hormone defense networking in rice: tales from a different world

TRPLSC-1077; No. of Pages 11

Hormone defense networking in rice:tales from a different worldDavid De Vleesschauwer1, Godelieve Gheysen2, and Monica Ho fte1

1 Laboratory of Phytopathology, Faculty of Bioscience Engineering, Ghent University, Coupure Links 653, 9000 Ghent, Belgium2 Laboratory of Applied Molecular Genetics, Faculty of Bioscience Engineering, Ghent University, Coupure Links 653, 9000 Ghent,

Belgium

Review

Glossary

Biotroph: a pathogen that establishes a long-term feeding relationship with the

living cells of the host, rather than killing the host cells as part of the infection

process.

Hemibiotroph: pathogens that are characterized by an initial period of

biotrophy before switching to a necrotrophic growth stage.

Lodging: bending of the shoot of a plant (shoot lodging) or the entire plant

(root lodging).

Microbe-associated molecular pattern (MAMP): a widely conserved microbial

molecule that is required for microbial fitness. Perception of MAMPs by

membrane-bound pattern-recognition receptors (PRRs) leads to an enhanced

state of immunity, termed MAMP-triggered immunity (MTI).

Necrotroph: a pathogen that kills living host tissues and feeds on the remains.

Necrotrophic pathogens are typically characterized by having a broad host

range and are considered insensitive to resistance gene-triggered plant

defense responses.

Priming: a process resulting in an enhanced capacity to mobilize pathogen- or

elicitor-induced cellular defense responses.

Single nucleotide polymorphisms (SNPs): a DNA sequence variation occurring

Recent advances in plant immunity research underpinthe pivotal role of small-molecule hormones in regulat-ing the plant defense signaling network. Although mostof our understanding comes from studies of dicot plantssuch as Arabidopsis thaliana, new studies in monocotsare providing additional insights into the defense-regulatory role of phytohormones. Here, we reviewthe roles of both classical and more recently identifiedstress hormones in regulating immunity in the modelmonocot rice (Oryza sativa) and highlight the impor-tance of hormone crosstalk in shaping the outcome ofrice–pathogen interactions. We also propose a defensemodel for rice that does not support a dichotomybetween the pathogen lifestyle and the effectivenessof the archetypal defense hormones salicylic acid (SA)and jasmonic acid (JA).

Hormones and plant immunityIn the absence of the adaptive immunity shown by animals,plants fend off pathogen attack through a combination ofconstitutive and inducible defense responses. Many ofthese responses are regulated by cross-communicatingsignal-transduction pathways, within which plant hor-mones fulfill central roles. SA, JA, and ethylene (ET) arethe archetypal defense hormones and their importance inthe hard wiring of the plant innate immune system is welldocumented, particularly in the model plant Arabidopsisthaliana [1,2]. In this plant species, SA is predominantlyassociated with resistance to biotrophic pathogens (seeGlossary), whereas necrotrophic pathogens are usuallydeterred by JA- and ET-driven defenses. Moreover, inter-action between these two types of defense is mostly antag-onistic, suggesting that plant innate immunity follows, inessence, a binary model with SA and JA–ET having oppos-ing influences [1,2].

More recently, other plant hormones, including abscisicacid (ABA), cytokinins (CKs), auxin, brassinosteroids (BRs),and gibberellins (GAs) have also emerged as crucial regu-lators of plant–microbe interactions. Although their signifi-cance is less well studied, there is mounting evidencesuggesting that these hormones influence disease outcomesby feeding into the SA–JA–ET backbone of the immune

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002

Corresponding author: Hofte, M. ([email protected]).

signaling circuitry [3,4]. Such interplay or ‘crosstalk’between individual hormone conduits is thought to enableplants to tailor their inducible defense arsenal to the type ofinvader encountered and to use their limited resources in acost-efficient manner [5].

Although most of our understanding of the plant defensenetwork has come from studies on Arabidopsis, new find-ings from studies in monocots such as rice (O. sativa)(Box 1) are starting to provide additional importantinsights into the immune-regulatory role of phytohor-mones [6]. Rice is not only one of the most important staplefood crops worldwide (Box 1), but is also an excellent modelfor monocots because of its relatively small and fullysequenced genome, its ease of transformation, and theaccumulated wealth of genetic and molecular resources [7].

Here, we survey recent progress in deciphering thedefense-regulatory role of hormones in rice. We first reviewthe main hormone signaling conduits operative in the ricedefense signaling network and then consider crosstalkbetween individual hormone pathways and the role playedby such interplay in molding pathological outcomes. Final-ly, we propose an alternative defense model for rice thatchallenges the commonly accepted binary model. This isnot intended to be a comprehensive review of all hormonemechanisms in rice but rather a discussion that highlights

when a single nucleotide differs between members of a biological species.

Systemic acquired resistance (SAR): the phenomenon in which plants acquire

an enhanced defensive capacity against future pathogen attack as a result of a

primary, limited infection with a necrotizing pathogen.

Thermogenesis: the generation of heat in the mitochondria as a result of

cellular respiration.

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Box 1. A brief introduction to Asia’s favorite staple food and its major pathogens

Consumed daily by more than 3 billion people living in tropical and

subtropical Asia, rice is arguably the world’s most important food

crop and is the staple food of almost 70% of the world’s poor [7]. Most

rice cultivars can be placed within two subspecies: O. sativa ssp.

japonica and O. sativa ssp. indica [98]. Japonica rice is usually grown

in temperate climates and has a short-to-intermediate stature and the

grains are round and sticky when cooked. Indica rice is grown in

tropical climates and has a tall-to-intermediate stature and the grains

are long and do not stick together when cooked. Recent evidence

suggests that japonica rice was first domesticated from a specific

population of Oryza rufipogon (Asian common wild rice) in Southern

China [99]. O. sativa ssp. indica subsequently developed from crosses

between japonica and local wild rice in South (East) Asia [99]. Rice can

be grown in submerged, irrigated, rain-fed lowland and rain-fed

upland environments. Irrigated lowland rice is mainly grown in

tropical Asia, provides 75% of total rice production and uses about

30% of the world’s developed freshwater resources. Aerobic rice, a

new way of growing rice under non-flooded conditions in aerated

soils, is currently gaining popularity in India and Southeast Asia [100].

Diseases have always had a huge impact on rice production,

causing annual yield losses conservatively estimated at 5% [100].

Fungal diseases such as rice blast (caused by M. oryzae), sheath

blight (R. solani), brown spot [C. miyabeanus (sexual stage), also

known as Bipolaris oryzae (asexual stage)], and bacterial blight (X.

oryzae pv. oryzae) are major production constraints on above-ground

plant parts [100]. Below ground, most damage is inflicted by root rot-

causing Pythium species and nematode species such as the root knot

nematodes M. graminicola and H. oryzae. As with many other

microbes, the lifestyles of these pathogens are not readily classified

as purely biotrophic or necrotrophic. For instance, X. oryzae pv.

oryzae is viewed by most as biotrophic but, by the definitions used for

fungi, is probably best classified as hemibiotrophic. R. solani and C.

miyabeanus are often seen as absolute necrotrophs. However,

microscopic examination has revealed that living cells are initially

colonized for a brief period before dead cells appear (D. De

Vleesschauwer, unpublished). Pathogens have previously been

classified [101] as those that are predominantly biotrophic hemibio-

trophs, such as X. oryzae pv. oryzae, M. oryzae, and M. graminicola,

and those that are predominantly necrotrophic hemibiotrophs, such

as H. oryzae, P. graminicola, R. solani, and C. miyabeanus. We

propose that the pathogens discussed in this review would thus line

up along the gradient shown in Figure I.

Meloidogynegraminicola

Xanthomonasoryzae pv.

oryzae

Magnaportheoryzae

Hirshmanniellaoryzae

Pythiumgraminicola

Bipolarisoryzae

Rhizoctoniasolani

Root knotnematode

Leaf blight Blast Root rotnematode

Pythium rootrot

Brownspot

Sheath blight

Upland,rainfed

lowland andaerobic rice

Irrigated andrainfed lowland

Upland andlowland

Irrigatedlowland

Aerobic rice Rainfedlowland

andupland

High-intensivelowland and

upland

Biotrophy Necrotrophy

Prevalence

Disease

Symptom

Pathogen

TRENDS in Plant Science

Figure I. Rice pathogens.

Review Trends in Plant Science xxx xxxx, Vol. xxx, No. x


the similarities and differences between findings in riceand in Arabidopsis based on the most recent publications.For additional background information on rice innate im-munity and the role of plant hormones herein, we refer thereader to a number of excellent recent reviews [6,8–10].

SA: protagonist or fringe player?The phenolic phytohormone SA is well known for its role inthermogenesis, flowering, plant defense signaling, andsystemic acquired resistance (SAR) [11]. However, differ-ent plant species vary greatly in their endogenous SAlevels and in their responsiveness to this hormone. Intobacco (Nicotiana tabacum) and Arabidopsis, basal levelsof SA are low (around 50 ng/g fresh weight), but levels canincrease by two orders of magnitude on pathogen infection.However, healthy rice leaves have high basal levels of SA(8–37 mg/g fresh weight), with no significant local or sys-temic changes on pathogen attack [12]. In tobacco, de novosynthesized SA is rapidly glycosylated into SA b-glucoside,

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whereas in rice most SA is present in the free-acid form[12,13]. Interestingly, this high SA content in rice appearsto function as an antioxidant that protects the plant fromoxidative damage caused by aging, pathogen attack, orabiotic stress [14].

The SA signaling pathway in rice shares downstreamcomponents with the SAR pathway in Arabidopsis [15–19].In SAR, the master regulatory protein NON-EXPRESSOROF PATHOGENESIS-RELATED GENES1 (AtNPR1) tra-nslocates to the nucleus when SA accumulation causeschanges in cellular redox potential [20]. In the nucleus,AtNPR1 interacts with transcription factors of the TGAfamily and activates specific defense genes [21]. A recentstudy showed that AtNPR1 also serves as a receptor for SA[22]. However, contradictory findings suggest that SA mayalso be perceived by the AtNPR1 paralogs AtNPR3 andAtNPR4 [23].

In rice, five NPR1-like genes have been identified,among which OsNPR1 (also called OsNH1) is the closest



AtNPR1 homolog [18]. Overexpression of OsNPR1 in riceconfers high levels of resistance to the leaf blight pathogenXanthomonas oryzae pv. oryzae and the blast fungusMagnaporthe oryzae associated with constitutive accumula-tion of PATHOGENESIS-RELATED (PR) transcripts[15,24]. By contrast, in Arabidopsis overexpressing AtNPR1,defense responses are not activated until induced by chemi-cal or pathogen treatment [25].

Despite its high endogenous SA levels, rice is not unre-sponsive to SA, but this is plant age dependent. Exoge-nously supplied SA can induce resistance to M. oryzae inadult plants (eight-leaf stage) but not in young plants (four-leaf stage) [26]. Plant activators such as probenazole andbenzothiadiazole that act either upstream or downstreamof SA can also induce plant defense responses in rice and, inthe case of benzothiadiazole, trigger protection against afairly broad range of pathogens with different lifestylesand modes of infection (i.e., Pythium graminicola, X. oryzaepv. oryzae, M. oryzae, and H. oryzae) (Box 1) [27–31].

The transcription factor OsWRKY45 is essential forplant activator-induced resistance. Chemical-induced re-sistance to X. oryzae pv. oryzae and M. oryzae is compro-mised in OsWRKY45 knockdown rice, whereas OsWRKY45overexpressing rice plants show an outstanding resistanceto both of these pathogens, but not to the sheath blightpathogen Rhizoctonia solani [32–34]. It has recently beenshown that OsWRKY45 is constantly degraded by thenuclear ubiquitin proteasome system (UPS) in the absenceof defense signals. On benzothiadiazole treatment orpathogen infection, OsWRKY45 accumulation exceedsdegradation, enabling OsWRKY45 to bind to target pro-moters, where transcriptional activity of OsWRKY45 ispresumably enhanced by UPS-mediated turnover [35].Interestingly, in Arabidopsis, AtNPR1 is regulated bythe UPS in a similar way [36]. However, in rice there isno evidence that OsNPR1 undergoes UPS-dependent deg-radation [35].

Together, these results highlight the unique complexitiesassociated with SA signal transduction in rice. Most notably,the rice SA conduit branches into OsNPR1- andOsWRKY45-dependent pathways that play complementaryroles in plant defense. Almost half of all benzothiadiazole-responsive genes and two-thirds of all benzothiadiazole-downregulated genes are dependent on OsNPR1 [19]. Thesedownregulated genes include several genes involved inphotosynthesis and protein synthesis, suggesting a functionfor OsNPR1 in relocating energy and resources from house-keeping cellular activities to defense reactions [32,35].Meanwhile, most genes upregulated by benzothiadiazoleare regulated by OsWRKY45 and many are directly associ-ated with plant defense, including various PR genes [34,35].This strikingly contrasts with the situation in Arabidopsis,where nearly all (>99%) benzothiadiazole-responsive genesare AtNPR1 dependent [37].

JA: a central node in the rice defense signaling networkJA and its metabolites, collectively known as jasmonates(JAs), are crucial lipid-derived regulators that fulfill essen-tial roles in plant defense and developmental processes.According to the classic defense model, JA is predominant-ly effective against necrotrophic pathogens and insect

herbivores and, in some instances, antagonizes SA-medi-ated biotroph resistance [2].

In rice, a strikingly different mechanism seems to oper-ate, with reports implicating JA in resistance againstpathogens with diverse lifestyles and infection strategies.Perhaps most intriguingly, studies with JA-modifiedplants have revealed that JA is a powerful activator ofresistance to the (hemi)biotrophs M. oryzae and X. oryzaepv. oryzae [38–43]. Yet, similar to its role in dicots, JA hasalso been firmly implicated in immunity to the necrotrophR. solani. JA application reduces disease development inthis interaction and intact JA biosynthesis was found to beindispensable for sheath blight resistance induced by thewater-soluble B vitamin riboflavin [44]. Moreover, ectopicexpression of the pathogen-inducible transcription factorOsWRKY30 enhances resistance to sheath blight concomi-tant with an increase in JA accumulation and the expres-sion of JA-responsive PR genes, further connecting JAsignaling to necrotroph resistance [45]. A fast-growingnumber of studies have also affirmed the crucial role ofrice JA action in resistance to nematode pathogens andinsect herbivores [30,46–51].

The abovementioned studies clearly indicate that theeffectiveness of the JA pathway in rice cannot be predictedbased on the lifestyle of the invading pathogen. Further-more, given the effectiveness and broad-spectrum nature ofJA-induced resistance, it is tempting to speculate that, inrice, JA might function as an endogenous priming agentthat amplifies pathogen-induced defense reactions irre-spective of the parasitic habits of the pathogen. In supportof this notion, JA synthesis has recently been identified asa common response to microbe-associated molecular pattern(MAMP) perception in cultured rice cells [52]. Moreover,earlier reports implicated JA in boosting defense-geneexpression and disease resistance induced by aging, me-chanical wounding, and plant activators [53–56]. Despitethe attractiveness of this idea, further experimentation isneeded to validate this ‘priming’ hypothesis and unequivo-cally delineate the role of JA and its position within the ricedefense signaling network.

ETET, one of the three classical defense hormones, is a majorcomponent of the hormonal blend that is released onpathogen attack. Although there are exceptions, it is wide-ly accepted that ET cooperates with JA in mounting im-munity against necrotrophic pathogens [2,3]. However, wehave shown that ET is also a powerful suppressor ofresistance to the necrotrophic brown spot fungus Cochlio-bolus miyabeanus [57]. Hormone measurements and tran-script profiling revealed that the ET pathway was stronglyactivated in susceptible plants but not in resistant plants,suggesting that ET acts as a virulence factor for C. miya-beanus [57]. Similarly, another study has reported thatincreased ET levels confer higher susceptibility to X. oryzaepv. oryzae [58]. However, ET can also act positively on riceimmunity, drawing on evidence from ET-overproducingrice transformants that show increased resistance to boththe hemibiotroph M. oryzae and the necrotroph R. solani[59]. Together with the opposite effects of ET pretreatmenton blast, leaf blight, and brown spot development, these

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Box 2. Semi-dwarf varieties and GA: revisiting the green

revolution

Semi-dwarf varieties of rice that carry a mutation in the Semi-Dwarf

(SD)-1 locus on chromosome 1 were developed in the 1960s. This

mutation originated from the Taiwanese short, heavy-tillering indica

variety Dee-geo-woo-gen, which was used to produce Taichung

Native 1 (TN-1) in Taiwan and later was crossed with the Indonesian

good-tasting, tall indica variety Peta at the International Rice

Research Institute (IRRI), resulting in the IR8 variety [102,103]. The

semi-dwarf IR8 variety carrying the sd-1 allele from Dee-geo-woo-

gen produced record yields throughout Asia and was called ‘miracle

rice’ because it responded well to nitrogen fertilization without

lodging and produced twice the amount of rice grains that tall

varieties produced. Thus began the rice ‘green revolution’. TN-1 and

IR8 were subsequently used in many breeding programs to develop

new, high-yield semi-dwarf plant types with better pest and disease

resistance and better grain quality [103].

In 2002, three research groups independently reported that sd-1

rice contains a defective GA20 oxidase gene [102,104,105]. GA20

oxidase is a key enzyme that catalyzes the three steps

GA53!GA44!GA19!GA20 in the biosynthesis of GAs in higher

plants. There are four GA20ox-like genes in the rice genome and

semi-dwarf rice appears to be defective in GA20ox-2. The sd-1 allele

of Dee-geo-woo-gen and IR8 contains a 383 bp deletion in GA20ox-2

[104,105]. Semi-dwarf varieties of rice that have been developed

independently in Japan and the USA were found to carry different

alleles of the same recessive sd-1 gene [102]. Recently, it was

reported that the GA20ox-2 gene was also involved in the early

steps of rice domestication [106]. The SD1 amino acid sequence

carries two non-synonymous single nucleotide polymorphisms in

the first exon [glutamate (E) and glycine (G)] and third exon

[glutamine (Q) and arginine (R)]. All tested accessions of the Asian

wild rice O. rufipogon and most O. sativa ssp. indica accessions

contain SD1-GR and 16 diverse japonica landraces (including both

tropical and temperate japonica) carry the SD1-EQ allele, which is

linked with shorter culm length and low GA biosynthetic activity.

These results suggest that ancient humans had already used the

green revolution gene [106].



data thus favor a scenario in which ET acts as a two-faceddefense regulator in rice, the effect of which may dependnot only on pathogen lifestyle and overall infection biology,but also on specialized features of each interaction.

ABACompared with SA, JA, and ET, the role played by the‘abiotic stress’ hormone ABA in plant innate immunity isless well understood and even contentious. Although bothpositive and negative effects of ABA on disease resistancehave been reported, ABA predominantly behaves as anegative regulator of immunity [60,61]. In rice, exogenousABA can suppress basal immunity to both X. oryzae pv.oryzae and M. oryzae. Moreover, successful infection withthese pathogens is commonly associated with extensivereprogramming of ABA-response and -biosynthesis genes,suggesting that these pathogens hijack the rice ABA path-way to cause disease [29,62–64]. Interestingly, ABA alsoantagonizes defense against the migratory root rot nema-tode Hirschmanniella oryzae [30] and apparently contra-dictory data implicate ABA as a positive signal in theactivation of resistance against the necrotroph C. miya-beanus [57]. Like ET, ABA therefore appears to play anambiguous role in the rice immune signaling network,acting as either a positive or a negative regulator of diseaseresistance by interfering at multiple levels with biotic andabiotic stress signaling cascades.

New kids in town: ‘developmental hormones’ do ricedefenseUnlike the classical stress hormones ABA, SA, ET, and JA,the GAs, auxins, BRs, and CKs were historically mainlystudied for their role in plant growth and development andonly recently emerged as key determinants in the outcomeof plant–pathogen interactions. In the following sections,we briefly highlight recent studies that suggest roles forthese ‘developmental hormones’ in governing rice defenseresponses.

GAs

GAs are diterpenoid plant hormones that were originallyidentified from the fungal pathogen Gibberella fujikuroi,which causes the ‘foolish seedling’ disease bakanae inrice [65]. The GA pathway holds great agricultural impor-tance and manipulation of this pathway has been one ofthe driving factors behind the green revolution (Box 2).Current concepts suggest that GA promotes plant growthby regulating the degradation of a class of nuclear growth-repressing proteins called DELLAs. A study using Arabi-dopsis mutants lacking four of the five DELLA proteinsproposed that DELLAs promote resistance to necrotrophsand susceptibility to biotrophs, partly by modulating theSA:JA balance in favor of JA [66]. Accordingly, pretreat-ment with GA restricts JA signaling, resulting in enhancedSA signaling and biotroph resistance [66].

In rice, topical GA application has been shown to lowerresistance to the (hemi)biotrophs M. oryzae and X. oryzaepv. oryzae [67,68]. Similarly, transgenic rice overexpres-sing a GA-deactivating enzyme, designated ELONGATEDUPPERMOST INTERNODE (EUI), accumulated lowlevels of GA and SA and showed enhanced resistance to

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M. oryzae and X. oryzae pv. oryzae, whereas loss-of-functionmutations in EUI were more vulnerable to these pathogens[68]. These phenotypes and additional analyses of GA-perception and -biosynthesis mutants [67,69] indicate thatGA impairs (hemi)biotroph resistance in rice.

Although the mechanism of GA action on rice innateimmunity remains poorly understood, several studiespoint to some possibilities, with GA being increasinglylinked to suppression of defense-related gene expressionand phytoalexin biosynthesis and to the modulation of SAand JA levels [67–69]. In addition, bioassays with mutantlines deficient in GA biosynthesis, perception, or signalingsuggest that SLENDER RICE 1 (SLR1), the onlyDELLA protein in rice, plays a prominent role. SLR1-overaccumulating or gain-of-function mutants show in-creased susceptibility to the necrotroph P. graminicola[28] but enhanced resistance to the (hemi)biotrophs X.oryzae pv. oryzae and M. oryzae [69]. In agreement with JApositively regulating (hemi)biotroph resistance in rice (seeabove), SLR1 serves as a main target of JA-mediatedgrowth inhibition and immunity and is required for ex-pression of JA-inducible rice genes [70]. Opposite to theArabidopsis DELLAs, rice SLR1 thus seems to promotesusceptibility to the necrotroph P. graminicola and resis-tance to the (hemi)biotrophs X. oryzae pv. oryzae andM. oryzae. Resistance to (hemi)biotrophic pathogens is



at least in part promoted by amplifying JA-dependentdefenses. Whether SLR1 is also involved in susceptibilityto other necrotrophic rice pathogens, such as R. solani andC. miyabeanus, remains to be elucidated.

Auxins

Like GAs, auxins control nearly every aspect of plantgrowth and development. Consistent with auxins promot-ing biotroph susceptibility in dicots [71], work from severallaboratories has revealed indole acetic acid (IAA), the mainauxin in rice, to be a virulence factor of the (hemi)biotrophsM. oryzae and X. oryzae pv. oryzae. Like many othermicrobes, these pathogens produce and secrete IAA them-selves and also increase IAA biosynthesis and/or signalingon infection [72]. Accordingly, rice transformants withreduced levels of free IAA owing to increased expressionof auxin-conjugating GRETCHEN HAGEN 3 (GH3) pro-teins show enhanced resistance to M. oryzae and X. oryzaepv. oryzae [72–74]. However, unlike in Arabidopsis whereauxin is believed to repress SA levels and signaling, auxin-induced biotroph susceptibility in rice is not associatedwith changes in SA or JA signaling. Instead, it has beenproposed that pathogen-induced auxin triggers the expres-sion of cell wall-loosening expansins, thereby facilitatingpathogen entry and allowing increased nutrient leakage[73]. It remains to be verified whether auxin is also in-volved in promoting resistance to necrotrophic rice patho-gens, as was previously shown in Arabidopsis [75].

BRs

BRs are a unique class of growth-promoting steroid hor-mones that have also emerged as modulators of plantimmunity. In 2003, a study [31] showed that BR treatmentof tobacco and rice induces resistance against variousfungal, viral, and bacterial pathogens exhibiting distinctparasitic habits. This increase in resistance was indepen-dent of SA accumulation and PR gene expression, suggest-ing that BRs regulate plant immunity through an SA-independent pathway [31]. However, recent work by ourgroup and others points to a more complex scenario [21,67–70]. Working with the root pathogen P. graminicola, wefound that activation of BR signaling renders rice hyper-susceptible to pathogen attack. Interestingly, P. gramini-cola appears to co-opt the rice BR machinery to act as adecoy to suppress SA- and GA-mediated defenses thatnormally limit P. graminicola growth [28]. BR has alsobeen shown to disable effective JA-dependent defensesagainst the rice root knot nematode Meloidogyne grami-nicola [76]. Together with work in Arabidopsis showing theability of BR to impede MAMP-triggered immunity [77–79],these findings highlight the importance of BR homeostasisin the establishment of plant immunity.

Cytokinins

Cytokinins are one of the latest developmental hormonesto be linked to plant immunity. In Arabidopsis, high con-centrations of CK increased SA-mediated resistance tobiotrophic pathogens, whereas lower concentrations ofCK resulted in increased biotroph susceptibility [80,81].Different results were obtained in a study investigating therole of CK in rice resistance to M. oryzae [82]. In this study,

pretreatment with low levels of CK had no significant effecton disease susceptibility, whereas higher doses increasedblast incidence. However, in the case of X. oryzae pv. oryzaeinoculation, increased susceptibility was observed in re-sponse to a wide range of CK concentrations (J. Xu et al.,unpublished). Analysis of the underlying mechanisms sug-gests that CK signaling can cascade to either the benefit orthe detriment of the plant. Indeed, whereas the observa-tions that M. oryzae secretes CK in vitro and elevates CKlevels in planta point to a disease-promoting effect, gene-expression studies have also revealed CK to act synergis-tically with SA to activate PR gene expression, thus con-tributing to host immunity [82].

Collaboration and antagonism: crosstalk in rice defensesignalingSA–JA crosstalk

One of the best-studied examples of defense-related signalcrosstalk is the interaction between the SA and JA re-sponse pathways. Although there is evidence for bothpositive and negative SA–JA interplay in many plantspecies, antagonistic interactions tend to prevail [83]. Ac-cumulating evidence suggests that this SA–JA antagonismis also conserved in rice. For instance, SA inhibits JA-induced activation of both RSOsPR10, which encodes aroot-specific homolog of the rice PR protein OsPR10, andthe ET response factor gene 1 (OsERF1), a proposed regu-lator of RSOsPR10 [84]. Furthermore, during the earlyresponse to wounding, JA levels rise whereas SA levelsdecrease, suggesting negative crosstalk in the direction ofJA damping SA action [85].

Over the past few years, several regulatory proteinsinvolved in SA–JA crosstalk have been identified, keyamong which is NPR1 (see above). As in Arabidopsis,overexpression of OsNPR1 is characterized by strong acti-vation of SA-responsive genes and concomitant suppres-sion of JA marker genes [18]. Moreover, OsNPR1 antisenserice plants show elevated JA levels and increased expres-sion of JA biosynthesis genes on insect infestation [86].Accordingly, overexpression of OsNPR1 not only confersrobust resistance against M. oryzae and X. oryzae pv. oryzae[15,18,19,24], but it also renders rice more susceptible toherbivorous insects [18]. In a similar vein, rice overexpres-sing AtNPR1 shows both enhanced pathogen resistanceand reduced tolerance to abiotic stress [16,17,87]. Together,these studies favor a scenario wherein OsNPR1 positivelyregulates SA-dependent pathogen resistance in rice whilesuppressing JA-mediated defenses to herbivorous insectsand abiotic stress tolerance.

A role in SA–JA crosstalk has also been suggested forOsWRKY13. Functioning upstream of OsNPR1, this tran-scription factor acts as an activator of SA-mediateddefenses and a repressor of JA responses [88–90].

Although it is evident from the examples above thatrice SA and JA pathways act antagonistically, positiveinteractions have also been reported. For instance, acti-vation of JA biosynthesis in mutant plants deficient in thehydroperoxide lyase OsHPL3 coincides with increases inSA levels and enhanced expression of SA-responsive PRgenes [46,49]. Synchronously augmented SA and JAlevels have also been observed in rice plants silenced

5



for the phospholipase D genes OsPLDa3 and OsPLDa4[91]. Moreover, recent microarray experiments haverevealed that over 50% of all benzothiadiazole or SA-upregulated rice genes are also activated by JA [42,92].These genes include master defense regulators such asOsWRKY45 as well as OsPR1a, the closest rice homolog ofthe archetypal SA marker PR1. Together, these findingsbring a new twist to the classical crosstalk model andsuggest that, although hyperactivation of either JA or theSA pathway has the ability to override the other, bothhormones may feed into a common rice defense systemthat is effective against both biotrophic and necrotrophicpathogens (Figure 1).

ABA–SA, ABA–ET, and ABA–JA crosstalk

In Arabidopsis, ABA has been repeatedly shown to para-lyze plant defenses by antagonizing the SA pathway [60].In a similar manner, it has been proposed that ABAconditions susceptibility to X. oryzae pv. oryzae and M.oryzae by interfering upstream of OsWRKY45 andOsNPR1 [29,64]. ABA can also interact intimately withthe ET signaling pathway. Lines silenced for the ABA-inducible mitogen-activated protein kinase OsMPK6 (pre-viously also known as OsMPK5) overproduce ET and showenhanced resistance to M. oryzae; however, they are alsohypersensitive to abiotic stresses and C. miyabeanus[57,93,94]. By contrast, inactivation of the central ET-signal transducer OsEIN2 triggers increased resistanceto C. miyabeanus as well as hypersensitivity to M. oryzae,ABA, and abiotic stress [57,93]. Together, these findingssuggest that OsMPK6 and OsEIN2 function as molecularswitches between the rice ET and ABA pathways, withcorresponding trade-offs between C. miyabeanus defenseand abiotic stress tolerance on the one hand and resistanceto M. oryzae on the other.

Interestingly, OsMPK6 is also implicated in JA-mediated defense against chewing herbivores, suggest-ing positive crosstalk in the direction of ABA boosting JAaction [95]. By contrast, ABA interacts antagonisticallywith the JA, ET, and SA pathways, which are requiredfor resistance against the migratory nematode H. oryzae[30]. This suggests that the nature of interactions be-tween these pathways can be complex and also attackerdependent.

JA–GA, GA–BR, BR–SA, and BR–JA crosstalk

On pathogen attack, plants rapidly shift cellular resourcesfrom normal growth processes to defense responses. Evi-dence from studies in dicots suggests that this growthversus defense conflict is regulated in part through antag-onism between the ‘growth hormone’ GA and the ‘defensehormone’ JA [70,96]. Studies with mutants deficient in theputative rice JA receptor CORONATINE INSENSITIVE 1(OsCOI) indicate that this JA–GA antagonism is alsoconserved in rice [70]. Furthermore, the observation thatJA attenuates GA-induced degradation of the DELLArepressor SLR1 provides a mechanistic framework forhow JA suppresses GA action by stabilizing a centralsuppressor of GA signaling [70]. A similar mechanismunderpins BR inhibition of GA signaling in rice roots[28]. Finally, BRs are also known to antagonize SA and

6

JA pathways by interfering downstream and upstream ofhormone synthesis, respectively [28,76].

ModelContrary to the binary SA versus JA–ET defense model forArabidopsis, disease resistance in rice appears to be con-trolled by a more complicated signaling network that doesnot support a dichotomy between the effectiveness of theSA, JA, and ET pathways and the lifestyle of a givenpathogen (Figure 2). Most intriguingly, SA and JA promoteresistance against both (hemi)biotrophic and necrotrophicpathogens, whereas ET can have either positive or nega-tive impacts on disease resistance that are seeminglyindependent of the pathogen’s parasitic habits.

The effect of developmental hormones is equally com-plex. CK is able to increase SA-mediated defenses, butpromotes susceptibility to X. oryzae pv. oryzae, whereas GAenhances (hemi)biotroph susceptibility at least in part bysuppressing JA-mediated defenses. By contrast, auxinpromotes (hemi)biotroph susceptibility in a SA- and JA-independent manner.

Analogous to its role in dicots, the abiotic stress hor-mone ABA negatively interacts with the SA, JA, and ETpathways and, usually, suppresses rice disease resistance.However, in some instances, such antagonistic crosstalkmay also positively influence disease outcomes, as wasreported for the necrotrophic brown spot fungus C. miya-beanus.

Finally, BR promotes (hemi)biotroph resistancethrough an as yet to be defined mechanism but suppressesdefense in root tissues via antagonism with SA, JA, or GA.

Concluding remarksFueled by the advent of large-scale ‘omics’ technologies andthe burgeoning field of computational biology, the past fewyears have witnessed paradigm-shifting advances in ourunderstanding of hormone defense networking in the dicotmodel Arabidopsis. However, as illustrated throughoutthis review, the conceptual framework emerging fromthese studies does not always translate to other plantpathosystems. The unique complexities associated withhormone defense signaling in rice underscore the impor-tance of using alternative plant model systems and call fora re-evaluation of overly generalized defense models.

Despite recent progress, our understanding of how hor-mones influence pathological outcomes in rice is still lag-ging far behind that of Arabidopsis and other dicots. Forinstance, the role and function of the classical defensehormones SA and JA remain unclear, there is little infor-mation available about rice interactions with nematodes,insects, and viruses, and there is still much to be learnedabout the regulatory nodes connecting individual hormonepathways in rice (Box 3). Moreover, few studies haveconsidered the involvement of a range of hormones inany one rice–pathogen interaction and none addressesthe kinetics and signature of the blend of hormones pro-duced on pathogen attack. In addition, there is a paucity ofknowledge regarding how rice pathogen effectors confervirulence by tapping into the host hormone machinery.Deepening our knowledge in this area is of crucial impor-tance if we are to harness the knowledge of pathogen

Biotrophy Hemibiotrophy

Common defense systemPR gene expression

WRKY13

SA

JA

BTHTiadinil

SA-dependentresponses

JA-dependentresponses

Probenazole

OsSSI2

26S proteasome

Ubiqui�n(Ub)

Ubiqui�n(Ub)

OsSGT1

OsJAZs

OsJAZs

SAG

Pathogen infec�on

R. solaniH. oryzaeXoo M. oryzaeP. graminicola

Necrotroph Necrotroph

UbUb

UbUb

Ub

Δ redox

NPR1cytosolic

NPR1nuclear

NuclearWRKY45

WRKY45

SCFOsCOI1

SAsynthesis

JAsynthesis


Figure 1. Salicylic acid (SA) and jasmonic acid (JA) signaling pathways in rice. In contrast to dicots, where basal SA levels are low, rice plants accumulate high levels of

endogenous SA that do not change significantly on pathogen attack [12]. However, pathogen inoculation does activate the SA signal-transduction cascade, which branches

into OsNPR1- and OsWRKY45-dependent pathways [19,32,33]. OsWRKY45 undergoes ubiquitin proteasome (UPS)-dependent degradation in the nucleus. This UPS-

dependent turnover plays a dual role in the rice defense program by, on the one hand, preventing spurious defense activation in the absence of pathogen attack and, on the

other hand, enhancing OsWRKY45 transcriptional activity [35]. By contrast, OsNPR1 is not stabilized by proteasome inhibition under uninfected conditions, but is controlled

by the upstream regulator OsWRKY13 [35,88,89]. Following pathogen infection, SA-induced redox changes reduce the intermolecular disulfide bonds that normally keep

OsNPR1 in an inactive oligomeric state in the cytosol [18]. This reduction in turn releases monomeric OsNPR1, which is translocated to the nucleus where it interacts with

TGA transcription factors to activate defense-gene expression [15–18]. Cytosolic, but not nuclear, OsNPR1 also functions to suppress JA responses through a mechanism

that remains to be defined [18]. As in dicots, rice JA is most likely to be perceived by the F-box protein OsCOI1 and signals through UPS-mediated removal of jasmonate

ZIM-domain (OsJAZ) proteins that act as transcriptional repressors of JA responses [42,70,107]. Increased JA levels resulting from either pathogen attack or mechanical

wounding inhibit SA biosynthesis, resulting in suppression of SA signaling [40,85]. Despite this reciprocal antagonism, SA and JA are hypothesized to feed into a common

defense system that is presumably regulated by OsWRKY45 and controls the expression of a large majority of rice PR genes. Activation of SA, JA, and SA–JA coregulated

defenses all add to establishing resistance against various pathogens exhibiting different lifestyles and infection strategies. Probenazole is a plant activator that acts

upstream of SA, whereas benzothiadiazole and tiadinil function downstream of SA [34]. OsSSI2, a stearoyl-acyl carrier-protein desaturase, negatively regulates the SA

pathway [108], whereas SA glucosyltransferase (OsSGT1) promotes probenazole-inducible resistance by catalyzing the conversion of free SA into SA-O-b-glucoside (SAG)

[109]. Abbreviation: Xoo, Xanthomonas oryzae pv. oryzae. Positive and negative regulatory actions are indicated by arrows and lines with bars, respectively.



7

Biotrophresistance

(Ps, Ha, Eo)

Defense signaling

Pathogen signal

Arabidopsis thaliana Oryza sa�va

ABA

SA

GA

CK

Auxin

BR

JA/ET

+

Defense signaling

ABA

SA

Auxin

BR

JA

ET

Pathogen signal

Abio�cstress

tolerance

Nec

rotr

oph

res

ista

nce

Rs

Cm

(Hem

i)bio

trop

h re

sist

ance

Mo

XooPg

GA

CK+ _

_

_

+

+ _

Abio�cstress

tolerance

Necrotrophresistance(Bc, Ab, Pi,

Ec)


Figure 2. Model depicting probable hormone defense networking in the model plants Arabidopsis thaliana (left) and Oryza sativa (right). Note that although the role of

salicylic acid (SA) in biotroph resistance and the role of jasmonic acid (JA) and ethylene (ET) in necrotroph resistance is clear in many Arabidopsis–pathogen interactions,

there are also numerous exceptions to this rule [1]. Positive and negative regulatory actions are indicated by arrows and lines with bars, respectively. Plus signs indicate

synergistic signal interactions and minus signs refer to antagonistic crosstalk. Hormone abbreviations: ABA, abscisic acid; BR, brassinosteroid; CK, cytokinin; ET, ethylene;

GA, gibberellic acid; JA, jasmonic acid; SA, salicylic acid. Pathogen abbreviations: Ab, Alternaria brassicicola; Bc, Botrytis cinerea; Cm, Cochliobolus miyabeanus; Ec,

Erwinia carotovora; Eo, Erysiphe orontii; Ha, Hyaloperonospora arabidopsidis; Mo, Magnaporthe oryzae; Pg, Pythium graminicola; Pi, Pythium irregulare; Ps, Pseudomonas

syringae; Rs, Rhizoctonia solani; Xoo, Xanthomonas oryzae pv. oryzae. The Arabidopsis model is adapted from [4].

Box 3. Summary points and outstanding questions

Summary points

� Rice is endowed with high basal levels of free SA that are only

weakly responsive to pathogen attack and act as a preformed

antioxidant. Downstream of SA biosynthesis, the rice SA conduit

branches into OsNPR1- and OsWRKY45-dependent pathways that

play complementary roles in defense.

� Although hyperactivation of one can attenuate the other, rice SA

and JA signaling pathways are likely to feed into a common

defense system that is effective against both biotrophic and

necrotrophic pathogens.

� ET plays an ambiguous role in the rice defense response, acting as

either a positive or a negative regulator of disease resistance

independent of the lifestyle and mode of infection of the pathogen.

� Contrary to Arabidopsis, rice has only one DELLA protein, SLR1,

which conditions resistance to (hemi)biotrophic pathogens and

susceptibility to the necrotroph P. graminicola.

� Auxin induces susceptibility to (hemi)biotrophic rice pathogens in

a SA- and JA-independent fashion, whereas cytokinins enhance

SA-dependent rice immunity.

� BRs and ABA either promote or suppress rice innate immunity

depending on the lifestyle of the pathogen and the type of plant

tissue.

Outstanding questions

� How are SA and JA perceived in rice, how do their signaling

pathways interact at the molecular level, and what is the relative

contribution of each hormone to the rice defense response?

� What are the spatiotemporal dynamics of specific hormones during

a given rice–pathogen interaction? How do rice pathogens perturb

hormonal crosstalk to interfere with plant immune responses?

� What is the role of hormones other than SA and JA in

orchestrating the defense of rice against nematodes, viral

pathogens, and insect herbivores?

� To what extent do abiotic stresses impact on rice defense

signaling interactions and how do rice plants integrate and fine-

tune responses to simultaneous or successive stressors?



8

virulence strategies that interfere with hormone-mediatedimmunity for engineering durable disease resistance inrice [97]. Finally, there is a clear need for studies with riceplants that are simultaneously subjected to different bioticand/or abiotic stresses. Because combined biotic and abi-otic stresses take an estimated 30–60% bite out of potentialglobal rice yield, elucidating the cellular and molecularmechanisms underpinning hormone-mediated stresscrosstalk remains an important goal in the field [6].

AcknowledgmentsThe authors apologize to colleagues whose work could not be cited owingto space limitations. They thank Rita Sharma, Kris Audenaert, andCharissa Verbeeck for critical comments. They also thank Kamrun Naharand Lander Bauters for providing pictures of nematode diseasesymptoms. This work was supported by grants from the Special ResearchFund of Ghent University (GOA 01GB3013) and the Research FoundationFlanders (FWO, project G.0833.12N) and a FWO postdoctoral fellowshipto D.D.V.

References1 Pieterse, C.M.J. et al. (2009) Networking by small-molecule hormones

in plant immunity. Nat. Chem. Biol. 5, 308–3162 Robert-Seilaniantz, A. et al. (2011) Hormone crosstalk in plant disease

and defense: more than just jasmonate-salicylate antagonism. Annu.Rev. Phytopathol. 49, 26.21–26.27

3 Pieterse, C.M.J. et al. (2012) Hormonal modulation of plant immunity.Annu. Rev. Cell Dev. Biol. 28, 489–521

4 Robert-Seilaniantz, A. et al. (2007) Pathological hormone imbalances.Curr. Opin. Plant Biol. 10, 372–379

5 Verhage, A. et al. (2010) Plant immunity: It’s the hormones talking,but what do they say? Plant Physiol. 154, 536–540

6 Sharma, R. et al. (2013) Recent advances in dissecting stress-regulatory crosstalk in rice. Mol. Plant 6, 250–260

http://refhub.elsevier.com/S1360-1385(13)00129-5/sbref0005















7 Jung, K.H. et al. (2008) Towards a better bowl of rice: assigningfunction to tens of thousands of rice genes. Nat. Rev. Genet. 9, 91–101

8 Chen, X.W. and Ronald, P.C. (2011) Innate immunity in rice. TrendsPlant Sci. 16, 451–459

9 Liu, W. et al. (2013) Recent progress in understanding PAMP- andeffector-triggered immunity against the rice blast fungusMagnaporthe oryzae. Mol. Plant 6, 605–620

10 Yang, D.L. et al. (2013) Roles of plant hormones and their interplay inrice immunity. Mol. Plant 6, 675–685

11 Vlot, A.C. et al. (2009) Salicylic acid, a multifaceted hormone tocombat disease. Annu. Rev. Phytopathol. 47, 177–206

12 Silverman, P. et al. (1995) Salicylic acid in rice: biosynthesis,conjugation, and possible role. Plant Physiol. 108, 633–639

13 Enyedi, A.J. et al. (1992) Localization, conjugation, and function ofsalicylic acid in tobacco during the hypersensitive reaction to tobaccomosaic virus. Proc. Natl. Acad. Sci. U.S.A. 89, 2480–2484

14 Yang, Y.N. et al. (2004) Endogenous salicylic acid protects rice plantsfrom oxidative damage caused by aging as well as biotic and abioticstress. Plant J. 40, 909–919

15 Chern, M. et al. (2005) Overexpression of a rice NPR1 homolog leads toconstitutive activation of defense response and hypersensitivity tolight. Mol. Plant Microbe Interact. 18, 511–520

16 Chern, M.S. et al. (2001) Evidence for a disease-resistance pathway inrice similar to the NPR1-mediated signaling pathway in Arabidopsis.Plant J. 27, 101–113

17 Fitzgerald, H.A. et al. (2004) Overexpression of (At)NPR1 in rice leadsto a BTH- and environment-induced lesion-mimic/cell deathphenotype. Mol. Plant Microbe Interact. 17, 140–151

18 Yuan, Y. et al. (2007) Functional analysis of rice NPR1-like genesreveals that OsNPR1/NH1 is the rice orthologue conferring diseaseresistance with enhanced herbivore susceptibility. Plant Biotechnol.J. 5, 313–324

19 Sugano, S. et al. (2010) Role of OsNPR1 in rice defense program asrevealed by genomewide expression analysis. Plant Mol. Biol. 74,549–562

20 An, C. and Mou, Z. (2011) Salicylic acid and its function in plantimmunity. J. Integr. Plant Biol. 53, 412–428

21 Despres, C. et al. (2003) The Arabidopsis NPR1 disease resistanceprotein is a novel cofactor that confers redox regulation of DNAbinding activity to the basic domain/leucine zipper transcriptionfactor TGA1. Plant Cell 15, 2181–2191

22 Wu, Y. et al. (2012) The Arabidopsis NPR1 protein is a receptor for theplant defense hormone salicylic acid. Cell Rep. 1, 639–647

23 Fu, Z.Q. et al. (2012) NPR3 and NPR4 are receptors for the immunesignal salicylic acid in plants. Nature 486, 228–232

24 Feng, J.X. et al. (2011) Involvement of OsNPR1/NH1 in rice basalresistance to blast fungus Magnaporthe oryzae. Eur. J. Plant Pathol.131, 221–235

25 Cao, H. et al. (1998) Generation of broad-spectrum disease resistanceby overexpression of an essential regulatory gene in systemic acquiredresistance. Proc. Natl. Acad. Sci. U.S.A. 95, 6531–6536

26 Iwai, T. et al. (2007) Probenazole-induced accumulation of salicylicacid confers resistance to Magnaporthe grisea in adult rice plants.Plant Cell Physiol. 48, 915–924

27 De Vleesschauwer, D. et al. (2008) Pseudomonas fluorescensWCS374r-induced systemic resistance in rice againstMagnaporthe oryzae is based on pseudobactin-mediated primingfor a salicylic acid-repressible multifaceted defense response.Plant Physiol. 148, 1996–2012

28 De Vleesschauwer, D. et al. (2012) Brassinosteroids antagonizegibberellin- and salicylate-mediated root immunity in rice. PlantPhysiol. 158, 1833–1846

29 Jiang, C-J. et al. (2010) Abscisic acid interacts antagonistically withsalicylic acid signaling pathway in rice–Magnaporthe griseainteraction. Mol. Plant Microbe Interact. 23, 791–798

30 Nahar, K. et al. (2012) Abscisic acid interacts antagonistically withclassical defense pathways in rice-migratory nematode interaction.New Phytol. 196, 901–913

31 Nakashita, H. et al. (2003) Brassinosteroid functions in a broad rangeof disease resistance in tobacco and rice. Plant J. 33, 887–898

32 Shimono, M. et al. (2012) Rice WRKY45 plays important rolesin fungal and bacterial disease resistance. Mol. Plant Pathol. 13,83–94

33 Shimono, M. et al. (2007) Rice WRKY45 plays a crucial rolein benzothiadiazole-inducible blast resistance. Plant Cell 19,2064–2076

34 Takatsuji, H. et al. (2010) Salicylic acid signaling pathway in rice andthe potential applications of its regulators. Jpn Agr. Res. Q. 44, 217–223

35 Matsushita, A. et al. (2013) Nuclear ubiquitin proteasomedegradation affects WRKY45 function in the rice defense program.Plant J. 73, 302–313

36 Spoel, S.H. et al. (2009) Proteasome-mediated turnover of thetranscription coactivator NPR1 plays dual roles in regulating plantimmunity. Cell 137, 860–872

37 Wang, D. et al. (2006) A genomic approach to identify regulatory nodesin the transcriptional network of systemic acquired resistance inplants. PLoS Pathog. 2, 1042–1050

38 Deng, H. et al. (2012) A CCCH-type zinc finger nucleic acid-bindingprotein quantitatively confers resistance against rice bacterial blightdisease. Plant Physiol. 158, 876–889

39 Riemann, M. et al. (2013) Identification of rice allene oxide cyclasemutants and the function of jasmonate for defence againstMagnaporthe oryzae. Plant J. 74, 226–228

40 Tao, Z. et al. (2009) A pair of allelic WRKY genes play opposite roles inrice–bacteria interactions. Plant Physiol. 151, 936–948

41 Xiao, W. et al. (2009) A rice gene of de novo origin negatively regulatespathogen-induced defense response. PLoS ONE 4, e4603

42 Yamada, S. et al. (2012) Involvement of OsJAZ8 in jasmonate-induced resistance to bacterial blight in rice. Plant Cell Physiol. 53,2060–2072

43 Mei, C.S. et al. (2006) Inducible overexpression of a rice allene oxidesynthase gene increases the endogenous jasmonic acid level, PR geneexpression, and host resistance to fungal infection. Mol. Plant MicrobeInteract. 19, 1127–1137

44 Taheri, P. and Tarighi, S. (2010) Riboflavin induces resistance in riceagainst Rhizoctonia solani via jasmonate-mediated priming ofphenylpropanoid pathway. J. Plant Physiol. 167, 201–208

45 Peng, X. et al. (2012) Constitutive expression of rice WRKY30 geneincreases the endogenous jasmonic acid accumulation, PR geneexpression and resistance to fungal pathogens in rice. Planta 236,1485–1498

46 Liu, X. et al. (2012) Activation of the jasmonic acid pathway bydepletion of the hydroperoxide lyase OsHPL3 reveals crosstalkbetween the HPL and AOS branches of the oxylipin pathway inrice. PLoS ONE 7, e50089

47 Lu, J. et al. (2011) An EAR-motif-containing ERF transcription factoraffects herbivore-induced signaling, defense and resistance in rice.Plant J. 68, 583–596

48 Nahar, K. et al. (2011) The jasmonate pathway is a key player insystemically induced defense against root knot nematodes in rice.Plant Physiol. 157, 305–316

49 Tong, X. et al. (2012) The rice hydroperoxide lyase OsHPL3 functionsin defense responses by modulating the oxylipin pathway. Plant J. 71,763–775

50 Ye, M. et al. (2012) Silencing COI1 in rice increases susceptibilityto chewing insects and impairs inducible defense. PLoS ONE 7,e36214

51 Zhou, G. et al. (2009) Silencing OsHI-LOX makes rice moresusceptible to chewing herbivores, but enhances resistance to aphloem feeder. Plant J. 60, 638–648

52 Desaki, Y. et al. (2012) Positive crosstalk of MAMP signalingpathways in rice cells. PLoS ONE 7, e51953

53 Schweizer, P. et al. (1998) Induced systemic resistance in woundedrice plants. Plant J. 14, 475–481

54 Schweizer, P. et al. (1997) Gene-expression patterns and levels ofjasmonic acid in rice treated with the resistance inducer 2,6-dichloroisonicotinic acid. Plant Physiol. 115, 61–70

55 Schweizer, P. et al. (1997) Jasmonate-inducible genes are activated inrice by pathogen attack without a concomitant increase in endogenousjasmonic acid levels. Plant Physiol. 114, 79–88

56 Xie, X.Z. et al. (2011) Phytochromes regulate SA and JA signalingpathways in rice and are required for developmentally controlledresistance to Magnaporthe grisea. Mol. Plant 4, 688–696

57 De Vleesschauwer, D. et al. (2010) Abscisic acid-induced resistanceagainst the brown spot pathogen Cochliobolus miyabeanus in rice

9





















































































































































involves MAP kinase-mediated repression of ethylene signaling.Plant Physiol. 152, 2036–2052

58 Shen, X. et al. (2011) OsEDR1 negatively regulates rice bacterialresistance via activation of ethylene biosynthesis. Plant Cell Environ.34, 179–191

59 Helliwell, E.E. et al. (2013) Transgenic rice with inducible ethyleneproduction exhibits broad-spectrum disease resistance to the fungalpathogens Magnaporthe oryzae and Rhizoctonia solani. PlantBiotechnol. J. 11, 33–42

60 Cao, F.Y. et al. (2011) The roles of ABA in plant–pathogeninteractions. J. Plant Res. 124, 489–499

61 Asselbergh, B. et al. (2008) Global switches and fine-tuning – ABAmodulates plant pathogen defense. Mol. Plant Microbe Interact. 21,709–719

62 Koga, H. et al. (2004) Abscisic acid and low temperatures suppress thewhole plant-specific resistance reaction of rice plants to the infectionof Magnaporthe grisea. Physiol. Mol. Plant Pathol. 65, 3–9

63 Yazawa, K. et al. (2012) Reduction of abscisic acid levels or inhibitionof abscisic acid signaling in rice during the early phase ofMagnaporthe oryzae infection decreases its susceptibility to thefungus. Physiol. Mol. Plant Pathol. 78, 1–7

64 Xu, J. et al. (2013) Abscisic acid promotes susceptibility to the rice leafblight pathogen Xanthomonas oryzae pv. oryzae by suppressingsalicylic acid-mediated defenses. PLoS ONE 8, e67413

65 Kurosawa, E. (1926) Experimental studies on the nature of thesubstance secreted by the ‘bakanae’ fungus. Nat. Hist. Soc.Formosa 16, 213–227

66 Navarro, L. et al. (2008) DELLAs control plant immune responses bymodulating the balance and salicylic acid signaling. Curr. Biol. 18,650–655

67 Qin, X. et al. (2013) Gibberellin 20-oxidase gene OsGA20ox3 regulatesplant stature and disease development in rice. Mol. Plant MicrobeInteract. 26, 227–239

68 Yang, D-L. et al. (2008) Altered disease development in the eui mutantsand Eui overexpressors indicates that gibberellins negatively regulaterice basal disease resistance. Mol. Plant 1, 528–537

69 Tanaka, N. et al. (2006) gid1, a gibberellin-insensitive dwarf mutant,shows altered regulation of probenazole-inducible protein (PBZ1) inresponse to cold stress and pathogen attack. Plant Cell Environ. 29,619–631

70 Yang, D-L. et al. (2012) Plant hormone jasmonate prioritizes defenseover growth by interfering with gibberellin signaling cascade. Proc.Natl. Acad. Sci. U.S.A. 109, E1192–E1200

71 Navarro, L. et al. (2006) A plant miRNA contributes to antibacterialresistance by repressing auxin signaling. Science 312, 436–439

72 Fu, J. et al. (2011) Manipulating broad-spectrum disease resistance bysuppressing pathogen-induced auxin accumulation in rice. PlantPhysiol. 155, 589–602

73 Ding, X. et al. (2008) Activation of the indole-3-acetic acid-amidosynthetase GH3-8 suppresses expansin expression and promotessalicylate- and jasmonate-independent basal immunity in rice.Plant Cell 20, 228–240

74 Domingo, C. et al. (2009) Constitutive expression of OsGH3.1reduces auxin content and enhances defense response andresistance to a fungal pathogen in rice. Mol. Plant MicrobeInteract. 22, 201–210

75 Llorente, F. et al. (2008) Repression of the auxin response pathwayincreases Arabidopsis susceptibility to necrotrophic fungi. Mol. Plant1, 496–509

76 Nahar, K. et al. (2013) Brassinosteroids suppress rice defense againstroot-knot nematodes through antagonism with the jasmonatepathway. Mol. Plant Microbe Interact. 26, 106–115

77 Albrecht, C. et al. (2012) Brassinosteroids inhibit pathogen-associatedmolecular pattern-triggered immune signaling independent ofthe receptor kinase BAK1. Proc. Natl. Acad. Sci. U.S.A. 109, 303–308

78 Belkhadir, Y. et al. (2012) Brassinosteroids modulate the efficiency ofplant immune responses to microbe-associated molecular patterns.Proc. Natl. Acad. Sci. U.S.A. 109, 297–302

79 Jaillais, Y. et al. (2011) Extracellular leucine-rich repeats as aplatform for receptor/coreceptor complex formation. Proc. Natl.Acad. Sci. U.S.A. 108, 8503–8507

10

80 Argueso, C.T. et al. (2012) Two-component elements mediateinteractions between cytokinin and salicylic acid in plantimmunity. PLoS Genet. 8, e1002448

81 Choi, J. et al. (2010) The cytokinin-activated transcriptionfactor ARR2 promotes plant Immunity via TGA3/NPR1-dependent salicylic acid signaling in Arabidopsis. Dev. Cell 19,284–295

82 Jiang, C-J. et al. (2013) Cytokinins act synergistically with salicylicacid to activate defense gene expression in rice. Mol. Plant MicrobeInteract. 26, 287–296

83 Thaler, J.S. et al. (2012) Evolution of jasmonate and salicylate signalcrosstalk. Trends Plant Sci. 17, 260–270

84 Takeuchi, K. et al. (2011) RSOsPR10 expression in response toenvironmental stresses is regulated antagonistically by jasmonate/ethylene and salicylic acid signaling pathways in rice roots. Plant CellPhysiol. 52, 1686–1696

85 Lee, A. et al. (2004) Inverse correlation between jasmonic acid andsalicylic acid during early wound response in rice. Biochem. Biophys.Res. Commun. 318, 734–738

86 Li, R. et al. (2013) OsNPR1 negatively regulates herbivore-induced JAand ethylene signaling and plant resistance to a chewing herbivore inrice. Physiol. Plant. 147, 340–351

87 Quilis, J. et al. (2008) The Arabidopsis AtNPR1 inversely modulatesdefense responses against fungal, bacterial, or viral pathogens whileconferring hypersensitivity to abiotic stresses in transgenic rice. Mol.Plant Microbe Interact. 21, 1215–1231

88 Qiu, D. et al. (2007) OsWRKY13 mediates rice disease resistanceby regulating defense-related genes in salicylate- and jasmonate-dependent signaling. Mol. Plant Microbe Interact. 20, 492–499

89 Qiu, D. et al. (2009) Exploring transcriptional signalling mediated byOsWRKY13, a potential regulator of multiple physiological processesin rice. BMC Plant Biol. 9, 74

90 Qiu, D. et al. (2008) Rice gene network inferred from expressionprofiling of plants overexpressing OsWRKY13, a positive regulatorof disease resistance. Mol. Plant 1, 538–551

91 Qi, J. et al. (2011) The chloroplast-localized phospholipases D alpha 4and alpha 5 regulate herbivore-induced direct and indirect defenses inrice. Plant Physiol. 157, 1987–1999

92 Garg, R. et al. (2012) Microarray analysis reveals overlapping andspecific transcriptional responses to different plant hormones in rice.Plant Signal. Behav. 7, 1–6

93 Bailey, T.A. et al. (2009) Role of ethylene, abscisic acid and MAPkinase pathways in rice blast resistance. In Advances in Genetics,Genomics and Control of Rice Blast Disease (Wang, G.L. and Valent,B., eds), pp. 185–190, Springer

94 Xiong, L.Z. and Yang, Y.N. (2003) Disease resistance andabiotic stress tolerance in rice are inversely modulated by anabscisic acid-inducible mitogen-activated protein kinase. Plant Cell15, 745–759

95 Wang, Q. et al. (2013) OsMPK3 positively regulates the JA signalingpathway and plant resistance to a chewing herbivore in rice. PlantCell Rep. 7, 1075–1084

96 Heinrich, M. et al. (2013) High levels of jasmonic acid antagonize thebiosynthesis of gibberellins and inhibit the growth of Nicotianaattenuata stems. Plant J. 73, 591–606

97 Grant, M.R. et al. (2013) Exploiting pathogens’ tricks of the trade forengineering of plant disease resistance: challenges and opportunities.Microb. Biotechnol. 6, 212–222

98 Kovach, M.J. et al. (2007) New insights into the history of ricedomestication. Trends Genet. 23, 578–587

99 Huang, X. et al. (2012) A map of rice genome variation reveals theorigin of cultivated rice. Nature 490, 497–501

100 Mew, T.W. et al. (2004) Looking ahead in rice disease research andmanagement. Crit. Rev. Plant Sci. 23, 103–127

101 Parbery, D.G. (1996) Trophism and the ecology of fungi associatedwith plants. Biol. Rev. Camb. Philos. Soc. 71, 473–527

102 Spielmeyer, W. et al. (2002) Semidwarf (sd-1), ‘‘green revolution’’ rice,contains a defective gibberellin 20-oxidase gene. Proc. Natl. Acad. Sci.U.S.A. 99, 9043–9048

103 Khush, G.S. (1999) Green revolution: preparing for the 21st century.Genome 42, 646–655

















































































































































104 Sasaki, A. et al. (2002) Green revolution: a mutant gibberellin-synthesisgene in rice – new insight into the rice variant that helped to avertfamine over thirty years ago. Nature 416, 701–702

105 Monna, L. et al. (2002) Positional cloning of rice semidwarfing gene,sd-1: rice ‘‘green revolution gene’’ encodes a mutant enzyme involvedin gibberellin synthesis. DNA Res. 9, 11–17

106 Asano, K. et al. (2011) Artificial selection for a green revolution geneduring japonica rice domestication. Proc. Natl. Acad. Sci. U.S.A. 108,11034–11039

107 Seo, J-S. et al. (2011) OsbHLH148, a basic helix-loop-helix protein,interacts with OsJAZ proteins in a jasmonate signaling pathwayleading to drought tolerance in rice. Plant J. 65, 907–921

108 Jiang, C-J. et al. (2009) Suppression of the rice fatty-acid desaturasegene OsSSI2 enhances resistance to blast and leaf blight diseases inrice. Mol. Plant Microbe Interact. 22, 820–829

109 Umemura, K. et al. (2009) Contribution of salicylic acidglucosyltransferase, OsSGT1, to chemically induced diseaseresistance in rice plants. Plant J. 57, 463–472

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