jasmonates induce both defense responses and communication in monocotyledonous and dicotyledonous...

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Jasmonates Induce Both Defensive and Infochemical Strategies in

Monocotyledonous and Dicotyledonous Plants

Kazunori Okada1, Hiroshi Abe

2, Gen-ichiro Arimura

3*

1 Biotechnology Research Center, The University of Tokyo, Tokyo 113-8657, Japan

2 Experimental Plant Division, RIKEN BioResource Center, Tsukuba 305-0074, Japan

3 Department of Biological Science & Technology, Faculty of Industrial Science &

Technology, Tokyo University of Science, Tokyo 125-8585, Japan

*Correspondence should be addressed to:

Gen-ichiro Arimura

Department of Biological Science & Technology, Faculty of Industrial Science &

Technology, Tokyo University of Science, 6-3-1 Niijuku, Katsushika-ku, Tokyo

125-8585, Japan

Tel: 81 3 5876 1467

Fax: 81 3 5876 1639

E-mail: [email protected]

© The Author 2014. Published by Oxford University Press on behalf of Japanese Society of Plant Physiologists. All rights reserved. For Permissions, please e-mail: [email protected]

Plant and Cell Physiology Advance Access published November 4, 2014 at O

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Abstract

Jasmonic acid and its derivatives (jasmonates: JAs) are phytohormones with essential

roles in plant defense against pathogenesis and herbivorous arthropods. Both the up-

and down-regulation of defense responses are dependent on signaling pathways

mediated by JAs as well as other stress hormones (for example, salicylic acid),

generally those involving the transcriptional and post-transcriptional regulation of

transcription factors via protein modification and epigenetic regulation. In addition to

the typical model plant Arabidopsis (a dicotyledon), advances in genetics research have

made rice a model monocot in which innovative pest control traits can be introduced and

whose JA signaling pathway can be studied. In this review, we introduce the dynamic

functions of JAs in plant defense strategy using defensive substances (e.g., indole

alkaloids and terpenoid phytoalexins) and airborne signals (e.g., green leaf volatiles and

volatile terpenes) in response to biotrophic and necrotrophic pathogens as well as

aboveground and belowground herbivores. We then discuss the important issue of how

the mutualism of herbivorous arthropods with viruses or bacteria can cause cross-talk

between JA and other phytohormones to counter the defense systems.

Keywords

jasmonates; plant defense response; specialized metabolites; transcription factor;

volatile organic compounds

Abbreviations

AOC, allene oxide cyclase; ERF, ethylene response factor; GA, gibberellin; GLV, green

leaf volatile; GST, glutathione transferase; HIPV, herbivore-induced plant volatile; ISR,

induced systemic resistance; JA, jasmonic acid; JAs, jasmonates; JA-Ile,

jasmonoyl-L-isoleucine; JMT, S-adenosyl-L-methionine:jasmonic acid carboxyl

methyltransferase; MeJA, methyl jasmonate; MEP, methylerythritol phosphate; OPDA,

12-oxo-phytodienoic acid; OPR, 12-oxophytodienoate reductase; PR,

pathogenesis-related; RKN, root-knot nematode; SA, salicylic acid; SCF,

skp1-cullin-F-box; TI, trypsin inhibitor; TMTT,

(E,E)-4,8,12-trimethyltrideca-1,3,7,11-tetraene; TSWV, tomato spotted wilt virus; VOC,

volatile organic compound, WCR, western corn rootworm.

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Introduction

One of the significant factors determining plant growth and reproduction is defense; a

defended plant can withstand against pathogens and herbivores. Plants have developed

an impressive array of immune and defense responses in their cells. The success of

plants’ defense strategies is based on their ability to rapidly recognize specific pests and

promote signal transduction to induce defense molecules. In this paper, we review

recent advances in knowledge about jasmonates (JAs), hormones used for plant defense

processes ranging from direct defense using phytoalexins to indirect defense using

infochemicals (e.g., those that are related to plant communication and the attraction of

natural enemies of pests). Great progress has been made in the last decade towards

understanding the ubiquitous involvement of JAs and their cross-talk with other

phytohormones in the defense of monocotyledonous and dicotyledonous plants.

JA-Mediated Plant Defenses Against Pathogens

In a plant’s immune system, the plant hormone jasmonic acid (JA) and its derivatives

(JAs) have been recognized as key regulators that play crucial roles in plant defense

responses to pathogens (Pieterse et al. 2012). In the last decade, numerous studies have

been carried out using genetically modified Arabidopsis plants (e.g.,

coronatine-insensitive1 (coi1) mutants) in which JA synthesis or signaling is modulated;

consequently, the functions of JAs in plant resistance to both biotrophic and

necrotrophic pathogens have been convincingly demonstrated (Supplementary Table 1).

Briefly, the F-box COI1 protein, which functions as part of the JA -receptor, interacts

with the Skp1/Cullin counterparts to form the Skp1-Cullin-F-box (SCF)COI1

ubiquitin

E3 ligase complex; interacts physically with JAZ repressor proteins in the presence of

JA conjugated with amino acid isoleucine [jasmonoyl-L-isoleucine (JA-Ile), the active

form of JA], to promote the expression of JA-responsive genes (Thines et al. 2007). The

significance of COI1 protein for JA signaling was also confirmed by previous findings

that the expression levels of more than 80% of JA-responsive genes (e.g.,

pathogenesis-related (PR) proteins) decline in coi1 mutants (Devoto et al. 2005; Feys et

al. 1994; Xie et al. 1998). Such a decline makes the mutants susceptible to

necrotorophic pathogens. Likewise, a jar1-1 mutant defective in an active enzyme

involved in JA-Ile synthesis exhibits diminished expression of its JA-regulated genes

and is highly susceptible to a soil fungus, Pythium irregulare (Staswick et al. 2002;

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Staswick et al. 1998). Conversely, the constitutive expression of vegetative storage

protein 1 (cev1), a JA-hypersensitive Arabidopsis mutant, is defensive itself against a

fungal pathogen (Erysiphe cichoracearum) because it can constitutively produce JA and

ethylene (Ellis and Turner 2001). There is, therefore, no doubt about the positive and

extensive contributions of the JA-COI1 signaling system to plant pathogenesis

immunity in Arabidopsis.

Recently, Hu et al. (2013) reported that JAV1, JA-associated VQ motif gene 1,

functions as one of the negative regulators in JA-mediated protection against both insect

attack and pathogen infection. The JA-COI1 signaling system, which is associated with

the degradation of JAV1 via the 26S proteasome, activated the expression of defensive

genes and the acquisition of resistance to caterpillars of Spodoptera exigua and the

necrotrophic fungus Botrytis cinerea. If uninfected, JAV1 may interact with

transcription factors (e.g., WRKYs) to turn off their active functions. After pest

invasion, the degradation of JAV1 may cause the activation of various down-stream

regulators, leading to the positive regulation of respective down-stream signal cascades.

This negative regulation may be required for damaged plants to fine-tune their

JA-responsive defense reactions in order to modulate their energy and resource balance

between growth/development and defense during and after suffering stress.

Methyl jasmonate (MeJA), an airborne jasmonate, can also induce defense-related

genes, including PDF1.2 (Manners et al. 1998). S-adenosyl-L-methionine:jasmonic acid

carboxyl methyltransferase (JMT) is responsible for converting JA to MeJA (Seo et al.

2001). Transgenic Arabidopsis plants overexpressing a JMT gene exhibit the elevated

production of MeJA but not JA, resulting in the constitutive expression of

JA-responsive genes VSP and PDF1.2. Moreover, those transgenic plants were able to

defend themselves against infection by B. cinerea, indicating that this methylated form

of JA is one of the active molecules in plant defense response (Seo et al. 2001). Thorpe

and co-workers reported that the transport of MeJA in tobacco involves both xylem and

phloem pathways, and these pathways rely on sucrose transporter-like carriers (possibly

the same carriers) between the phloem and xylem. The enhanced transport of both sugar

and MeJA may be owing to the MeJA-induced enhancement of the energy of the

plasma membrane (Thorpe et al. 2007), which may help to explain how MeJA plays a

systemic role in plant defense even though it is a volatile chemical.

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Other JA derivatives are known as well. Arabidopsis opr3 mutants lacking any

12-oxophytodienoate reductase (OPR) activity fail to convert 12-oxo-phytodienoic acid

(OPDA) to OPC8:0, which is essential for JA biosynthesis (Stintzi and Browse 2000).

Unlike JA-insensitive plants such as the coi1-1 and jar1-1 mutants, OPR mutants (opr3)

displayed increased resistance to the necrotrophic fungus Alternaria brassicicola. Thus,

OPDA may play a role that is independent of JA’s in defense against certain pathogen

species. Taken together, the above findings indicate that several JA derivatives are

produced by plants and contribute to the diversity of plant defense actions.

In contrast to the above findings in dicots, the JA signaling pathway in monocots

(e.g., maize and rice) has not been thoroughly investigated. This is mostly because of

the shortage of mutants and transgenic plant resources available rather than the shortage

of DNA/cDNA resources and sequences. Recently, genetic engineering approaches have

begun to dissect the involvement of JA signaling in pathogen resistance in rice, and our

knowledge of the JA pathway has increased dramatically in the last few years.

Transgenic rice plants constitutively expressing AOS2, an allene oxide synthase

involved in JA production, showed increased resistance to attack by pathogenic fungi

and robustly induced the expression of anti-pathogen-related genes (i.e., PR1a, PR3 and

PR5) (Mei et al. 2006). Most recently, two jasmonate-deficient allene oxide cyclase

(AOC) mutants, cpm2 and hebiba, have been characterized as susceptible to the fungal

hyphae of an incompatible, generally avirulent strain of Magnaporthe oryzae (Riemann

et al. 2013). Similarly, rice osjar1-2 mutants appeared more susceptible to blast fungus

than did wild-type plants (Shimizu et al. 2013), indicating that JA-Ile (the JAR1

product) mediates the defense response against blast fungus in rice, as it does in

Arabidopsis. Moreover, the silencing of OsCOI1 increased plants’ susceptibility to

chewing insects along with the number of genes down-regulated for trypsin protease

inhibitor, peroxidase, and polyphenol oxidase (polyphenol oxidase oxidizes phenolics to

highly toxic quinones) (Ye et al. 2012).

Intriguingly, rice in which OsCOI1a and OsCOI1b had been knocked down

exhibited elongated plant height, internode length, and cell length (also the case in

gibberellin (GA)-overaccumulating mutant eui1), as well as decreased sensitivity to JA.

It was shown in the transformed lines that repressed JA signaling caused both the

degradation of a DELLA repressor regulator and the consequent activation of a PIF

positive regulator for plant growth in GA signaling; thus it can be said that repressed JA

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signaling promotes plants’ ability to grow (Yang et al. 2012). In other words, plants are

likely to strategically switch between the mode of normal growth and defense actions

using negative crosstalk between GA and JA signaling.

It is generally accepted that monocotyledonous plants tend to possess a COI1

family, unlike Arabidopsis: 3 members of COI1 homologues have been predicted in rice

and functionally characterized. When rice COI1 homologs OsCOI1a and OsCOI1b were

independently introduced into an Arabidopsis coi1-1 mutant, JA insensitivity was fully

complemented in both. By contrast, the homolog OsCOI2 was not sufficient to

complement JA insensitivity, probably because one of the critical amino acid residues

responsible for the binding of JAs is not conserved in OsCOI2: highly conserved

tyrosine (Tyr) in AtCOI1 (Tyr-386), OsCOI1a (Tyr-389), and OsCOI1b (Tyr-386) is

replaced by histidine (His) in OsCOI2 (His-391). Instead, a single substitution of the

His-391 residue with Tyr in OsCOI2 resulted in the interaction of OsCOI2 with massive

OsJAZ proteins and the complementation of JA insensitivity in the coi1-1 mutant (Lee

et al. 2013). Those examples suggest that OsCOI1 has different preferences for JAZ

partners: some homologs can interact with heterozygous plant JAZ but the others cannot.

A diversity of molecular interactions may be required for the JA-responsive gene

superfamily to take advantage of various environmental situations.

Moreover, rice OsJAZ8 is known to interact with OsCOI1b (referred to OsCOI1H

in the original paper) in a COR-dependent manner. The overexpression of OsJAZ8ΔC,

which is defective in the C-terminal region responsible for the binding to COI1s

(defined as a Jas motif, a 20-amino-acid length of the conserved domain in JAZ family)

caused an insensitivity to JA and an increased susceptibility to bacterial blight

Xanthomonas oryzae pv. oryzae (Yamada et al. 2012). These findings reveal that the

COI1-JAZ signaling system, which conserved not only Arabidopsis but also rice, is the

central machinery for JA-mediated plant defenses against pathogens.

In other cases of monocots, e.g., wheat, at least two COI1 homologs (TaCOI1 and

TaCOI2) are responsible for root growth, although it is not known whether these

homologs function in JA signaling (Bennypaul et al. 2012). In Brachypodium

distachyon, three COI1-like proteins exhibiting relatively high identities of amino acid

sequence compared to those in Arabidopsis COI1 (LOC100829997, LOC100825916,

and LOC100845226) have been found, although their functions are obscure

(unpublished). B. distachyon, commonly called purple false brome, has been established

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as an experimental model species of Poaceae, because of its small physical stature (approximately 20 cm at maturity), self-fertilizing life cycle of less than 4 months,

simple growth requirements, and efficient transformation system (Draper et al. 2001;

Vain et al. 2008). Undoubtedly, such benefits will help us to dissect and understand the

mechanisms underlying Poaceae JA-COI1 signaling.

Transcriptional Regulation of Specialized Metabolites in Plants

JAs have a pivotal role in regulating the biosynthesis of multiple components of

specialized metabolic pathways. Classically, Gundlach et al. (1992) showed that

alkaloid synthesis in a variety of plant cell cultures was linked to the increase of

endogenous JA levels in cells induced by a rough yeast elicitor. Nowadays, we know

that JA mediates the production of distinct classes of specialized metabolites, including

terpenes, terpene indole alkaloids, phenylpropanoids, flavonoids, and nicotine, etc.

(Wasternack and Hause 2013). In dicots, typical metabolites are well known as

vinblastine in Catharanthus roseus, camalexin in Arabidopsis, and nicotine in tobacco.

In monocots, diterpenoid phytoalexins such as momilactones and phytocassanes, and

sakuranetin, a flavonoid phytoalexin, have been found in rice (Miyamoto et al. 2014b).

The JA-induced productions of zealexin (sesquiterpenoid phytoalexins) and kauralexin

(diterpenoid phytoalexins), both of which have also been discovered in maize (Schmelz

et al. 2014) (Fig. 1).

The transcriptional regulation involved in the JA-dependent production of

specialized metabolites has been well studied in tobacco (Nicotiana tabacum). Tobacco

produces nicotine in the roots, and its synthesis is elicited by foliage herbivores

(folivores) via a JA-mediated signaling cascade in the leaves (Shoji et al. 2010). Most of

the structural genes involved in nicotine production are transcriptionally regulated by an

ethylene response factor (ERF) subfamily, encoded by genes clustered in the

NIC2-locus. The NIC2-locus ERFs are close homologs of ORCA3, a JA-responsive

transcriptional activator of indole alkaloid biosynthesis in C. roseus (Memelink et al.

2001). Furthermore, NIC2-locus-encoded ERF189 and ORCA3 ERF factors are,

respectively, regulated hierarchically by NtMYC2 and CrMYC2, master regulators in

the JA signaling pathway; these regulators are conserved in a suite of plant taxa (Shoji

and Hashimoto 2011; Zhang et al. 2011). Notably, two distant plant species, tobacco

(Solanaceae) and periwinkle (Apocynaceae), rely on closely related transcription factor

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genes to control the expression of JA-inducible structural genes for distinct specialized

metabolites (i.e., nicotine in tobacco and indole alkaloides in periwinkle) (Shoji et al.

2010).

Glucosinolates and indolic compounds, present in almost all plants of the order

Brassicales, are produced under the control of well-characterized regulatory

mechanisms (Grubb and Abel 2006; Sønderby et al. 2010). Camalexin, an

indole-specialized metabolite, is the major phytoalexin produced in Brassicales,

including Arabidopsis (Ausubel et al. 1995; Nafisi et al. 2007; Tsuji et al. 1992), and the

transcriptional networks regulating its production have been extensively investigated

(Mao et al. 2011; Qiu et al. 2008; Saga et al. 2012). In particular, WRKY33 acts

down-stream of two pathogen-responsive mitogen-activated protein kinases, MPK3 and

MPK6, to activate genes that synthesize camalexin in B. cinerea- or JA-treated

Arabidopsis plants (Mao et al. 2011; Takahashi et al. 2007). MPK4 and its substrate

MKS1 (a VQ-family protein) interact with WRKY33 in vivo, and WRKY33 is released

from complexes with MPK4 upon infection with the pathogenic bacterium

Pseudomonas syringae (Qiu et al. 2008). Camalexin biosynthesis is likely regulated

additionally by ANAC042, a member of the NAC family of transcription factors.

Expression of the ANAC042 gene is induced in Arabidopsis by bacterial elicitor

flagellin in an ethylene-dependent but salicylic-acid (SA)-independent manner. This

expression is, however, repressed by the application of MeJA; such repression

demonstrates antagonistic cross-talk between ethylene and JA signaling in the

transcriptional controls of ANAC042. Notably, it appears that transcript levels of

WRKY33 are not affected in the roots of an ANAC042-defective mutant (Saga et al.

2012); it would imply that ANAC042 is at least not an up-stream regulator of WRKY33.

There should be distinct regulation driven by either ANAC042 or WRKY33 in the

induction of camalexin biosynthesis by bacterial pathogens.

The application of chitooctaose elicitor (biotic stress) or CuCl2 (abiotic stress) to

rice cells rapidly but transiently increases endogenous JA accumulation following the

induced biosynthesis of momilactone A, a diterpenoid phytoalexin (Nojiri et al. 1996;

Rakwal et al. 1996). In a similar way, the infection of rice leaves with blast fungus M.

oryzae also induces the production of both JA-Ile and phytoalexin in the infected area

(Riemann et al. 2013; Wakuta et al. 2011). The involvement of JAs in the production of

phytoalexins was further supported by the finding that the application of JA solution to

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rice leaves induces the production of momilactones as well as diterpenoid-type

phytoalexins, phytocassanes and a flavonoid type, sakuranetin (Shimizu et al. 2012;

Shimizu et al. 2013). The role of JAs in pathogen resistance was investigated using two

OsAOC mutants (cpm2 and hebiba); in both mutants, the constitutive production of JAs

and the wound-induced production of JAs were suppressed. The mutants suffered

aggressive damage from infection with M. oryzae, probably because they were unable

to accumulate momilactones as well as wild-type plants were (Riemann et al. 2013). In

contrast, it was found that the rice Tos17 JAR1 mutant osjar1-2 selectively decreases

the production of the flavonoid phytoalexin (sakuranetin) but not that of diterpenoid

phytoalexins (momilactones and phytocassanes) in leaves in response to heavy metal

stress or M. oryzae infection (Shimizu et al. 2013). Collectively, these results illuminate

how both JA-dependent and JA-independent pathways operate to regulate rice

diterpenoid phytoalexin biosynthesis in response to both biotic and abiotic stress

responses.

Comprehensive rice microarray analyses demonstrate that a subset of genes

encoding diterpene synthases (OsCPS2, OsCPS4, OsKSL4 and OsKSL7), cytochrome

P450s (CYP99A2, CYP99A3, CYP71Z7, CYP76M6, CYP76M7 and CYP76M8) and

the dehydrogenase OsMAS are expressed simultaneously after elicitation with either JA

or chitooctaose (Miyamoto et al. 2012; Okada et al. 2007). Intriguingly, all those genes

involved in the biosynthetic pathway for momilactone and phytocassane are exclusively

clustered on rice chromosomes 4 and 2, respectively, suggesting the existence of

integrated transcriptional systems in a manner that depends on the metabolic pathway.

When the elicitor-inducible OsTGAP1 (TGA factor for phytoalexin production 1),

which binds to the TGACG motif (an elicitor-responsive cis-acting element), is

overexpressed in rice cells, both momilactone and phytocassane are accumulated at the

same time as the chitooctaose is being elicited. This simultaneity probably occurs

because multiple genes are being up-regulated at the same time, including OsKSL4,

OsKSL7, and OsDXS3, all of which are involved in the commitment step of the

biosynthesis of the terpenoid phytoalexn, including methylerythritol phosphate (MEP)

pathway in the cells (Okada et al. 2009).

Recently, a direct target gene of OsTGAP1 has been identified by combining

ChIP-seq and transcriptome analyses. The result revealed that OsDXS3, but not other

genes involved in terpenoid phytoalexn biosynthesis, was directly regulated by

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OsTGAP1. Nonetheless, a suite of potential OsTGAP1-binding regions is present in the

intergenic regions within and near the cluster region, suggesting that transcriptional

regulation may be driven primarily by the integrated transcriptional machinery with

multiple cis-sensors that are bound with a single trans-activator within a wide range of

promoter and enhancer regions. Altogether, OsTGAP1 is likely to be incorporated in the

positive transcript regulation system for an array of genes involved in the MEP pathway,

hereby bringing about the elicitor-inducible production of at least two phytoalexin

classes (Miyamoto et al. 2014a).

There are several WRKY-type transcription factors functioning in either up- or

down-regulation. OsWRKY53, a group I-type WRKY transcription factor, has been

found to act as a positive regulator of multiple momilactone biosynthetic pathway genes

(OsCPS4 and CYP99A2) (Chujo et al. 2014). OsWRKY45, a group III-type WRKY

transcription factor, is involved in the regulation of diterpenoid phytoalexin production

in the SA/cytokinin signaling pathway, and this WRKY transcription factor plays a

central role in the benzothiadiazole-mediated priming of diterpenoid phytoalexin

biosynthetic genes in rice leaves (Akagi et al. 2014). Conversely, the group IIa WRKY

transcription factor OsWRKY76 plays negative roles in rice defense against M. oryzae

(Yokotani et al. 2013). Another group IIa WRKY transcription factor, OsWRKY28, also

acts as a negative regulator of basal defense responses against blast fungus M. oryzae by

suppressing defense-related gene expression levels (Chujo et al. 2013). Again, these

WRKY transcription factors are JA-inducible but act to negatively coordinate the

JA-mediated genes needed for fine-tuning defense actions in rice.

In fact, the JA-associated transcriptional control of specialized metabolic pathway

genes is known to be complex. One example of this complexity is that ERF and MYC2

transcription factors synergistically regulate the expression of genes that synthesize

nicotine in tobacco (Shoji and Hashimoto 2011), and another example is that different

types of WRKY and TGA factors in rice antagonistically regulate the genes for

biosynthesizing diterpene phytoalexin production (Chujo et al. 2013; Okada et al. 2009;

Yokotani et al. 2013). Moreover, chromatin remodeling and histone modification have

recently been highlighted as another mode of transcriptional regulation. Chromatin

decondensation and histone modification are particularly required for the transcriptional

regulation of triterpenoid biosynthetic gene cluster regions in Arabidopsis and oat plants

(Field and Osbourn 2008; Wegel et al. 2009). These phenomena are and will be topics

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of great interest in this field (Fig. 2).

JA Signaling and Its Cross-talk with Other Phytohormones in Plant-Herbivore

Interactions

As reviewed above, cross-talk among phytohormones involved in signaling plays an

important role in plant defenses. Since knowledge of the molecular and ecological

significance for such cross-talk involving not only pathogenesis but also herbivore

attack has recently been updated, several of the mechanisms of such cross-talk are

discussed in this chapter (Fig. 3).

Of the interactions between plants and piercing-sucking herbivores, those

involving aphids have been studied most because they pose serious threats to agriculture

and horticulture. Avila et al. (2012) reported that JA-deficient spr2 mutants of tomatoes

show elevated aphid resistance, indicating that JA signaling has a negative impact on

basal aphid resistance. Intriguingly, the increased aphid resistance in spr2 mutants can

be restored to wild-type levels of susceptibility by overexpressing a salicylate

hydroxylase gene, as this gene suppresses SA accumulation. Resistance in spr2 is,

conversely, lost when the expression of NONEXPRESSOR OF

PATHOGENESIS-RELATED PROTEINS 1 (NPR1), a positive regulator of SA

signaling, is suppressed. These findings indicate that aphid resistance in spr2 mutants is

linked to SA signaling, given that JA and SA signaling are antagonistic for plant-aphid

interactions. However, the function of JA in aphid resistance is still controversial. For

instance, it has been shown in Arabidopsis that JA-insensitive mutants (coi1-1) are

susceptible to aphids (Mewis et al. 2005) and, conversely, that activating JA signaling in

an Arabidopsis mutant (cev1) increases aphid resistance (Ellis et al. 2002). Those data

are not in accord with the above-described reports in tomato, implying JA has a

host-specific function.

Again, the coordinated regulation of defense responses between the JA and SA

pathways is mostly observed in plants infested with sucking arthropods, including aphid,

whitefly and spider mite (Arimura et al. 2009). Zarate et al. (2007) reported that in

Arabidopsis, feeding by the silverleaf whitefly tended to induce the SA-dependent plant

defense, which is antagonistic to the JA-dependent plant defense. Such antagonism can

result when herbivores attempt to deactivate plant defenses (the ‘‘decoy’’ hypothesis) to

enhance insect performance, and is generally widespread among other herbivores as

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well. For instance, Helicoverpa zea larvae egest saliva containing glucose oxidase into

their feeding sites, which suppresses the JA-regulated defenses that deter larval growth

on tobacco leaves (Musser et al. 2002). This is because glucose oxidase catalyzes the

production of hydrogen peroxide, which elicits SA production in the host leaves (Diezel

et al. 2009). In turn, regarding mollusks (e.g., slugs and snails), one slug species

(Deroceras reticulatum) can secrete locomotion mucus containing SA to a damaged leaf

area and thereby activate the SA-responsive gene PR1 in Arabidopsis (Kästner et al.

2014). These cases suggest mucus may negatively regulate plant defenses just as

glucose oxidase in H. zea larval saliva does.

Moreover, a case of an herbivores’ “decoy” involves Colorado potato beetle

(Leptinotarsa decemlineata) larvae, which rely on symbiotic bacteria in their saliva to

suppress antiherbivore defenses in tomato (Solanum lycopersicum) (Chung et al. 2013).

When larvae feed on host plants, they secrete symbiotic bacteria, including the genera

Stenotrophomonas, Pseudomonas, and Enterobacter, to the infested area; as a result, JA

signaling is suppressed and SA signaling is enhanced (Chung et al. 2013). Such

manipulation of the hormone balance benefits the herbivore rather than the plant host,

as SA-responsive immunity is nearly useless at this stage. In these cases, the herbivore

strategically disturbs the JA-responsive defense pathway by exploiting symbiotic

bacteria as a decoy, misleading the plant host cells into reacting to the perceived threat

of microbial pathogenesis.

In cases of plant-herbivore-virus interactions, the deactivation of the

JA-dependent plant defense has complex consequences. For instance, tomato spotted

wilt virus (TSWV) infection enhances the performance of western flower thrips

(Frankliniella occidentalis) and makes plants more attractive to thrips (Maris et al.

2004). TSWV infection suppressed thrips-induced JA signaling in Arabidopsis host

plants due to TSWV-induced SA actions (Abe et al. 2012); the paralyzed defense ability

of host plants benefited the thrips. Because TSWV is not transovarially transmitted,

thrips can acquire TSWV only through infected host plants (Wijkamp et al. 1996).

Moreover, thrips larvae are more comfortable on plants inoculated with viruliferous

adult females than on plants inoculated with non-viruliferous females (Abe et al. 2012):

this confirms a recent report that Southern rice black-streaked dwarf virus infection in

rice plants also improves the performance of the insect vector, Sogatella furcifera

(Zhang et al. 2014). In summary, these observations indicate that the negative impact of

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TSWV infection on the JA-induced defense system in its host is ultimately beneficial to

the vector thrips, indicating there is a mutualism between thrips and TSWVs.

In rice plants, the SA-JA antagonisms have been intensively studied (De

Vleesschauwer et al. 2013; Li et al. 2013; Zhou et al. 2009). Attenuated JA production

in lipoxygenase-silenced rice plants corresponds to increased SA levels; increased SA

levels enhance plants’ resistance to planthoppers and also lower susceptiblity to

caterpillar feeding (Zhou et al. 2009). These phenotypes were similarly observed in rice

plants overexpressing antisense rice NPR1 (OsNPR1) gene: i.e., enhanced JA response

and caterpillar resistance (Li et al. 2013).

Notably, the expression of various genes including OsNPR1 is induced not only

by JA but also by SA (Garg et al. 2012; Li et al. 2013). Tamaoki et al. (2013) has shown

that although one-third of genes induced by the SA agonist benzothiadiazole (BTH) are

down-regulated by JA application, more than half of all the BTH-induced genes are

up-regulated by JA application. This ratio suggests JA and SA interact synergistically in

the transcriptional regulation of most of defensive genes in this monocot species.

Moreover, this responsiveness is even dependent on foliage age. For instance, it has

been reported that PR1 protein levels in rice in response to both JA and SA are high in

the older rice leaf (the second and third leaves of five-leaf stage) but limited in the

young leaf (the fifth leaves of five-leaf stage) (Xie et al. 2011). NRR, the

NPR1-interacting protein, was found to negatively regulate age-related resistance. In

Arabidopsis, age-dependent immunity to pathogens was lacking in the SA-deficient

mutant sid2-1 (Kus et al. 2002), suggesting the importance of a specific factor(s)

coordinating with SA signaling.

Defense Responses to Root Herbivores

In contrast to foliage herbivores (folivores), little is known about underground plant

defense and signaling systems in root herbivores. One belowground maize plant signal is,

for example, induced by the root-feeding beetle (Western corn rootworm, WCR); the

signal, the sesquiterpene (E)-β-caryophyllene, attracts a parasitic nematode, a natural

enemy of WCR (Rasmann et al. 2005). Root damage by the WCR can also profoundly

alter the defensive state of maize aboveground, as feeding by WCR belowground

increases the resistance to the leaf herbivore Spodoptera littoralis and the fungal

pathogen Setosphaeria turcica (Erb et al. 2009). The vertical response of the plant in

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this case does not follow a classical pattern of wound induction but, rather, is mainly

caused by hydraulic changes and abscisic acid signaling (Erb et al. 2011; Rasmann et al.

2005).

On the other hand, root-knot nematodes (RKNs) are plant-parasitic nematodes that

invade roots and stems of various plant taxa and thereby inhibit the absorption of

nutrients and the uptake of water (Wyss et al. 1992; Wyss and Zunke 1986). RKNs are

known to induce dynamic changes in the architecture of host plant cells: cells undergo

repeated karyogenesis without cytogenesis in response to nematode invasion and

produce giant cells that serve as the nutrient source for RKN (Williamson and Gleason

2003). According to several studies, it is likely that at least three hormones, namely, JA,

SA and ethylene, positively regulate plant defense properties against RKNs in several

plant species (Fudali et al. 2013; Fujimoto et al. 2011; Priya et al. 2011). Curiously, a loss

of JA function can even increase plant resistance to RKN attack in tomato, indicating a

reversible effect of JA signaling. Recent studies based on a functional genomics

approach have also shown the possible involvement of GA and auxin in plant resistance

to RKN invasion (Beneventi et al. 2013). Moreover, antagonistic cross-talk between

brassinosteroids and JA is involved in RKN resistance in rice (Nahar et al. 2013).

RKNs are known to secrete effectors that suppress host defenses. The calreticulin

from Meloidogyne incognita (Mi-CRT), a calcium-binding protein, is synthesized in the

subventral glands of RKN and secreted by the nematode into the apoplasm of infected

tissues; there it helps ensure the success of the infection (Jaubert et al. 2005). Although

little is known about the exact function of Mi-CRT after it is secreted into plant cells,

Mi-CRT is predicted to chelate calcium in the apoplasm and prevent calcium influx, and

thereby suppress plant basal defenses during the interaction (Jaouannet et al. 2013). Ca2+

signaling regulates SA-mediated immunity in Arabidopsis (Qiu et al. 2012). Systematic

studies should be conducted to clarify interactions between the effector/elicitor secreted

during the RKN host plant immune response.

Induced Biosynthesis of Volatile Infochemicals That Serve as Attractants of the

Arthropods and as Alerts for Plant Communications

As extensively reviewed above, a large number of specialized metabolites are

induced in many plant taxa in response to pathogen and herbivore attack. Of these,

volatile organic compounds (VOCs) (e.g., terpenes, green leaf volatiles [GLVs],

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phenylpropanoids, etc.) act as airborne signals which often affect the behavior of

herbivores, natural enemies of herbivores, and neighboring plants (Arimura et al. 2009).

Since JAs are master switches, up-regulating them induces the de novo synthesis of

VOCs after such biotic stresses, the exogenous application of JAs (JA or MeJA) can

induce blends of VOCs in both monocots and dicots, as if they had been attacked by

herbivores (Arimura et al. 2009). Therefore, the ability to biosynthesize VOCs appears

to be massively weakened in tomato mutant plants which are deficient in the JA

biosynthetic pathway (def1) (Degenhardt et al. 2010; van Schie et al. 2007) and in

transgenic rice plants overexpressing OsJAZ8, a repressor of JA signaling, which are

insensitive to JA (Taniguchi et al. 2014). In turn, the application of JAs and damage by

the fall armyworm (Spodoptera frugiperda) elicit the emission of dramatically increased

VOCs in rice leaves (Cheng et al. 2007; Obara et al. 2002; Yuan et al. 2008).

Likewise, in the lima bean, it has been shown that continuous damage by the

chewing caterpillar S. littoralis is required to induce JA biosynthesis; damage leads to

the massive emission of a VOC blend including (E)-β-ocimene and (Z)-3-hexenyl

acetate (Arimura et al. 2008). The expression of an (E)-β-ocimene synthase gene (PlOS)

coincided to JA accumulation induced very locally in mechanically damaged or S.

littoralis-infested leaf area. In contrast, JA does not affect the transcription of

geranyllinalool synthase (PlTPS2) or the production of either geranyllinalool

(non-volatilable) or its degradation product, volatile

(E,E)-4,8,12-trimethyltrideca-1,3,7,11-tetraene (TMTT) in lima beans (Brillada et al.

2013). We recently produced transgenic Lotus japonicas plants that heterogeneously

express PlTPS2 and thus produced geranyllinalool and TMTT. Those transgenic plants

attracted the generalist predatory mite Neoseiulus californicus but not the specialist

Phytoseiulus persimilis (Brillada et al. 2013). Intriguingly, the specialist predator P.

persimilis was attracted only when transgenic plants were infested with spider mites, in

other words, when TMTT was blended with mite-induced, endogenous plant volatiles

[including (Z)-3-hexenyl acetate, (E)-β-ocimene and (E)-4,8-dimethyl-1,3,7-nonatriene]

(Brillada et al. 2013).

For TMTT induction, SA is likely incorporated into the signal. In lima bean

plants infested with spider mites, SA is likely to negatively affect de novo JA synthesis

by blocking the conversion of OPDA, early intermediates of the JA-biosynthetic

pathway, so OPDA might be relevant to the biosynthesis of TMTT (Koch et al. 1999).

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OPDA has been shown to activate a set of genes that specifically responded to OPDA but

not to JAs in Arabidopsis (Taki et al. 2005). Intriguingly, insect glutathione transferase

(GST) is responsible for the isomerization of the JA precursor OPDA (toxic form) to

iso-OPDA (non-toxic form), in the gut of S. littoralis and cotton bollworm (Helicoverpa

armigera) (Dabrowska et al. 2009). Plant OPDA is fated to be partly modulated by

insect GSTs, which play an important role in detoxification, as has been shown for the

detoxification of glucosinolates, the hydroxamic acid,

2,4-dihydroxy-7-methoxy-1,4-benzoxazin-3-one, and furocoumarins (Dabrowska et al.

2009).

SA and JAs are also converted to their volatile forms, methyl salicylate (Park et al.

2007) and cis-jasmone or methyl jasmonate (Farmer and Ryan 1990; Matthes et al.

2010), respectively, and transmitted systemically from damaged parts to undamaged

parts within and between plant(s). Along with those volatile hormones, the major

compounds that are involved in airborne signaling are volatile terpenes, and C5-C10

alkenals and alkanals, including GLVs: the leaf aldehyde (E)-2-hexenal, (Z)-3-hexenal,

the leaf alcohol (Z)-3-hexenol, and (Z)-3-hexenyl acetate, most of which are induced via

JA signaling following herbivore-induced or wound stimuli (Supplementary Table 2).

Those volatile compounds are able to elicit both direct and indirect defense responses in

receivers (Fig. 4). In some cases, receiver plants do not immediately act defensively, but

respond more strongly and more rapidly than non-receiver plants to damage by

herbivores. This phenomenon is known as priming. Since VOCs are emitted by

damaged plants for only a period of days after they are damaged (Arimura et al. 2004),

neighboring plants can receive volatile signals only when emitter plants are damaged, or

slightly later. However, plants do not know how much later the herbivores will arrive,

so they do not know how long they should store the record of volatile signals. Ali et al.

(2013) evaluated the “memory” of plants placed downwind of infested plants. Maize

plants produce and emit a blend of VOCs in response to attack by the specialist

herbivore Mythimna separate (HIPVs: Herbivore-Induced Plant Volatiles) possibly via

JA signaling (Ozawa et al. 2004), and in downwind conspecific plants exposed to those

HIPVs the expression of a defensive gene for Bowman-Birk type trypsin inhibitor (TI)

was not induced by HIPVs. Instead, the HIPVs’ signal was recalled by the plant when it

was later fed on; a “memory” was valid up to 5 days of post-exposure maintenance (Fig.

4). JA signaling is not directly involved in such a “memory” but is involved in the gene

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activation in receiver leaves subsequently stimulated by herbivory. Notably, in the

up-stream sequence of a TI gene, non-methylated cytosine residues were observed in the

genome of plants exposed to HIPVs more frequently than in the genome of plants

exposed to the volatiles of uninfested plants. These findings provide an innovative

explanation for the memory of VOC-mediated habituation for plant defense (Fig. 4). As

described in the preceding section, epigenetic modification of chromatin is currently the

most promising candidate for the molecular mechanism of defense priming (Kim and

Felton 2013). DNA methylation and histone posttranslational modifications induce

changes in chromatin structure, and these changes alter gene transcription (Jaskiewicz et

al. 2011).

In recent years, volatile communication has become a well-studied phenomenon.

This is because the ecological consequences of volatile communication have been

extensively documented and because our understanding of the mechanisms underlying

how leaf cells recognize volatiles and cellular signaling pathways makes the problems

more tractable. For instance, a part of the molecular mechanisms underlying volatile

perception has been recently revealed: after tomato plants perceive the alcoholic GLV

[(Z)-3-hexenol] emitted from infested, neighboring tomato plants, the receiver plants

accumulate the volatile compound in their glycosylated form in the leaf cells (Sugimoto

et al. 2014). The biosynthesis of the glycosylated product, however, appears to occur

independently of JA signaling. Although JA signaling is most likely involved in the

production of VOCs, two questions remain unanswered: whether JA signaling is

involved in induced or primed defense responses after plants take up the volatile

compounds inside cells, and whether the VOCs are chemically modified or their

information is transferred to a cellular defense-related signaling pathway.

Conclusion

Upon induced defense response against biotic and abiotic stresses, the central signaling

relies on a conventional JA-Ile induced, COI1-JAZ signaling pathway in both monocots

and dicots. Significant progress is expanding our understanding that the mode of

elicitation, cross-talk between JA and sub-members of signal molecules (e.g., microbe-

or virus-elicited SA signal) and the induced specialized metabolites and defense/

infochemical products (volatiles and non-volatiles) vary from species to species. In

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other words, more characteristic studies challenging host plant species specificity will

allow us to decipher events that occur up-stream and down-stream of JA signaling,

demonstrating species-specific defensive and infochemical strategies.

Funding

This work was financially supported in part by the Research Fund of Tokyo University

of Science; a Grant-in-Aid for Scientific Research from the Japan Society for the

Promotion of Science to G.A. (No. 24770019); and the Program for Promotion of Basic

and Applied Researches for Innovations in Bio-oriented Industry to K.O.

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Figure legends

Fig. 1 Chemical structures of typical phytoalexins in monocots and dicots

Fig. 2 JA-mediated regulation of specialized metabolites in plants.

The JA-mediated biosynthesis of specialized metabolites (e.g., diterpenoid phytoalexins

in rice) is postulated to be regulated at three different phases. When JA-Ile is first

perceived, SCFCOI1-JAZ-MYC2 receptor complex is most likely to function as a core

module for the initiation of JA signaling. MYC2, a bHLH transcription factor, is broadly

known as the master regulator across plant species. A MAP kinase cascade

(MKK4-MPK3/6) has been solidly confirmed as the pathway leading to

phosphorylation of the WRKY-type transcription factors. During the phase of

transcriptional regulation, various types of transcription factors (e.g., ERF, TGA, and

WRKY) are regulated both positively and negatively. VQ-domain-containing proteins

are likely to play a role in the potential modulation of WRKY activity, as shown in

Arabidopsis, where JAV1 and MKS1 (VQ family proteins) both function negatively in

the pathway. Chromatin remodeling participates in an additional regulation system,

independently from the above two phases. In that system, chromatin decondensation

and histone modification (e.g., acetylation) would contribute to transcriptional

regulation for defense responses.

Fig. 3 Multitrophic interactions, symbioses and mutualisms in ecological system.

Fig. 4 Volatile communications in nature. Volatile organic chemicals (VOCs) emitted

from herbivore-infested leaves mediate both intra-plant and inter-plant communications

for defense responses. The mechanism for the priming of anti-herbivore responses by

volatile communications is in part explained by epigenetic modifications in which a

suite of demethylations are carried out in the promoter region of defense gene(s) in the

receiver leaves (Ali et al. 2013; Sugimoto and Arimura 2013). JA, jasmonic acid; VOCs,

volatile organic chemicals.

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jasmonates induce both defense responses and communication in monocotyledonous and dicotyledonous...

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