions, for instance, has led to the identification of SLI1, a novel protein that may im-
pair phloem ingestion (80). A genome-wide association study has also been used in Arabidopsis
to determine loci that control variation in GS profiles in various environmental or developmen-
tal conditions (14, 20) or loci that are linked to the combined response to P. rapae feeding and
drought (29). In maize, quantitative trait locus mapping led to the identification of a benzoxazi-
noid O-methyl transferase whose deactivation by a transposon is associated with increased callose
accumulation and aphid resistance (114). Through a similar approach, an α-bergamotene syn-
thase involved in pollinator and herbivore natural enemy attraction was identified in N. attenuata
(198). As genomes and mapping populations become available for other plant model species, such
strategies may prove valuable for exploiting natural genetic diversity and discovering novel and
important defense genes.

HERBIVORE ADAPTATIONS TO PLANT DEFENSES

Like plant defenses, herbivore adaptations to plant defenses are diverse and fascinating. Techno-
logical advances such as next-generation sequencing and the development of RNA interference

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have begun to yield novel insights into the molecular biology of plant–insect interactions from
the insect’s perspective.
Effectors: proteins or
molecules released by
Detoxification and Neutralization of Plant Defenses
an attacker to suppress
plant defenses Herbivores possess a variety of detoxification systems that allow them to deal with host toxins. Sev-
eral genes that allow herbivores to cope with plant defenses have been identified. Silencing the
cytochrome P450 CYP6AE14 in the cotton bollworm decreases larval growth, and the effect is
more dramatic in the presence of gossypol (113). However, additional studies have not confirmed
a role of CYP6AE14 in gossypol detoxification, so this enzyme may be involved in general stress
responsiveness (84). In M. sexta, silencing CYP6B46 reduces nicotine levels in the hemolymph
and renders M. sexta caterpillars more susceptible against wolf spiders (85). Excreted nicotine
levels remain the same, however, and the exact function of CYP6B46 remains to be elucidated.
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M. sexta caterpillars with reduced β-glucosidase levels no longer deglycosylate the hydroxyger-
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anyllinalool diterpene glycoside lyciumoside IV and show developmental effects when feeding on
lyciumoside IV–containing diets (135). Herbivores may also be able to deactivate the structural
defenses of their host plants. BPH secretes NlEG1, an enzyme with cellulose-degrading endo-β-
1,4-glucanase activity, into rice plants. Silencing NlEG1 decreases the capacity of BPH to reach
the phloem with its stylet and reduces its fitness, suggesting that NlEG1 helps BPH to break down
plant cell walls (70). Together, these examples illustrate the capacity of insects to deal with plant
defenses. They also illustrate the limits of inferring function from sequence homology and call for
orthogonal biochemical experiments to distinguish between herbivore genes that are specifically
involved in detoxification and host-plant adaptation, on the one hand, and genes that are part of
general stress-coping mechanisms, on the other. Many other studies have associated biochemical
features of insect herbivores with adaptation to plant defense metabolites (95), including highly
conserved molecular changes that render sodium-potassium pumps resistant to toxic cardiac gly-
cosides (35); glycosylation of benzoxazinoids to avoid production of toxic hemiacetals (102); di-
version and detoxification of GS through a series of different enzymes (181); and deactivation,
sequestration, and reactivation of various plant toxins as a potential means of self-defense (131,
138). Testing for the importance of these traits through molecular manipulation of insect genes is
an exciting future prospect.

Plant Defense Suppression

Insect herbivores may be able to inject salivary molecules into plants to suppress defense induction.
Putative defense suppressors (so-called effectors) have been described mainly in phloem feeders.
For instance, when transiently overexpressed in Nicotiana benthamiana using Agrobacterium tumefa-
ciens, Me10 and Me23 from the potato aphid M. euphorbiae increase aphid performance, and Me10
had similar effects in tomato when delivered through Pst (5). Furthermore, stable expression of
C002, Mp1, and Mp2 from M. persicae in Arabidopsis increases aphid performance, whereas silenc-
ing C002 and Mp2 through plant-mediated RNA interference reduces it (37, 134). The molecular
mechanisms by which these putative effectors increase aphid performance are currently unclear.
Me47 from M. euphorbiae has glutathione-S-transferase activity against isothiocyanates and may
thus have a role in detoxification. However, Me47 suppresses, rather than enhances, M. euphorbiae
performance on Arabidopsis, which produces isothiocyanates during GS breakdown (76). In tomato
cells, Me10 interacts in the cytoplasm with the 14-3-3 isoform TFT7 (21). 14-3-3 are scaffolding
proteins involved in plant–pathogen interactions (99) and may thus constitute an important target
of aphid effectors.

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Much less is known about effectors from lepidopteran insects. Glucose oxidase in Helicoverpa
zea salivary glands inhibits nicotine production (121). OSs from Anticarsia gemmatalis contain a
modified inceptin that inhibits plant defenses. Strikingly, deletion of only one amino acid from in-
ceptin transforms a defense-inducing HAMP into an effector (147). Unknown proteins or peptides
from lepidopteran OS suppress defenses in Arabidopsis and N. attenuata (28, 145). Clearly, more
studies are needed to identify effectors from chewing herbivores and demonstrate their function
by gene knockout methodologies.
Apart from injecting their own effectors during feeding, insect herbivores may use additional
molecular strategies to suppress plant defenses. The capacity of the Colorado potato beetle to sup-
press plant defenses is abolished in individuals that are treated with antibiotics (26). The beetle
saliva contains numerous bacteria, and reinoculating antibiotic-treated individuals with bacterial
isolates or treating plants with flagellin from one group of isolates (Pseudomonas sp.) restores de-
fense suppression, suggesting that beetles use bacterial flagellin as an effector that triggers the SA
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pathway and, in turn, inhibits JA defenses through a crosstalk mechanism (26). JA-dependent plant
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defenses are also suppressed following egg deposition through activation of the SA pathway that
triggers similar SA/JA crosstalk, but the involved effector molecules have yet to be discovered (17).
In response to bacterial and fungal effectors, some plant genotypes have evolved numerous
intracellular immune receptors that detect effector activity and trigger hyperactivation of defenses.
These receptors that are encoded by so-called resistance genes are nucleotide binding site– and
LRR domain–containing proteins. Strikingly, very few plant nucleotide binding site LRR proteins
acting against insects have been characterized, and all are efficient against phloem-sucking insects
(Supplemental Table 1). The reason for such bias is unknown and merits further investigation.

Behavioral Adaptations
The onset and outcome of plant–herbivore interactions often depend on behavioral responses of
herbivores. Many plant defenses, for instance, do not operate primarily through intoxication, but
rather through deterrence or repellency (13, 106). The capacity of herbivores to choose the right
plants and tissues or to avoid defenses through behavioral strategies is a key adaptation that allows
them to survive within diverse plant communities that include toxic or unsuitable individuals. So
far, studies addressing the molecular underpinning of host-plant choice and herbivore behavior
are surprisingly rare. Potential chemosensory receptor proteins have been identified in different
herbivores (38), and gene-editing approaches for major herbivore pests are becoming available
(193). In a proof-of-concept study using S. littoralis, mutation of olfactory receptor coreceptor
(Orco) genes by CRISPR/Cas9 shows that antennae of Orco moths no longer respond to plant
volatiles (83). Thus, functional studies involving molecular manipulation of herbivore behavior
are becoming possible and have the potential to enhance substantially our understanding of how
insects detect and respond to plant cues.

FASCINATING BUT UNEXPLORED INTERACTIONS

Most molecular insights into plant–herbivore interactions are derived from a few model systems.
We argue that the time is ripe to leave the beaten track and to address unexplored but fascinating
examples of plant–insect interactions in model and nonmodel species (Figure 3). Below, we discuss
a few examples.

 Some specialized herbivores induce striking changes in plant leaf morphology to pro-
duce galls. These diverse and elaborate structures generally provide shelter against natural

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a b

c d e
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Figure 3
Examples of fascinating plant–insect interactions that await molecular characterization. (a) Members of the
Passiflora genus develop egg-like structures (inset) that repel oviposition by Heliconius butterflies (b) A
leaf-mining insect drills tunnels underneath epidermis of a hazelnut leaf. (c) Gall from Mikiola fagi on a
beech leaf. (d) Transverse cut of beech gall uncovers M. fagi larva (arrowhead). (e) Mutualistic interaction
between bullhorn acacia (Vachellia cornigera) and Pseudomyrmex ferruginea ants. Ants feed from extrafloral
nectar-producing structures (arrowhead) and live in hollowed-out thorns. Photo credits: (a–d) Zigmunds
Orlovskis and (e) Angel DiBilio/[Link] (image number 476197198).

enemies (166). How insect-derived cues prevent plant defense and dramatically alter plant
development is largely unknown.
 As a stunning example of a potential plant defense mechanism that targets insect behavior,
cyanogenic glycoside–containing plants of the Passiflora genus display egg-like structures
evenly dispersed on leaves, possibly to repel oviposition by the adapted herbivore Heliconius
cydno (180). The evolution, genetic basis, and exact ecological consequences of this phe-
nomenon are unknown.
 The extrafloral nectar and modified leaflet tips (Beltian bodies) of acacia trees provide
food, and their swollen thorns function as homes. Ants constantly patrol these trees to
remove unwanted insect herbivores and parasitic plants. The origin, establishment, and
stability of this type of tritrophic interaction have rarely been studied at the molecular
level.
 Insect- and plant-associated microbes strongly influence plant–insect interactions. Remark-
able examples include, for instance, larvae of the Colorado potato beetle that contain
defense-suppressing bacteria in their OSs (26) and effector proteins from insect-vectored
phytoplasma that inhibit JA defenses (167). For plant-associated microbes, high-throughput
sequencing has allowed the identification of numerous leaf-inhabiting microbes, but how
they influence plant–insect interactions is poorly studied.

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CONCLUSIONS
Two decades of intense research on molecular plant–herbivore interactions in monocot and di-
cot plant species have unveiled a significant number of conserved molecular players involved in
plant responses to insects. The rich catalog of defense genes allows for a better understanding
of (a) the intricate signaling network underlying plant defenses, (b) the genetic basis of defense
traits, and (c) mechanisms of herbivore adaptations to plant defenses. Future challenges include
filling the existing gaps in our understanding of how perception is connected to downstream steps,
how specificity is obtained with common signaling modules between herbivory and pathogene-
sis, and how insects perceive and respond to plant toxins. Leaving the beaten track and exploring
the diversity of interactions between plants and herbivorous insects will also be essential. Her-
bivores have established specific interactions with plants over evolutionary time, including both
biochemical and behavioral adaptations, which in turn have shaped the evolution of specific plant
defense regulation and expression patterns. Understanding the molecular mechanisms underly-
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ing these phenomena holds the key to appreciate fully the beauty and diversity of plant–herbivore
interactions.

SUMMARY POINTS
1. Plants detect and respond to damage-associated molecular patterns (DAMPs) and
herbivore-associated molecular patterns (HAMPs) by activating defense responses.
DAMP receptors have recently been identified, thus paving the way to understanding
the relative importance of DAMPs and HAMPs for plant–herbivore interactions.
2. Early signaling events in plant defense responses involve Ca2+ , reactive oxygen species,
and mitogen-activated protein kinase signaling. Each layer is important for plant defense
and often includes both positive and negative regulators. Species-specific topologies of
early defense signaling networks are emerging and require further investigation.
3. The jasmonate pathway is an essential component of defense against chewing herbivores.
In addition, several other small molecules, including growth and stress hormones as well
as volatile and nonvolatile secondary metabolites can regulate plant defenses. Plants thus
have a substantial arsenal of conserved and specific signaling molecules at their disposal
to specifically regulate defenses against herbivores.
4. Transcription factors, including MYCs and WRKYs, play a crucial role in regulating
defense signaling and activating the transcription of defense genes. Recent work shows
how transcription factors mechanistically link early defense signaling, hormone signal-
ing, and defense deployment.
5. Plants display strong spatiotemporal variation in the expression of defense metabolites
and proteins as well as physical barriers and tolerance traits. Transcriptional regulation
of the underlying defense genes by developmental hormones and secondary metabolite
transport are emerging as mechanisms by which defenses are regulated in space and time.
6. Insects counter plant defenses through behavioral and biochemical adaptations, in-
cluding the production of defense-suppressing effectors. The (simultaneous) molecu-
lar manipulation of plant defenses and insect counterdefenses allows for unprecedented
insights into plant–herbivore interactions and connects plant defense and herbivore
defense/immunity networks.

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7. The current standard model of molecular interactions between plants and insect her-
bivores is derived from a handful of model species. Expanding molecular research to
include more diverse and fascinating interactions will be essential to complement our
current knowledge.

DISCLOSURE STATEMENT
The authors are not aware of any affiliations, memberships, funding, or financial holdings that
might be perceived as affecting the objectivity of this review.
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ACKNOWLEDGMENTS
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The Swiss National Science Foundation (grants 160786 and 155781 to M.E. and 31003A_169278
to P.R.), the University of Bern, and the University of Lausanne supported this work. We apologize
to researchers whose work was not mentioned or cited in this review owing to space limitations.

LITERATURE CITED
1. Acevedo FE, Rivera-Vega LJ, Chung SH, Ray S, Felton GW. 2015. Cues from chewing insects—the
intersection of DAMPs, HAMPs, MAMPs and effectors. Curr. Opin. Plant Biol. 26:80–86
2. Adebesin F, Widhalm JR, Boachon B, Lefèvre F, Pierman B, et al. 2017. Emission of volatile organic
compounds from petunia flowers is facilitated by an ABC transporter. Science 356:1386–88
3. Ahmad S, Veyrat N, Gordon-Weeks R, Zhang Y, Martin J, et al. 2011. Benzoxazinoid metabolites reg-
ulate innate immunity against aphids and fungi in maize. Plant Physiol. 157:317–27
4. Ashton AR. 2011. Guanylyl cyclase activity in plants? PNAS 108:E96
5. Atamian HS, Chaudhary R, Cin VD, Bao E, Girke T, Kaloshian I. 2013. In planta expression or delivery
of potato aphid Macrosiphum euphorbiae effectors Me10 and Me23 enhances aphid fecundity. Mol. Plant-
Microbe Interact. 26:67–74
6. Barth C, Jander G. 2006. Arabidopsis myrosinases TGG1 and TGG2 have redundant function in glu-
cosinolate breakdown and insect defense. Plant J. 46:549–62
7. Barton KE, Boege K. 2017. Future directions in the ontogeny of plant defence: understanding the evo-
lutionary causes and consequences. Ecol. Lett. 20:403–11
8. Blanc C, Coluccia F, L’Haridon F, Torres M, Ortiz-Berrocal M, et al. 2018. The cuticle mutant eca2
modifies plant defense responses to biotrophic and necrotrophic pathogens and herbivory insects. Mol.
Plant-Microbe Interact. 31:344–55
9. Bleeker PM, Mirabella R, Diergaarde PJ, Vandoorn A, Tissier A, et al. 2012. Improved herbivore re-
sistance in cultivated tomato with the sesquiterpene biosynthetic pathway from a wild relative. PNAS
109:20124–29
10. Block A, Christensen SA, Hunter CT, Alborn HT. 2018. Herbivore-derived fatty-acid amides elicit
reactive oxygen species burst in plants. J. Exp. Bot. 69:1235–45
11. Bodenhausen N, Reymond P. 2007. Signaling pathways controlling induced resistance to insect herbi-
vores in Arabidopsis. Mol. Plant-Microbe Interact. 20:1406–20
12. Bonaventure G, Gfeller A, Proebsting WM, Hörtensteiner S, Chételat A, et al. 2007. A gain-of-function
allele of TPC1 activates oxylipin biogenesis after leaf wounding in Arabidopsis. Plant J. 49:889–98
13. Bont Z, Arce C, Huber M, Huang W, Mestrot A, et al. 2017. A herbivore tag-and-trace system reveals
contact- and density-dependent repellence of a root toxin. J. Chem. Ecol. 43:295–306
14. Brachi B, Meyer CG, Villoutreix R, Platt A, Morton TC, et al. 2015. Coselected genes determine adaptive
variation in herbivore resistance throughout the native range of Arabidopsis thaliana. PNAS 112:4032–37

548 Erb • Reymond

PP70CH19_Reymond [Link] March 26, 2019 13:29

15. Bricchi I, Leitner M, Foti M, Mithöfer A, Boland W, Maffei ME. 2010. Robotic mechanical wounding
(MecWorm) versus herbivore-induced responses: early signaling and volatile emission in Lima bean
(Phaseolus lunatus L.). Planta 232:719–29
16. Bruce TJA, Aradottir GI, Smart LE, Martin JL, Caulfield JC, et al. 2015. The first crop plant genetically
engineered to release an insect pheromone for defence. Sci. Rep. 5:11183
17. Bruessow F, Gouhier-Darimont C, Buchala A, Metraux J-P, Reymond P. 2010. Insect eggs suppress
plant defence against chewing herbivores. Plant J. 62:876–85
18. Brütting C, Schäfer M, Vanková R, Gase K, Baldwin IT, Meldau S. 2017. Changes in cytokinins 18. Demonstrates that
are sufficient to alter developmental patterns of defense metabolites in Nicotiana attenuata. Plant cytokinins regulate
J. 89:15–30 developmental variation
19. Brutus A, Sicilia F, Macone A, Cervone F, De Lorenzo G. 2010. A domain swap approach reveals a role in defense expression.
of the plant wall-associated kinase 1 (WAK1) as a receptor of oligogalacturonides. PNAS 107:9452–57
20. Chan EKF, Rowe HC, Corwin JA, Joseph B, Kliebenstein DJ. 2011. Combining genome-wide associ-
ation mapping and transcriptional networks to identify novel genes controlling glucosinolates in Ara-
Annu. Rev. Plant Biol. 2019.70:527-557. Downloaded from [Link]

bidopsis thaliana. PLOS Biol. 8:e1001125

Access provided by University of Stellenbosch on 03/07/22. For personal use only.

21. Chaudhary R, Peng H-C, He J, MacWilliams J, Teixeira M, et al. 2018. Aphid effector Me10 interacts
with tomato TFT7, a 14-3-3 isoform involved in aphid resistance. New Phytol. 221:1518–28
22. Chauvin A, Caldelari D, Wolfender J-L, Farmer EE. 2013. Four 13-lipoxygenases contribute to rapid
jasmonate synthesis in wounded Arabidopsis thaliana leaves: a role for lipoxygenase 6 in responses to
long-distance wound signals. New Phytol. 197:566–75
23. Chen H, Wilkerson CG, Kuchar JA, Phinney BS, Howe GA. 2005. Jasmonate-inducible plant enzymes
degrade essential amino acids in the herbivore midgut. PNAS 102:19237–42 25. Identifies DORN1
24. Chini A, Monte I, Zamarreño AM, Hamberg M, Lassueur S, et al. 2018. An OPR3-independent pathway as the receptor for the
uses 4,5-didehydrojasmonate for jasmonate synthesis. Nat. Chem. Biol. 14:171–78 extracellular DAMP
signal ATP.
25. Choi J, Tanaka K, Cao Y, Qi Y, Qiu J, et al. 2014. Identification of a plant receptor for extracellular
ATP. Science 343:290–94
26. Chung SH, Rosa C, Scully ED, Peiffer M, Tooker JF, et al. 2013. Herbivore exploits orally se- 26. Shows that bacteria
creted bacteria to suppress plant defenses. PNAS 110:15728–33 contained in insect OSs
27. Clay NK, Adio AM, Denoux C, Jander G, Ausubel FM. 2009. Glucosinolate metabolites required for an can suppress plant
Arabidopsis innate immune response. Science 323:95–101 defenses.
28. Consales F, Schweizer F, Erb M, Gouhier-Darimont C, Bodenhausen N, et al. 2012. Insect oral secre-
tions suppress wound-induced responses in Arabidopsis. J. Exp. Bot. 63:727–37
29. Davila Olivas NH, Kruijer W, Gort G, Wijnen CL, van Loon JJA, Dicke M. 2017. Genome-wide associ-
ation analysis reveals distinct genetic architectures for single and combined stress responses in Arabidopsis
thaliana. New Phytol. 213:838–51
30. De Moraes CM, Mescher MC, Tumlinson JH. 2001. Caterpillar-induced nocturnal plant volatiles repel
conspecific females. Nature 410:577–80
31. de Vos M, Jander G. 2009. Myzus persicae (green peach aphid) salivary components induce defence re-
sponses in Arabidopsis thaliana. Plant Cell Environ. 32:1548–60
32. Degenhardt J, Hiltpold I, Köllner TG, Frey M, Gierl A, et al. 2009. Restoring a maize root signal that
attracts insect-killing nematodes to control a major pest. PNAS 106:13213–18
33. Diezel C, von Dahl CC, Gaquerel E, Baldwin IT. 2009. Different lepidopteran elicitors account for
cross-talk in herbivory-induced phytohormone signaling. Plant Physiol. 150:1576–86
34. Dinh ST, Baldwin IT, Galis I. 2013. The HERBIVORE ELICITOR-REGULATED1 gene enhances ab-
scisic acid levels and defenses against herbivores in Nicotiana attenuata plants. Plant Physiol. 162:2106–24
35. Dobler S, Dalla S, Wagschal V, Agrawal AA. 2012. Community-wide convergent evolution in insect
adaptation to toxic cardenolides by substitutions in the Na,K-ATPase. PNAS 109:13040–45
36. Du M, Zhao J, Tzeng DTW, Liu Y, Deng L, et al. 2017. MYC2 orchestrates a hierarchical transcriptional
cascade that regulates jasmonate-mediated plant immunity in tomato. Plant Cell 29:1883–906
37. Elzinga DA, de Vos M, Jander G. 2014. Suppression of plant defenses by a Myzus persicae (green peach
aphid) salivary effector protein. Mol. Plant-Microbe Interact. 27:747–56

[Link] • Plant–Insect Interactions 549

PP70CH19_Reymond [Link] March 26, 2019 13:29

38. Engsontia P, Sangket U, Chotigeat W, Satasook C. 2014. Molecular evolution of the odorant and gus-
tatory receptor genes in lepidopteran insects: implications for their adaptation and speciation. J. Mol.
Evol. 79:21–39
39. Erb M. 2018. Volatiles as inducers and suppressors of plant defense and immunity-origins, specificity,
perception and signaling. Curr. Opin. Plant Biol. 44:117–21
40. Erb M, Veyrat N, Robert CAM, Xu H, Frey M, et al. 2015. Indole is an essential herbivore-induced
volatile priming signal in maize. Nat. Commun. 6:6273
41. Farmer EE. 2014. Leaf Defence. Oxford, UK: Oxford Univ. Press
42. Feng W, Kita D, Peaucelle A, Cartwright HN, Doan V, et al. 2018. The FERONIA receptor kinase
maintains cell-wall integrity during salt stress through Ca2+ signaling. Curr. Biol. 28:666–75.e5
43. Fernández-Calvo P, Chini A, Fernández-Barbero G, Chico JM, Gimenez-Ibanez S, et al. 2011. The
Arabidopsis bHLH transcription factors MYC3 and MYC4 are targets of JAZ repressors and act additively
with MYC2 in the activation of jasmonate responses. Plant Cell 23:701–15
44. Fragoso V, Rothe E, Baldwin IT, Kim S-G. 2014. Root jasmonic acid synthesis and perception regulate
Annu. Rev. Plant Biol. 2019.70:527-557. Downloaded from [Link]

folivore-induced shoot metabolites and increase Nicotiana attenuata resistance. New Phytol. 202:1335–45
Access provided by University of Stellenbosch on 03/07/22. For personal use only.

45. Gigolashvili T, Berger B, Flügge U-I. 2009. Specific and coordinated control of indolic and aliphatic
glucosinolate biosynthesis by R2R3-MYB transcription factors in Arabidopsis thaliana. Phytochem. Rev.
8:3–13
46. Gilardoni PA, Hettenhausen C, Baldwin IT, Bonaventure G. 2011. Nicotiana attenuata LECTIN
RECEPTOR KINASE1 suppresses the insect-mediated inhibition of induced defense responses during
Manduca sexta herbivory. Plant Cell 23:3512–32
47. Glauser G, Dubugnon L, Mousavi SAR, Rudaz S, Wolfender J-L, Farmer EE. 2009. Velocity estimates
for signal propagation leading to systemic jasmonic acid accumulation in wounded Arabidopsis. J. Biol.
Chem. 284:34506–13
48. Gonneau M, Desprez T, Martin M, Doblas VG, Bacete L, et al. 2018. Receptor kinase THESEUS1 is
a rapid alkalinization factor 34 receptor in Arabidopsis. Curr. Biol. 28:2452–58.e4
49. Gonzales-Vigil E, Bianchetti CM, Phillips GN, Howe GA. 2011. Adaptive evolution of threonine deam-
inase in plant defense against insect herbivores. PNAS 108:5897–902
50. Goodspeed D, Chehab EW, Min-Venditti A, Braam J, Covington MF. 2012. Arabidopsis synchronizes
jasmonate-mediated defense with insect circadian behavior. PNAS 109:4674–77
51. Gouhier-Darimont C, Schmiesing A, Bonnet C, Lassueur S, Reymond P. 2013. Signalling of Arabidopsis
thaliana response to Pieris brassicae eggs shares similarities with PAMP-triggered immunity. J. Exp. Bot.
64:665–74
52. Guo J, Xu C, Wu D, Zhao Y, Qiu Y, et al. 2018. Bph6 encodes an exocyst-localized protein and confers
broad resistance to planthoppers in rice. Nat. Genet. 50:297–306
53. Halitschke R, Stenberg JA, Kessler D, Kessler A, Baldwin IT. 2008. Shared signals—“alarm calls” from
plants increase apparency to herbivores and their enemies in nature. Ecol. Lett. 11:24–34
54. Handrick V, Robert CAM, Ahern KR, Zhou S, Machado RAR, et al. 2016. Biosynthesis of 8-O-
methylated benzoxazinoid defense compounds in maize. Plant Cell 28:1682–700
55. Haruta M, Sabat G, Stecker K, Minkoff BB, Sussman MR. 2014. A peptide hormone and its receptor
protein kinase regulate plant cell expansion. Science 343:408–11
56. Hettenhausen C, Schuman MC, Wu J. 2015. MAPK signaling: a key element in plant defense response
to insects. Insect Sci. 22:157–64
57. Hématy K, Sado P-E, Van Tuinen A, Rochange S, Desnos T, et al. 2007. A receptor-like kinase mediates
the response of Arabidopsis cells to the inhibition of cellulose synthesis. Curr. Biol. 17:922–31
58. Hildreth SB, Gehman EA, Yang H, Lu R-H, Ritesh KC, et al. 2011. Tobacco nicotine uptake permease
(NUP1) affects alkaloid metabolism. PNAS 108:18179–84
59. Hilleary R, Gilroy S. 2018. Systemic signaling in response to wounding and pathogens. Curr. Opin. Plant
Biol. 43:57–62
60. Hillwig MS, Chiozza M, Casteel CL, Lau ST, Hohenstein J, et al. 2016. Abscisic acid deficiency increases
defence responses against Myzus persicae in Arabidopsis. Mol. Plant Pathol. 17:225–35

550 Erb • Reymond

PP70CH19_Reymond [Link] March 26, 2019 13:29

61. Hong G-J, Xue X-Y, Mao Y-B, Wang L-J, Chen X-Y. 2012. Arabidopsis MYC2 interacts with DELLA
proteins in regulating sesquiterpene synthase gene expression. Plant Cell 24:2635–48
62. Howe GA, Jander G. 2008. Plant immunity to insect herbivores. Annu. Rev. Plant Biol. 59:41–66
63. Howe GA, Major IT, Koo AJ. 2018. Modularity in jasmonate signaling for multistress resilience. Annu.
Rev. Plant Biol. 69:387–415
64. Hu L, Ye M, Kuai P, Ye M, Erb M, Lou Y. 2018. OsLRR-RLK1, an early responsive leucine-rich repeat
receptor-like kinase, initiates rice defense responses against a chewing herbivore. New Phytol. 219:1097–
11
65. Hu L, Ye M, Li R, Zhang T, Zhou G, et al. 2015. The rice transcription factor WRKY53 suppresses
herbivore-induced defenses by acting as a negative feedback modulator of mitogen-activated protein
kinase activity. Plant Physiol. 169:2907–21
66. Hu P, Zhou W, Cheng Z, Fan M, Wang L, Xie D. 2013. JAV1 controls jasmonate-regulated plant
defense. Mol. Cell 50:504–15
67. Huber M, Epping J, Schulze Gronover C, Fricke J, Aziz Z, et al. 2016. A latex metabolite benefits plant
Annu. Rev. Plant Biol. 2019.70:527-557. Downloaded from [Link]

fitness under root herbivore attack. PLOS Biol. 14:e1002332

Access provided by University of Stellenbosch on 03/07/22. For personal use only.

68. Huffaker A, Pearce G, Veyrat N, Erb M, Turlings TCJ, et al. 2013. Plant elicitor peptides are conserved
signals regulating direct and indirect antiherbivore defense. PNAS 110:5707–12
69. Huffaker A, Ryan CA. 2007. Endogenous peptide defense signals in Arabidopsis differentially amplify
signaling for the innate immune response. PNAS 104:10732–36
70. Ji R, Ye W, Chen H, Zeng J, Li H, et al. 2017. A salivary endo-β-1,4-glucanase acts as an effector that
enables the brown planthopper to feed on rice. Plant Physiol. 173:1920–32
71. Johnson R, Narvaez J, An G, Ryan C. 1989. Expression of proteinase inhibitors I and II in transgenic
tobacco plants: effects on natural defense against Manduca sexta larvae. PNAS 86:9871–75
72. Kandoth PK, Ranf S, Pancholi SS, Jayanty S, Walla MD, et al. 2007. Tomato MAPKs LeMPK1,
LeMPK2, and LeMPK3 function in the systemin-mediated defense response against herbivorous in-
sects. PNAS 104:12205–10
73. Kang J-H, Wang L, Giri A, Baldwin IT. 2006. Silencing threonine deaminase and JAR4 in Nicotiana
attenuata impairs jasmonic acid-isoleucine-mediated defenses against Manduca sexta. Plant Cell 18:3303–
20
74. Katz E, Nisani S, Yadav BS, Woldemariam MG, Shai B, et al. 2015. The glucosinolate breakdown 74. Provides a mode of
product indole-3-carbinol acts as an auxin antagonist in roots of Arabidopsis thaliana. Plant J. action by which
82:547–55 defensive secondary
75. Kessler A, Baldwin IT. 2002. Plant responses to insect herbivory: the emerging molecular analysis. Annu. metabolites act as
Rev. Plant Biol. 53:299–328 within-plant signaling
76. Kettles GJ, Kaloshian I. 2016. The potato aphid salivary effector Me47 is a glutathione-S-transferase molecules.
involved in modifying plant responses to aphid infestation. Front. Plant Sci. 7:1142
77. Kim S-G, Yon F, Gaquerel E, Gulati J, Baldwin IT. 2011. Tissue specific diurnal rhythms of metabolites
and their regulation during herbivore attack in a native tobacco, Nicotiana attenuata. PLOS ONE 6:e26214
78. Kivimäki M, Kärkkäinen K, Gaudeul M, Løe G, Agren J. 2007. Gene, phenotype and function:
GLABROUS1 and resistance to herbivory in natural populations of Arabidopsis lyrata. Mol. Ecol. 16:453–
62
79. Klauser D, Desurmont GA, Glauser G, Vallat A, Flury P, et al. 2015. The Arabidopsis Pep-PEPR system
is induced by herbivore feeding and contributes to JA-mediated plant defence against herbivory. J. Exp.
Bot. 66:5327–36
80. Kloth KJ, Busscher-Lange J, Wiegers GL, Kruijer W, Buijs G, et al. 2017. SIEVE ELEMENT-LINING
CHAPERONE1 restricts aphid feeding on Arabidopsis during heat stress. Plant Cell 29:2450–64
81. Kohorn BD, Johansen S, Shishido A, Todorova T, Martinez R, et al. 2009. Pectin activation of MAP
kinase and gene expression is WAK2 dependent. Plant J. 60:974–82
82. Koo AJK, Gao X, Jones AD, Howe GA. 2009. A rapid wound signal activates the systemic synthesis of
bioactive jasmonates in Arabidopsis. Plant J. 59:974–86
83. Koutroumpa FA, Monsempes C, François M-C, de Cian A, Royer C, et al. 2016. Heritable genome
editing with CRISPR/Cas9 induces anosmia in a crop pest moth. Sci. Rep. 6:29620

[Link] • Plant–Insect Interactions 551

PP70CH19_Reymond [Link] March 26, 2019 13:29

84. Krempl C, Heidel-Fischer HM, Jiménez-Alemán GH, Reichelt M, Menezes RC, et al. 2016. Gossypol
toxicity and detoxification in Helicoverpa armigera and Heliothis virescens. Insect Biochem. Mol. Biol. 78:69–
77
85. Kumar P, Pandit SS, Steppuhn A, Baldwin IT. 2014. Natural history-driven, plant-mediated RNAi-
based study reveals CYP6B46’s role in a nicotine-mediated antipredator herbivore defense. PNAS
111:1245–52
86. Kusnierczyk A, Winge P, Jørstad TS, Troczyńska J, Rossiter JT, Bones AM. 2008. Towards global un-
derstanding of plant defence against aphids—timing and dynamics of early Arabidopsis defence responses
to cabbage aphid (Brevicoryne brassicae) attack. Plant Cell Environ. 31:1097–115
87. Lan Z, Krosse S, Achard P, van Dam NM, Bede JC. 2014. DELLA proteins modulate Arabidopsis defences
induced in response to caterpillar herbivory. J. Exp. Bot. 65:571–83
88. Lenglet A, Jaślan D, Toyota M, Mueller M, Müller T, et al. 2017. Control of basal jasmonate signalling
and defence through modulation of intracellular cation flux capacity. New Phytol. 216:1161–69
89. Li D, Heiling S, Baldwin IT, Gaquerel E. 2016. Illuminating a plant’s tissue-specific metabolic diversity
Annu. Rev. Plant Biol. 2019.70:527-557. Downloaded from [Link]

using computational metabolomics and information theory. PNAS 113:E7610–18

Access provided by University of Stellenbosch on 03/07/22. For personal use only.

90. Li Q, Xie Q-G, Smith-Becker J, Navarre DA, Kaloshian I. 2006. Mi-1-mediated aphid resistance in-
volves salicylic acid and mitogen-activated protein kinase signaling cascades. Mol. Plant-Microbe Interact.
19:655–64
91. Li R, Llorca LC, Schuman MC, Wang Y, Wang L, et al. 2018. ZEITLUPE in the roots of wild tobacco
regulates jasmonate-mediated nicotine biosynthesis and resistance to a generalist herbivore. Plant Physiol.
177:833–46
92. Li R, Wang M, Wang Y, Schuman MC, Weinhold A, et al. 2017. Flower-specific jasmonate signaling
regulates constitutive floral defenses in wild tobacco. PNAS 114:E7205–14
93. Shows how a WRKY 93. Li R, Zhang J, Li J, Zhou G, Wang Q, et al. 2015. Prioritizing plant defence over growth through
factor enhances JA WRKY regulation facilitates infestation by non-target herbivores. eLife 4:e04805
signaling and suppresses 94. Li S, Wang H, Li F, Chen Z, Li X, et al. 2015. The maize transcription factor EREB58 mediates the
GA signaling, thereby jasmonate-induced production of sesquiterpene volatiles. Plant J. 84:296–308
modulating resistance
95. Li X, Schuler MA, Berenbaum MR. 2007. Molecular mechanisms of metabolic resistance to synthetic
against herbivores.
and natural xenobiotics. Annu. Rev. Entomol. 52:231–53
96. Lin W, Tang W, Anderson C, Yang Z. 2018. FERONIA’s sensing of cell wall pectin activates ROP
GTPase signaling in Arabidopsis. bioRxiv 269647. [Link]
97. Liu Y, Wu H, Chen H, Liu Y, He J, et al. 2015. A gene cluster encoding lectin receptor kinases confers
broad-spectrum and durable insect resistance in rice. Nat. Biotechnol. 33:301–5
98. Louis J, Peiffer M, Ray S, Luthe DS, Felton GW. 2013. Host-specific salivary elicitor(s) of European
corn borer induce defenses in tomato and maize. New Phytol. 199:66–73
99. Lozano-Durán R, Robatzek S. 2015. 14-3-3 proteins in plant-pathogen interactions. Mol. Plant-Microbe
Interact. 28:511–18
100. Lu J, Li J, Ju H, Liu X, Erb M, et al. 2014. Contrasting effects of ethylene biosynthesis on induced plant
resistance against a chewing and a piercing-sucking herbivore in rice. Mol. Plant. 7:1670–82
101. Lu J, Robert CAM, Riemann M, Cosme M, Mène-Saffrané L, et al. 2015. Induced jasmonate signaling
leads to contrasting effects on root damage and herbivore performance. Plant Physiol. 167:1100–16
102. Maag D, Dalvit C, Thevenet D, Köhler A, Wouters FC, et al. 2014. 3-β-D-glucopyranosyl-6-methoxy-
2-benzoxazolinone (MBOA-N-Glc) is an insect detoxification product of maize 1,4-benzoxazin-3-ones.
Phytochemistry 102:97–105
103. Maag D, Erb M, Bernal JS, Wolfender J-L, Turlings TCJ, Glauser G. 2015. Maize domestication and
anti-herbivore defences: leaf-specific dynamics during early ontogeny of maize and its wild ancestors.
PLOS ONE 10:e0135722
104. Maag D, Erb M, Köllner TG, Gershenzon J. 2015. Defensive weapons and defense signals in plants:
some metabolites serve both roles. BioEssays 37:167–74
105. Maag D, Köhler A, Robert CAM, Frey M, Wolfender J-L, et al. 2016. Highly localized and persistent
induction of Bx1-dependent herbivore resistance factors in maize. Plant J. 88:976–91

552 Erb • Reymond

PP70CH19_Reymond [Link] March 26, 2019 13:29

106. Machado RA, McClure M, Hervé MR, Baldwin IT, Erb M. 2016. Benefits of jasmonate-dependent
defenses against vertebrate herbivores in nature. eLife 5:e13720
107. Machado RAR, Baldwin IT, Erb M. 2017. Herbivory-induced jasmonates constrain plant sugar accu-
mulation and growth by antagonizing gibberellin signaling and not by promoting secondary metabolite
production. New Phytol. 215:803–12
108. Machado RAR, Ferrieri AP, Robert CAM, Glauser G, Kallenbach M, et al. 2013. Leaf-herbivore attack
reduces carbon reserves and regrowth from the roots via jasmonate and auxin signaling. New Phytol.
200:1234–46
109. Machado RAR, Robert CAM, Arce CCM, Ferrieri AP, Xu S, et al. 2016. Auxin is rapidly induced by her-
bivore attack and regulates a subset of systemic, jasmonate-dependent defenses. Plant Physiol. 172:521–32
110. Machado RAR, Zhou W, Ferrieri AP, Arce CCM, Baldwin IT, et al. 2017. Species-specific regulation of
herbivory-induced defoliation tolerance is associated with jasmonate inducibility. Ecol. Evol. 7:3703–12
111. Maffei ME, Bossi S, Spiteller D, Mithoefer A, Boland W. 2004. Effects of feeding Spodoptera littoralis on
lima bean leaves. I. Membrane potentials, intracellular calcium variations, oral secretions, and regurgitate
Annu. Rev. Plant Biol. 2019.70:527-557. Downloaded from [Link]

components. Plant Physiol. 134:1752–62

Access provided by University of Stellenbosch on 03/07/22. For personal use only.

112. Major IT, Yoshida Y, Campos ML, Kapali G, Xin X-F, et al. 2017. Regulation of growth-defense balance
by the JASMONATE ZIM-DOMAIN ( JAZ)-MYC transcriptional module. New Phytol. 215:1533–47
113. Mao Y-B, Cai W-J, Wang J-W, Hong G-J, Tao X-Y, et al. 2007. Silencing a cotton bollworm P450
monooxygenase gene by plant-mediated RNAi impairs larval tolerance of gossypol. Nat. Biotechnol.
25:1307–13
114. Meihls LN, Handrick V, Glauser G, Barbier H, Kaur H, et al. 2013. Natural variation in maize aphid re-
sistance is associated with 2,4-dihydroxy-7-methoxy-1,4-benzoxazin-3-one glucoside methyltransferase
activity. Plant Cell 25:2341–55
115. Meldau S, Erb M, Baldwin IT. 2012. Defence on demand: mechanisms behind optimal defence patterns.
Ann. Bot. 110:1503–14
116. Miller G, Schlauch K, Tam R, Cortes D, Torres MA, et al. 2009. The plant NADPH oxidase RBOHD
mediates rapid systemic signaling in response to diverse stimuli. Sci. Signal. 2:ra45
117. Mirabella R, Rauwerda H, Struys EA, Jakobs C, Triantaphylidès C, et al. 2008. The Arabidopsis her1
mutant implicates GABA in E-2-hexenal responsiveness. Plant J. 53:197–213
118. Monte I, Ishida S, Zamarreño AM, Hamberg M, Franco-Zorrilla JM, et al. 2018. Ligand-receptor co-
evolution shaped the jasmonate pathway in land plants. Nat. Chem. Biol. 14:480–88
119. Morita M, Shitan N, Sawada K, Van Montagu MCE, Inzé D, et al. 2009. Vacuolar transport of nicotine
is mediated by a multidrug and toxic compound extrusion (MATE) transporter in Nicotiana tabacum.
PNAS 106:2447–52
120. Mousavi SAR, Chauvin A, Pascaud F, Kellenberger S, Farmer EE. 2013. GLUTAMATE 120. Identifies
RECEPTOR-LIKE genes mediate leaf-to-leaf wound signalling. Nature 500:422–26 molecular components
121. Musser RO, Hum-Musser SM, Eichenseer H, Peiffer M, Ervin G, et al. 2002. Herbivory: caterpillar required for generation
saliva beats plant defences. Nature 416:599–600 of long-distance
electrical signals in
122. Müller R, de Vos M, Sun JY, Sønderby IE, Halkier BA, et al. 2010. Differential effects of indole and
response to wounding.
aliphatic glucosinolates on lepidopteran herbivores. J. Chem. Ecol. 36:905–13
123. Nguyen CT, Kurenda A, Stolz S, Chételat A, Farmer EE. 2018. Identification of cell populations nec-
essary for leaf-to-leaf electrical signaling in a wounded plant. PNAS 115:10178–83
124. Nour-Eldin HH, Andersen TG, Burow M, Madsen SR, Jørgensen ME, et al. 2012. NRT/PTR trans-
porters are essential for translocation of glucosinolate defence compounds to seeds. Nature 488:531–34
125. Onkokesung N, Reichelt M, van Doorn A, Schuurink RC, Dicke M. 2016. Differential costs of two dis-
tinct resistance mechanisms induced by different herbivore species in Arabidopsis. Plant Physiol. 170:891–
906
126. Onkokesung N, Reichelt M, van Doorn A, Schuurink RC, van Loon JJA, Dicke M. 2014. Modulation of
flavonoid metabolites in Arabidopsis thaliana through overexpression of the MYB75 transcription factor:
role of kaempferol-3,7-dirhamnoside in resistance to the specialist insect herbivore Pieris brassicae. J. Exp.
Bot. 65:2203–17

[Link] • Plant–Insect Interactions 553

PP70CH19_Reymond [Link] March 26, 2019 13:29

127. Orozco-Cardenas ML, McGurl B, Ryan CA. 1993. Expression of an antisense prosystemin gene in
tomato plants reduces resistance toward Manduca sexta larvae. PNAS 90:8273–76
128. Pandey SP, Shahi P, Gase K, Baldwin IT. 2008. Herbivory-induced changes in the small-RNA tran-
scriptome and phytohormone signaling in Nicotiana attenuata. PNAS 105:4559–64
129. Payne RME, Xu D, Foureau E, Teto Carqueijeiro MIS, Oudin A, et al. 2017. An NPF transporter exports
a central monoterpene indole alkaloid intermediate from the vacuole. Nat. Plants 3:16208
130. Pechan T, Cohen A, Williams WP, Luthe DS. 2002. Insect feeding mobilizes a unique plant defense
protease that disrupts the peritrophic matrix of caterpillars. PNAS 99:13319–23
131. Petschenka G, Agrawal AA. 2016. How herbivores coopt plant defenses: natural selection, specialization,
and sequestration. Curr. Opin. Insect Sci. 14:17–24
132. Pfalz M, Vogel H, Kroymann J. 2009. The gene controlling the indole glucosinolate modifier1 quan-
titative trait locus alters indole glucosinolate structures and aphid resistance in Arabidopsis. Plant Cell
21:985–99
133. Pieterse CMJ, Van der Does D, Zamioudis C, Leon-Reyes A, Van Wees SCM. 2012. Hormonal modu-
Annu. Rev. Plant Biol. 2019.70:527-557. Downloaded from [Link]

lation of plant immunity. Annu. Rev. Cell Dev. Biol. 28:489–521

Access provided by University of Stellenbosch on 03/07/22. For personal use only.

134. Pitino M, Hogenhout SA. 2013. Aphid protein effectors promote aphid colonization in a plant species-
specific manner. Mol. Plant-Microbe Interact. 26:130–39
135. Poreddy S, Mitra S, Schöttner M, Chandran J, Schneider B, et al. 2015. Detoxification of hostplant’s
chemical defence rather than its anti-predator co-option drives β-glucosidase-mediated lepidopteran
counteradaptation. Nat. Commun. 6:8525
136. Qi Z, Verma R, Gehring C, Yamaguchi Y, Zhao Y, et al. 2010. Ca2+ signaling by plant Arabidopsis thaliana
Pep peptides depends on AtPepR1, a receptor with guanylyl cyclase activity, and cGMP-activated Ca2+
channels. PNAS 107:21193–98
137. Reymond P, Bodenhausen N, Van Poecke RMP, Krishnamurthy V, Dicke M, Farmer EE. 2004. A con-
served transcript pattern in response to a specialist and a generalist herbivore. Plant Cell 16:3132–47
138. Robert CA, Zhang X, Machado RA, Schirmer S, Lori M, et al. 2017. Sequestration and activation of
plant toxins protect the western corn rootworm from enemies at multiple trophic levels. eLife 6:e29307
139. Robert CAM, Erb M, Hiltpold I, Hibbard BE, Gaillard MDP, et al. 2013. Genetically engineered maize
plants reveal distinct costs and benefits of constitutive volatile emissions in the field. Plant Biotechnol. J.
11:628–39
140. Sasaki-Sekimoto Y, Jikumaru Y, Obayashi T, Saito H, Masuda S, et al. 2013. Basic helix-loop-helix tran-
scription factors JASMONATE-ASSOCIATED MYC2-LIKE1 ( JAM1), JAM2, and JAM3 are negative
regulators of jasmonate responses in Arabidopsis. Plant Physiol. 163:291–304
141. Scala A, Mirabella R, Goedhart J, de Vries M, Haring MA, Schuurink RC. 2017. Forward genetic screens
identify a role for the mitochondrial HER2 in E-2-hexenal responsiveness. Plant Mol. Biol. 95:399–409
142. Schäfer M, Canales IDM, Brütting C, Baldwin IT, Meldau S. 2015. Cytokinin concentrations and
CHASE-DOMAIN CONTAINING HIS KINASE 2 (NaCHK2)- and NaCHK3-mediated perception
modulate herbivory-induced defense signaling and defenses in Nicotiana attenuata. New Phytol. 207:645–
58
143. Schäfer M, Fischer C, Meldau S, Seebald E, Oelmüller R, Baldwin IT. 2011. Lipase activity in insect
oral secretions mediates defense responses in Arabidopsis. Plant Physiol. 156:1520–34
144. Schilmiller AL, Koo AJK, Howe GA. 2007. Functional diversification of acyl-coenzyme A oxidases in
jasmonic acid biosynthesis and action. Plant Physiol. 143:812–24
145. Schittko U, Hermsmeier D, Baldwin IT. 2001. Molecular interactions between the specialist herbivore
Manduca sexta (Lepidoptera, Sphingidae) and its natural host Nicotiana attenuata. II. Accumulation of
147. Illustrates how a plant mRNAs in response to insect-derived cues. Plant Physiol. 125:701–10
modified HAMP 146. Schmelz EA, Carroll MJ, LeClere S, Phipps SM, Meredith J, et al. 2006. Fragments of ATP synthase
functions as an effector mediate plant perception of insect attack. PNAS 103:8894–99
in an adapted insect 147. Schmelz EA, Huffaker A, Carroll MJ, Alborn HT, Ali JG, Teal PEA. 2012. An amino acid sub-
herbivore. stitution inhibits specialist herbivore production of an antagonist effector and recovers insect-
induced plant defenses. Plant Physiol. 160:1468–78

554 Erb • Reymond

PP70CH19_Reymond [Link] March 26, 2019 13:29

148. Schnee C, Köllner TG, Held M, Turlings TCJ, Gershenzon J, Degenhardt J. 2006. The products of a
single maize sesquiterpene synthase form a volatile defense signal that attracts natural enemies of maize
herbivores. PNAS 103:1129–34
149. Scholz SS, Vadassery J, Heyer M, Reichelt M, Bender KW, et al. 2014. Mutation of the Arabidopsis
calmodulin-like protein CML37 deregulates the jasmonate pathway and enhances susceptibility to her-
bivory. Mol. Plant 7:1712–26
150. Schuman MC, Baldwin IT. 2016. The layers of plant responses to insect herbivores. Annu. Rev. Entomol.
61:373–94
151. Schuman MC, Barthel K, Baldwin IT. 2012. Herbivory-induced volatiles function as defenses increasing
fitness of the native plant Nicotiana attenuata in nature. eLife 1:e00007
152. Schwachtje J, Minchin PEH, Jahnke S, van Dongen JT, Schittko U, Baldwin IT. 2006. SNF1-related
kinases allow plants to tolerate herbivory by allocating carbon to roots. PNAS 103:12935–40
153. Schweizer F, Bodenhausen N, Lassueur S, Masclaux FG, Reymond P. 2013. Differential contribution
of transcription factors to Arabidopsis thaliana defense against Spodoptera littoralis. Front. Plant Sci. 4:13
Annu. Rev. Plant Biol. 2019.70:527-557. Downloaded from [Link]

154. Schweizer F, Fernández-Calvo P, Zander M, Diez-Diaz M, Fonseca S, et al. 2013. Arabidopsis 154. Identifies a
Access provided by University of Stellenbosch on 03/07/22. For personal use only.

basic helix-loop-helix transcription factors MYC2, MYC3, and MYC4 regulate glucosinolate complex of MYC and
biosynthesis, insect performance, and feeding behavior. Plant Cell 25:3117–32 MYB factors that
155. Shangguan X, Zhang J, Liu B, Zhao Y, Wang H, et al. 2018. A mucin-like protein of planthopper is regulate expression of
GS biosynthesis genes.
required for feeding and induces immunity response in plants. Plant Physiol. 176:552–65
156. Shiojiri K, Kishimoto K, Ozawa R, Kugimiya S, Urashimo S, et al. 2006. Changing green leaf volatile
biosynthesis in plants: an approach for improving plant resistance against both herbivores and pathogens.
PNAS 103:16672–76
157. Shitan N, Dalmas F, Dan K, Kato N, Ueda K, et al. 2013. Characterization of Coptis japonica CjABCB2,
an ATP-binding cassette protein involved in alkaloid transport. Phytochemistry 91:109–16
158. Shoji T, Inai K, Yazaki Y, Sato Y, Takase H, et al. 2009. Multidrug and toxic compound extrusion-type
transporters implicated in vacuolar sequestration of nicotine in tobacco roots. Plant Physiol. 149:708–18
159. Shoji T, Kajikawa M, Hashimoto T. 2010. Clustered transcription factor genes regulate nicotine biosyn-
thesis in tobacco. Plant Cell 22:3390–409
160. Song S, Huang H, Gao H, Wang J, Wu D, et al. 2014. Interaction between MYC2 and ETHYLENE
INSENSITIVE3 modulates antagonism between jasmonate and ethylene signaling in Arabidopsis. Plant
Cell 26:263–79
161. Song S, Huang H, Wang J, Liu B, Qi T, Xie D. 2017. MYC5 is involved in jasmonate-regulated plant
growth, leaf senescence and defense responses. Plant Cell Physiol. 58:1752–63
162. Song S, Qi T, Fan M, Zhang X, Gao H, et al. 2013. The bHLH subgroup IIId factors negatively regulate
jasmonate-mediated plant defense and development. PLOS Genet. 9:e1003653
163. Stahl E, Hilfiker O, Reymond P. 2018. Plant-arthropod interactions: Who is the winner? Plant J. 93:703–
28
164. Stegmann M, Monaghan J, Smakowska-Luzan E, Rovenich H, Lehner A, et al. 2017. The receptor kinase
FER is a RALF-regulated scaffold controlling plant immune signaling. Science 355:287–89
165. Steppuhn A, Gase K, Krock B, Halitschke R, Baldwin IT. 2004. Nicotine’s defensive function in nature.
PLOS Biol. 2:e217
166. Stone G. 2003. The adaptive significance of insect gall morphology. Trends Ecol. Evol. 18:512–22
167. Sugio A, Kingdom HN, Maclean AM, Grieve VM, Hogenhout SA. 2011. Phytoplasma protein effector
SAP11 enhances insect vector reproduction by manipulating plant development and defense hormone
biosynthesis. PNAS 108:E1254–63
168. Toyota M, Spencer D, Sawai-Toyota S, Jiaqi W, Zhang T, et al. 2018. Glutamate triggers long-distance,
calcium-based plant defense signaling. Science 361:1112–15
169. Tripathi D, Zhang T, Koo AJ, Stacey G, Tanaka K. 2018. Extracellular ATP acts on jasmonate signaling
to reinforce plant defense. Plant Physiol. 176:511–23
170. Truitt CL, Wei H-X, Pare PW. 2004. A plasma membrane protein from Zea mays binds with the herbi-
vore elicitor volicitin. Plant Cell 16:523–32

[Link] • Plant–Insect Interactions 555

PP70CH19_Reymond [Link] March 26, 2019 13:29

171. Turlings TCJ, Erb M. 2018. Tritrophic interactions mediated by herbivore-induced plant volatiles:
mechanisms, ecological relevance, and application potential. Annu. Rev. Entomol. 63:433–52
172. Vadassery J, Reichelt M, Hause B, Gershenzon J, Boland W, Mithöfer A. 2012. CML42-mediated cal-
cium signaling coordinates responses to Spodoptera herbivory and abiotic stresses in Arabidopsis. Plant
Physiol. 159:1159–75
173. Vaughan MM, Wang Q, Webster FX, Kiemle D, Hong YJ, et al. 2013. Formation of the unusual
semivolatile diterpene rhizathalene by the Arabidopsis class I terpene synthase TPS08 in the root stele is
involved in defense against belowground herbivory. Plant Cell 25:1108–25
174. Véry A-A, Sentenac H. 2002. Cation channels in the Arabidopsis plasma membrane. Trends Plant Sci.
7:168–75
175. Vincent TR, Avramova M, Canham J, Higgins P, Bilkey N, et al. 2017. Interplay of plasma membrane
and vacuolar ion channels, together with BAK1, elicits rapid cytosolic calcium elevations in Arabidopsis
during aphid feeding. Plant Cell 29:1460–79
176. Wang C, Zhou M, Zhang X, Yao J, Zhang Y, Mou Z. 2017. A lectin receptor kinase as a potential sensor
Annu. Rev. Plant Biol. 2019.70:527-557. Downloaded from [Link]

for extracellular nicotinamide adenine dinucleotide in Arabidopsis thaliana. eLife 6:e25474

Access provided by University of Stellenbosch on 03/07/22. For personal use only.

177. Wang K, Guo Q, Froehlich JE, Hersh HL, Zienkiewicz A, et al. 2018. Two abscisic acid responsive
plastid lipase genes involved in jasmonic acid biosynthesis in Arabidopsis thaliana. Plant Cell 30:1006–22
178. Demonstrates that 178. Wang L, Einig E, Almeida-Trapp M, Albert M, Fliegmann J, et al. 2018. The systemin receptor
perception of systemin SYR1 enhances resistance of tomato against herbivorous insects. Nat. Plants 4:152–56
depends on two 179. Wang Q, Li J, Hu L, Zhang T, Zhang G, Lou Y. 2013. OsMPK3 positively regulates the JA signaling
LRR-RK receptors, pathway and plant resistance to a chewing herbivore in rice. Plant Cell Rep. 32:1075–84
SYR1 and SYR2.
180. Williams KS, Gilbert LE. 1981. Insects as selective agents on plant vegetative morphology: Egg mimicry
reduces egg laying by butterflies. Science 212:467–69
181. Winde I, Wittstock U. 2011. Insect herbivore counteradaptations to the plant glucosinolate-myrosinase
system. Phytochemistry 72:1566–75
182. Woldemariam MG, Dinh ST, Oh Y, Gaquerel E, Baldwin IT, Galis I. 2013. NaMYC2 transcription
factor regulates a subset of plant defense responses in Nicotiana attenuata. BMC Plant Biol. 13:73
183. Wu J, Hettenhausen C, Meldau S, Baldwin IT. 2007. Herbivory rapidly activates MAPK signaling in
attacked and unattacked leaf regions but not between leaves of Nicotiana attenuata. Plant Cell 19:1096–
122
184. Wu J, Wang L, Wünsche H, Baldwin IT. 2013. Narboh D, a respiratory burst oxidase homolog in Nico-
tiana attenuata, is required for late defense responses after herbivore attack. J. Integr. Plant Biol. 55:187–98
185. Xiao Y, Wang Q, Erb M, Turlings TCJ, Ge L, et al. 2012. Specific herbivore-induced volatiles defend
plants and determine insect community composition in the field. Ecol. Lett. 15:1130–39
186. Yamaguchi Y, Huffaker A, Bryan AC, Tax FE, Ryan CA. 2010. PEPR2 is a second receptor for the Pep1
and Pep2 peptides and contributes to defense responses in Arabidopsis. Plant Cell 22:508–22
187. Identifies a 187. Yan C, Fan M, Yang M, Zhao J, Zhang W, et al. 2018. Injury activates Ca2+ /calmodulin-dependent
molecular link between phosphorylation of JAV1-JAZ8-WRKY51 complex for jasmonate biosynthesis. Mol. Cell 70:136–
insect-induced Ca2+
37
influx and activation of
188. Yang D-H, Hettenhausen C, Baldwin IT, Wu J. 2012. Silencing Nicotiana attenuata calcium-dependent
JA biosynthesis.
protein kinases, CDPK4 and CDPK5, strongly up-regulates wound- and herbivory-induced jasmonic
acid accumulations. Plant Physiol. 159:1591–607
189. Ye M, Veyrat N, Xu H, Hu L, Turlings TCJ, Erb M. 2018. An herbivore-induced plant volatile reduces
parasitoid attraction by changing the smell of caterpillars. Sci. Adv. 4:eaar4767
190. Yoo SJ, Kim S-H, Kim M-J, Ryu C-M, Kim YC, et al. 2014. Involvement of the OsMKK4-OsMPK1
cascade and its downstream transcription factor OsWRKY53 in the wounding response in rice. Plant
Pathol. J. 30:168–77
191. Zarate SI, Kempema LA, Walling LL. 2007. Silverleaf whitefly induces salicylic acid defenses and sup-
presses effectual jasmonic acid defenses. Plant Physiol. 143:866–75
192. Zhang C, Shi H, Chen L, Wang X, Lü B, et al. 2011. Harpin-induced expression and transgenic overex-
pression of the phloem protein gene AtPP2-A1 in Arabidopsis repress phloem feeding of the green peach
aphid Myzus persicae. BMC Plant Biol. 11:11

556 Erb • Reymond

PP70CH19_Reymond [Link] March 26, 2019 13:29

193. Zhang L, Reed RD. 2016. Genome editing in butterflies reveals that spalt promotes and Distal-less re-
presses eyespot colour patterns. Nat. Commun. 7:11769
194. Zhang X, Mou Z. 2009. Extracellular pyridine nucleotides induce PR gene expression and disease resis-
tance in Arabidopsis. Plant J. 57:302–12
195. Zhao C, Zayed O, Yu Z, Jiang W, Zhu P. 2018. Leucine-rich repeat extension proteins regulate plant
salt tolerance in Arabidopsis. PNAS 115:13123–28
196. Zheng L, McMullen MD, Bauer E, Schön C-C, Gierl A, Frey M. 2015. Prolonged expression of the
BX1 signature enzyme is associated with a recombination hotspot in the benzoxazinoid gene cluster in
Zea mays. J. Exp. Bot. 66:3917–30
197. Zhou G, Qi J, Ren N, Cheng J, Erb M, et al. 2009. Silencing OsHI-LOX makes rice more susceptible to
chewing herbivores, but enhances resistance to a phloem feeder. Plant J. 60:638–48
198. Zhou W, Kügler A, McGale E, Haverkamp A, Knaden M, et al. 2017. Tissue-specific emission of (E)-
α-bergamotene helps resolve the dilemma when pollinators are also herbivores. Curr. Biol. 27:1336–41
199. Züst T, Agrawal AA. 2016. Mechanisms and evolution of plant resistance to aphids. Nat. Plants. 2:15206
Annu. Rev. Plant Biol. 2019.70:527-557. Downloaded from [Link]
Access provided by University of Stellenbosch on 03/07/22. For personal use only.

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Annual Review of
Plant Biology

Volume 70, 2019

Contents

From Bacteriophage to Plant Genetics

Barbara Hohn p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p 1
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Assembly of the Complexes of the Oxidative Phosphorylation System

in Land Plant Mitochondria
Etienne H. Meyer, Elina Welchen, and Chris Carrie p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p23
Chloroplast Lipids and Their Biosynthesis
Georg Hölzl and Peter Dörmann p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p51
Conditional Protein Function via N-Degron Pathway–Mediated
Proteostasis in Stress Physiology
Nico Dissmeyer p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p83
The Scope, Functions, and Dynamics of Posttranslational Protein
Modifications
A. Harvey Millar, Joshua L. Heazlewood, Carmela Giglione, Michael J. Holdsworth,
Andreas Bachmair, and Waltraud X. Schulze p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p 119
Look Closely, the Beautiful May Be Small: Precursor-Derived
Peptides in Plants
Vilde Olsson, Lisa Joos, Shanshuo Zhu, Kris Gevaert, Melinka A. Butenko,
and Ive De Smet p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p 153
Next-Gen Approaches to Flavor-Related Metabolism
Guangtao Zhu, Junbo Gou, Harry Klee, and Sanwen Huang p p p p p p p p p p p p p p p p p p p p p p p p p p p 187
Heterotrimeric G-Protein Signaling in Plants: Conserved and Novel
Mechanisms
Sona Pandey p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p 213
Division Plane Establishment and Cytokinesis
Pantelis Livanos and Sabine Müller p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p 239
Control of Meristem Size
Munenori Kitagawa and David Jackson p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p 269
The Dynamics of Cambial Stem Cell Activity
Urs Fischer, Melis Kucukoglu, Ykä Helariutta, and Rishikesh P. Bhalerao p p p p p p p p p p p p p 293

vi
 PP70_FrontMatter ARI 30 March 2019 11:50

Thermomorphogenesis
Jorge J. Casal and Sureshkumar Balasubramanian p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p 321
Leaf Senescence: Systems and Dynamics Aspects
Hye Ryun Woo, Hyo Jung Kim, Pyung Ok Lim, and Hong Gil Nam p p p p p p p p p p p p p p p p p p p 347
Molecular Mechanisms of Plant Regeneration
Momoko Ikeuchi, David S. Favero, Yuki Sakamoto, Akira Iwase,
Duncan Coleman, Bart Rymen, and Keiko Sugimoto p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p 377
Functional Status of Xylem Through Time
Craig R. Brodersen, Adam B. Roddy, Jay W. Wason, and Andrew J. McElrone p p p p p p p 407
Molecular Networks of Seed Size Control in Plants
Na Li, Ran Xu, and Yunhai Li p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p 435
Annu. Rev. Plant Biol. 2019.70:527-557. Downloaded from [Link]
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Molecular and Environmental Regulation of Root Development

Hans Motte, Steffen Vanneste, and Tom Beeckman p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p 465
MicroRNAs and Their Regulatory Roles in Plant–Environment
Interactions
Xianwei Song, Yan Li, Xiaofeng Cao, and Yijun Qi p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p 489
Molecular Interactions Between Plants and Insect Herbivores
Matthias Erb and Philippe Reymond p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p 527
A Molecular View of Plant Local Adaptation: Incorporating
Stress-Response Networks
Acer VanWallendael, Ali Soltani, Nathan C. Emery, Murilo M. Peixoto,
Jason Olsen, and David B. Lowry p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p 559
Evolution of Glucosinolate Diversity via Whole-Genome
Duplications, Gene Rearrangements, and Substrate Promiscuity
Brenden Barco and Nicole K. Clay p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p 585
Comparative and Functional Algal Genomics
Crysten E. Blaby-Haas and Sabeeha S. Merchant p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p 605
The Genomics of Oryza Species Provides Insights into Rice
Domestication and Heterosis
Erwang Chen, Xuehui Huang, Zhixi Tian, Rod A. Wing, and Bin Han p p p p p p p p p p p p p p p 639
CRISPR/Cas Genome Editing and Precision Plant Breeding in
Agriculture
Kunling Chen, Yanpeng Wang, Rui Zhang, Huawei Zhang, and Caixia Gao p p p p p p p p p p 667
Risk Assessment and Regulation of Plants Modified by Modern
Biotechniques: Current Status and Future Challenges
Joachim Schiemann, Antje Dietz-Pfeilstetter, Frank Hartung, Christian Kohl,
Jörg Romeis, and Thorben Sprink p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p 699

Contents vii
 PP70_FrontMatter ARI 30 March 2019 11:50

Crop Biodiversity: An Unfinished Magnum Opus of Nature

Matthew B. Hufford, Jorge C. Berny Mier y Teran, and Paul Gepts p p p p p p p p p p p p p p p p p p p p 727
Crop Improvement Through Temperature Resilience
Jingyu Zhang, Xin-Min Li, Hong-Xuan Lin, and Kang Chong p p p p p p p p p p p p p p p p p p p p p p p p p 753
Water Use Efficiency as a Constraint and Target for Improving the
Resilience and Productivity of C3 and C4 Crops
Andrew D.B. Leakey, John N. Ferguson, Charles P. Pignon, Alex Wu,
Zhenong Jin, Graeme L. Hammer, and David B. Lobell p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p 781
A Fruitful Journey: Pollen Tube Navigation from Germination to
Fertilization
Mark A. Johnson, Jeffrey F. Harper, and Ravishankar Palanivelu p p p p p p p p p p p p p p p p p p p p p p 809
Annu. Rev. Plant Biol. 2019.70:527-557. Downloaded from [Link]
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Errata

An online log of corrections to Annual Review of Plant Biology articles may be found at
[Link]

viii Contents