National Science Review

REVIEW 3: 295–308, 2016

doi: 10.1093/nsr/nww015
Advance access publication 19 April 2016

AGRICULTURAL SCIENCES

Special Topic: Rice Breeding

Plant innate immunity in rice: a defense against pathogen
infection

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Wende Liu1,∗ and Guo-Liang Wang1,2,∗

ABSTRACT
A large number of pathogenic microorganisms cause rice diseases that lead to enormous yield losses
worldwide. Such losses are important because rice is a staple food for more than half of the world’s
population. Over the past two decades, the extensive study of the molecular interactions between rice
and the fungal pathogen Magnaporthe oryzae and between rice and the bacterial pathogen Xanthomonas
oryzae pv. oryzae has made rice a model for investigating plant–microbe interactions of monocotyledons.
Impressive progress has been recently achieved in understanding the molecular basis of rice
pathogen-associated molecular pattern-immunity and effector-triggered immunity. Here, we briefly
summarize these recent advances, emphasizing the diverse functions of the structurally conserved fungal
effectors, the regulatory mechanisms of the immune receptor complexes, and the novel strategies for
breeding disease resistance. We also discuss future research challenges.
Keywords: plant immunity, pathogen effectors, rice, diseases, Magnaporthe oryzae, Xanthomonas oryzae
pv. oryzae
1 State Key Laboratory

for Biology of Plant

Diseases and Insect INTRODUCTION PLANT INNATE IMMUNITY
Pests, Institute of Many microbial pathogens attack crop plants and Over the last two decades, extensive genetic and
Plant Protection, cause huge yield losses that threaten global food se- molecular studies of plant–microbe interactions
Chinese Academy of
curity. Although application of chemicals has sig- in several model systems have revealed that plants
Agricultural Sciences,
nificantly reduced plant diseases, planting of re- have evolved a two-branched innate immunity
Beijing 100193, China
and 2 Department of
sistant cultivars remains the most effective and system that detects and wards off various pathogens,
Plant Pathology, Ohio environmental-friendly strategy to control crop dis- resulting in disease resistance [1]. According to
State University, eases. Rice (Oryza sativa) is an important crop that is the standard zigzag model to illustrate the plant
Columbus, OH 43210, grown in Asia, Africa, and South and Central Amer- two-branched immune system in response to
USA ica. Over half of the global population consumes rice pathogens, the first branch uses transmembrane
as the main food source. Throughout the growing pattern-recognition receptors (PRRs) that rec-
∗ Corresponding season, a variety of pathogens, including fungi, bac- ognize conserved pathogen-associated molecular
authors. E-mails: teria, viruses, and nematodes, infect different parts of patterns (PAMPs), leading to an immune re-
wang.620@osu.edu; rice plants and greatly reduce yields. In the last two sponse called PAMP-triggered immunity (PTI).
liuwende@caas.cn decades, considerable knowledge has been obtained To circumvent PTI, fungal, bacterial, viral, and
regarding the recognition of pathogens by rice plants nematode pathogens evolve effector proteins that
Received 23 and the signaling events in rice innate immunity. suppress host defenses leading to effector-triggered
November 2015; Here, we summarize the advances in understanding susceptibility (ETS). The second branch, which
Revised 20 March rice innate immunity and the application of that un- mostly acts within the cell, uses highly polymorphic
2016; Accepted 22 derstanding to the breeding of disease-resistant vari- resistance (R) proteins that respond to pathogen
March 2016 eties. We also discuss the major challenges for future effectors, leading to a rapid and robust effector-
research. triggered immunity (ETI). However, this zigzag


C The Author(s) 2016. Published by Oxford University Press on behalf of China Science Publishing & Media Ltd. All rights reserved. For permissions, please e-mail:

journals.permissions@oup.com
296 Natl Sci Rev, 2016, Vol. 3, No. 3 REVIEW

Table 1. Major fungal, bacterial, nematode, and viral diseases of rice.

Diseases of rice Pathogen Rice yield loss References

Fungal disease
Rice blast Magnaporthe oryzae Up to 100% [2]
Rice sheath blight Rhizoctonia solani Up to 50% [3]
False smut Ustilaginoidea virens Up to 44% http://www.apsnet.org/publications/
(Cooke) Takah imageresources/Pages/FI00163.aspx
Sheath rot Sarocladium oryzae Up to 85% http://www.knowledgebank.irri.org/rice.htm
(Sawada) W. Gams & D.
Hawksworth

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Brown spot Cochliobolus miyabeanus Up to 45%, caused ‘Great [4]
Bengal Famine’ in 1942
Bakanae Fusarium fujikuroi Yield reductions and [5]
mycotoxin contamination
Bacterial disease
Bacterial blight Xanthomonas oryzae pv. 10–50% [6]
oryzae
Bacterial leaf streak Xanthomonas oryzae pv. 8–32% [7]
oryzicola
Bacterial panicle blight Burkholderia glumae Up to 85% [8]
Nematode disease
Rice root-knot nematode Meloidogyne graminicola Up to 87% [9]
Rice white tip nematode Aphelenchoides besseyi Up to 50% http://pest.ceris.purdue.edu/pest.php?
code=NEABABB
Rice stem nematode Ditylenchus angustus 20–90% http://www.cabi.org/isc/datasheet/19285
Rice cyst nematodea Heterodera elachista Unknown [10]
Heterodera oryzicola Up to 42% [10]
Heterodera oryzae Unknown [10]
Heterodera sacchari Similar with H. oryzicola [10]
Viral disease
Rice stripe Rice stripe virus 30%–40% http://en.jaas.ac.cn/zbs/highlights.asp
Rice black streaked dwarf Rice black streaked dwarf ∼60% http://www.cabi.org/isc/abstract/
virus 19881671518
Southern rice black Southern rice black Up to 100% http://en.jaas.ac.cn/zbs/highlights.asp
streaked dwarf streaked dwarf virus
Rice yellow mottle Rice yellow mottle virus 10%–100% http://www.knowledgebank.irri.org/training/
fact-sheets/pest-management/diseases/item/
rice-yellow-mottle-virus-fact-sheet
a
Total of four species of Heterodera genus have been discriminated that cause rice cyst nematode disease.

model does not fully apply to some unique as- MAJOR DISEASES IN RICE
pects in plant–virus interactions [11]. Although
Seventeen rice diseases caused by fungi, bacteria, ne-
there are limited comparative studies between
matodes, and viruses are listed in Table 1. Based
antiviral and antibacterial/antifungal immune
on scientific and economic importance, the most
responses, some reviewers proposed that RNA
important of these are rice blast caused by the
silencing (RNAi) evolved by plant that recognize
fungus Magnaporthe oryzae, bacterial blight caused
viral double-stranded RNA (dsRNA, corresponds
by the bacterium Xanthomonas oryzae pv. oryzae
to PAMP from fungi and bacteria) may have
(Xoo), root knot caused by the nematode Meloidog-
similar functions as PTI in blocking viral infection
yne graminicola, white tip caused by the nema-
[11,12]. As the result of the plant–virus coevolution,
tode Aphelenchoides besseyi and rice stem nema-
viral suppressors of RNAi (VSRs) are regarded as
tode disease caused by the nematode Ditylenchus
effectors to overcome host RNAi (regarding as
angustus. These pathogens were selected as the
ETS) [11,12]. Plant R proteins that recognize VSRs
top 10 plant pathogenic fungi, bacteria, and nema-
as avirulence proteins can mediate a strong defense
todes, respectively; by the review articles published
as ETI [11].
REVIEW Liu and Wang 297

understanding of rice innate immunity against bac-

terial and fungal pathogens were recently reviewed
by Liu et al. [19]. In this review, we consider the new
progress in the two model pathosystems and novel
insights into rice innate immunity against nematode
and viral pathogens.

RICE PRR REPERTOIRE AND PTI

In a long-term evolutionary arms race with

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pathogenic microorganisms, plants have evolved
a repertoire of PRR genes that recognize the
conserved microbial PAMPs, leading to the inhi-
bition of pathogen infection [1]. Plant PRRs are
cell-surface receptors that perceive PAMPs released
from the infecting pathogens in the extracellular
environment; the perception of PAMPs by PRRs
results in PTI responses. Plant PRRs are represented
by transmembrane receptor-like kinases (RLKs),
which typically contain extracellular leucine-rich
repeats and an intracellular kinase domain, and
Figure 1. The five most important diseases of rice according to the journal Molecular receptor-like proteins (RLPs), which lack a kinase
Plant Pathology. (a) Rice blast (neck/panicle blast) caused by the fungus M. oryzae, a domain [20]. Because RLPs lack a cytoplasmic
potent pathogen that infects all parts of rice but causes the greatest losses when it kinase domain, they recruit proteins containing
incites neck/panicle blast. The fungus initiates neck/panicle blast by infecting nodes kinase domains for the activation of the downstream
on the rice stem; this is followed by massive hyphal growth, resulting in the rotting of signaling pathways. More than 1131 RLK genes
the neck and the failure of grain filling. Image provided by Wende Liu. (b) Rice bac- have been identified in the rice genome; this is
terial blight caused by X. oryzae pv. oryzae. After X. oryzae pv. oryzae invades the
nearly two times the number in Arabidopsis and
plant through hydathodes or wounds, it multiplies in xylem vessels. Image courtesy of
probably results from duplication events in the
Yongfeng Liu, Institute of Plant Protection, Jiangsu Academy of Agricultural Sciences,
China. (c) Root knot caused by the nematode M. graminicola. Meloidogyne graminicola RLK genes of rice [21]. RLPs form a second major
larvae infect rice roots, causing characteristic terminal swellings/galls on the roots and class of cell-surface receptors in plants, and the rice
draining plant photosynthates and nutrients. Infection of young plants may be lethal, genome encodes 90 RLP genes [22]. Together,
whereas infection of mature plants decreases yield. (d) Rice white tip caused by the these receptor classes respond to a wide variety
nematode A. besseyi. The nematode enters rice florets, proliferates, and causes char- of activating ligands (lipid, protein, nucleic acids,
acteristic whitening of the leaf tips; the leaf tips then die, and grain yield is reduced. carbohydrate, etc.) from various exogenous sources,
Images in panels c and d are from Wenkun Huang, Institute of Plant Protection, Chinese such as pathogens and host-derived endogenous
Academy of Agricultural Sciences, China. (e) Rice stem nematode disease caused by danger signals. Studies have increasingly shown
D. angustus. This nematode is located in rice stubble and glumes during its dormant that conserved PAMPs such as bacterial flagellin,
stage. During the growing season, it penetrates the leaf sheaths and stalks, where it
peptidoglycan, lipopolysaccharide, and fungal
develops, reproduces, and causes leaf distortion and seed abortion. Image courtesy
chitin can be sensed by rice cells and trigger innate
of Jichun Wang, Institute of Plant Protection, Jilin Academy of Agricultural Sciences,
China. immunity [23–26].
Several rice PRR proteins including XA21, Os-
FLS2, CEBiP, OsCERK1, LYP4, and LYP6 have
Molecular Plant Pathology [13–15] (Fig. 1). In re- been well characterized (Table 2). The rice RLK
cent years, the following re-emerging diseases have gene Xa21 was one of the first innate immune
become increasingly important: rice sheath blight receptor genes to be isolated and confers resis-
caused by Rhizoctonia solani, rice false smut caused tance to a wide range of Xoo strains [27]. The
by Ustilaginoidea virens (Cooke) Takah, rice bac- XA21-mediated signaling network has been inten-
terial panicle blight caused by Burkholderia glumae, sively studied through genetic and biochemical
and rice stripe disease caused by rice stripe virus approaches [19,23]. A number of previous stud-
(RSV) [3,16–18]. Over the past two decades, the ies have identified several Xoo Rax (required for
rice/M. oryzae and rice/Xoo pathosystems in partic- activation of Xa21) genes that activate the XA21-
ular have been the focus of intensive studies and have mediated immune response [28]. These genes are
become molecular models for research on plant– loca ted in a single operon (raxSTAB) that in-
microbe interactions. The major advances in the cludes a tyrosine sulfotransferase (RaxST) and three
298 Natl Sci Rev, 2016, Vol. 3, No. 3 REVIEW

Table 2. PRR genes and co-receptors that are important for rice immunity.

PRR gene Protein structure Function Reference

CEBiP LysM RLP Chitin receptor [25]

LYP4 LysM RLP Chitin and PGN receptor [24]
LYP6 LysM RLP Chitin and PGN receptor [24]
OsFLS2 LRR RLK Recognizes flg22 and triggers immunity [29,30]
XA21 LRR RLK Recognizes RaxX21-sY and triggers immunity [27]
OsCERK1 LysM RLK Co-receptor of CEBiP, LYP4 and LYP6 [31]
OsRLCK185 Receptor-like Interacts with OsCERK1 and important for chitin- and [32]

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cytoplasmic kinases PGN-induced immunity
OsRLCK176 Receptor-like Interacts with OsCERK1 and important for chitin- and [33]
cytoplasmic kinases PGN-induced immunity
OsSERK1 LRR RLK Regulates BR-mediated development signaling [34]
OsSERK2 LRR RLK Co-receptor kinases of XA21 and regulates [35]
BR-mediated development signaling

components (RaxA, RaxB, and RaxC) of a pre- ing components [33]. Therefore, OsCERK1 func-
dicted type 1 secretion system [28]. Based on these tions as an adaptor in conjunction with OsLYP4 and
findings, researchers hypothesized that a tyrosine- OsLYP6 and plays dual roles in PGN and chitin sig-
sulfated, type 1-secreted protein activates XA21- naling in rice innate immunity. These results demon-
mediated immunity. Consistent with this hypothe- strate that multiple PRR proteins may work together
sis, a sulfated, 21-amino acid (AA) synthetic peptide to respond to PAMPs in rice.
(RaxX21-sY) derived from RaxX protein secreted
by Xoo was proved to be essential for triggering
XA21-mediated resistance [36]. Interestingly, RaxX
RICE R GENE REPERTOIRE AND ETI
residues between 40 to 55 share remarkable simi-
larity with Arabidopsis signaling factor PSY1 (sul- It is well known that nucleotide-binding and leucine-
fated, secreted 18-AA peptide) and four predicted rich repeat domain (NLR) proteins function as im-
rice PSY1 orthologs [36]. The high similarities sug- mune receptors in both animals and plants [37].
gest that when a rice plant lacks XA21, Xoo and other However, plant genomes contain many more NLRs
Xanthomonads might use sulfated RaxX to mimic than animal genomes, indicating differences in the
PSY1-like peptides in order to suppress host defense two immune systems. The rice genome, for exam-
responses and facilitate infection [36]. ple, contains about 480 NLR genes while the hu-
OsFLS2 is the rice ortholog of Arabidopsis FLS2, man genome has only about 10 [38]. Interestingly,
and heterologous expression of OsFLS2 in the fls2 the majority of the cloned R genes encode NLR
mutant can restore the fls2 mutant defects in Ara- proteins (Table 3), although several atypical R pro-
bidopsis [29]. Like FLS2, OsFLS2 can directly rec- teins containing a variety of conserved protein do-
ognize flg22 and trigger an immune response in rice mains/motifs are also identified (Fig. 2). Details
[30]. These results indicate that the flg22 signaling concerning the structure and function of the cloned
pathway is conserved between Arabidopsis and rice R genes have been reviewed and discussed in Liu
and that OsFLS2 may also provide PTI-mediated et al. [19].
defense in rice. Researchers have characterized sev- In the last 2 years, five new R genes (Pi50, Pi64,
eral chitin immune receptors (CEBiP, OsCERK1, Xa10, Xa23, and STV11) have been cloned. Among
LYP4, and LYP6) that directly or indirectly recog- them, Pi50 and Pi64 encode typical NLR proteins
nize chitin fragments and trigger defense responses [39,40]. NLR genes are usually located in clusters
in rice [24,25,31]. Intriguingly, OsCERK1, LYP4, in plant genomes; of the 480 NLR genes in rice,
and LYP6 are also important for triggering im- for example, 263 reside in 44 clusters [38]. Rice
mune responses to bacterial PGN in rice [24]. R genes Pi2, Pi9, and Piz-t are located in one of
Furthermore, recent evidence indicates that the these NLR gene clusters on chromosome 6, and
receptor-like cytoplasmic kinases OsRLCK185 and at least eight R genes are located at this locus
OsRLCK176 function downstream of OsCERK1 in in both wild and cultivated rice [41]. The newly
the chitin and PGN signaling pathways, suggest- cloned Pi50 gene is located at the Pi2/9 locus and
ing that chitin and PGN share intracellular signal- confers broad-spectrum resistance to M. oryzae [42].
REVIEW Liu and Wang 299

Table 3. The cloned rice resistance genes and M. oryzae and X. oryzae pv. oryzae avirulence genes.
Resistant genes Avirulence genes References

R gene Encoding protein Avr gene Encoding protein Pathogen

Pib NB-LRR AvrPib 75 AA secreted protein Magnaporthe [43,44]

oryzae
Pi-ta NB-LRR AvrPi-ta 224 AA secreted [45,46]
protein
Pi9 NB-LRR AvrPi9 91 AA secreted protein [47,48]
Pi2 NB-LRR ND – [49]

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Piz-t NB-LRR AvrPiz-t 108 AA secreted [49,50]
protein
Pi-d2 B lectin RLK ND – [51]
Pi33c – ACE1 Polyketide synthase [52]
Pii c – AvrPii 70 AA secreted protein [53]
Pi36 NB-LRR ND – [54]
Pi37 NB-LRR ND – [55]
Pi50a NB-LRR ND – [39]
Pi64 NB-LRR ND – [40]
Pikma NB-LRR Avr-Pik/km/kp 113 AA secreted [53,56]
protein, five alleles
(A–E)
Pit NB-LRR ND – [57]
Pi5a NB-LRR ND – [58]
Pid3 NB-LRR ND – [59]
Pid3-A4 NB-LRR ND – [60]
Pi54 NB-LRR ND – [59]
Pish NB-LRR ND – [61]
Pik NB-LRR Avr-Pik/km/kp 113 AA secreted [53,62]
protein, five alleles
(A–E)
Pikp NB-LRR Avr-Pik/km/kp 113 AA secreted [53,63]
protein, five alleles
(A–E)
Piaa,b NB-LRR Avr-Pia 85 AA secreted protein [53,64]
Pi-CO39a,b NB-LRR Avr1-CO39 89 AA secreted protein [65]
Pi25 NB-LRR ND – [66]
Pi1 NB-LRR ND – [67]
pi21 Proline-containing ND – [68]
protein
Pb1 NB-LRR ND – [69]
ND – PWL2 145 AA secreted [70]
protein
xa5 TFIIA transcription Avrxa5/PthXo7 Xanthomonas [71]
factor oryzae pv.
oryzae
xa13 MtN3/saliva Avrxa13/PthXo1 TALE [72]
domain protein
Xa25 MtN3/saliva ND [73]
domain protein
Xa3/Xa26 LRR-RLK AvrXa3 TALE [74,75]
Xa27 Rice unique gene AvrXa27 TALE [76]
Xa1 NB-LRR ND [77]
Os11N3 Homolog of AvrXa7 TALE [78]
(OsSWEET14) nodulin MtN3
300 Natl Sci Rev, 2016, Vol. 3, No. 3 REVIEW

Table 3 (Continued.)
Resistant genes Avirulence genes References

R gene Encoding protein Avr gene Encoding protein Pathogen

Xa10 Executor R protein, AvrXa10 TALE [79]

encodes 126 AA, with
four potential
transmembrane helices
Xa23 Executor R protein, AvrXa23 TALE [80]
encodes 113 AA, with

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four potential
transmembrane helices
Rxo1d NB-LRR AvrRxo1 – Xanthomonas [81,82]
oryzae pv.
oryzicola
STV11 Sulfotransferase ND – RSV [18]
a
The function of these three R genes requires two NB-LRR members.
b
These two R genes share the same NB-LRR gene locus.
c
The gene has not been cloned yet.
d
This gene was cloned from maize.
ND = not determined.

fer Pi50-mediated blast resistance in rice [39]. Pi50

shares more than 96% AA sequence identity with
Pi2, Pi9, and Piz-t, suggesting that Pi50 is derived
from the functional divergence of duplicated genes
[39]. The allelic gene Pi64 encodes a 1288-AA pro-
tein and is localized in both the cytoplasm and nu-
cleus [40]. Pi64 is constitutively expressed in all tis-
sues and at all development stages, and confers a
high level of resistance to both leaf and neck blast in
rice [40].
Both Xa10 and Xa23 are executor R proteins
that confer the transcription activator-like effector
(TALE)-dependent resistance to bacterial blight in
rice [79,80]. The XA10 protein localizes as hexam-
Figure 2. A diagram showing the domain diversity of rice ers in the endoplasmic reticulum (ER) and such
atypical R proteins. Eleven rice R proteins with different localization coincides with the ER Ca2+ depletion
domains are illustrated, including the bulb-type mannose- and XA10-induced cell death in plants [79]. These
specific lectin (B lectin) domain, the protein tyrosine kinase
results suggest that XA10 is an inducible protein
(Pkinase Tyr) domain, the heavy metal-associated (HMA) do-
main, the proline-rich motifs (PRMs), the transmembrane he-
that triggers programmed cell death by a conserved
lices (TM), the transcription initiation factor IIA, gamma sub- mechanism involving disruption of the ER and of
unit, helical (TFIIA gamma N) domain, the transcription initi- cellular Ca2+ homeostasis. The Xa23 protein shares
ation factor IIA, gamma subunit (TFIIA gamma C), the sugar 50% identity with XA10, and these two executor
efflux transporter for intercellular exchange (MtN3 slv) do- R proteins also have a similar predicted transmem-
main, the PQ loop repeat (PQ-loop) domain, the leucine rich brane helices structure [80]. Xa23 transcription is
repeat (LRR) domain, and the sulfotransferase family (Sulfo- specifically activated by the TALE AvrXa23, and
transfer 3) domain. Protein domains/motifs were predicted XA23 can trigger a strong immune response in rice,
by the SMART program (http://smart.embl-heidelberg.de/) tobacco, and tomato [80]. The promoters of both
with a normal mode. Figures are not drawn to scale. Xa10 and Xa23 contain a TALE-binding element
that is essential for cognate TALE-induced resis-
The Pi50 cluster contains four duplicated genes tance [79,80]. These results suggest that the rice
(Pi50 NBS4 1/2 and Pi50 NBS4 3/4) that differ in genome has evolved an executor R gene family, the
only four AAs [39]. Complementation tests revealed members of which function in disease resistance by
that Pi50 NBS4 1/2 but not Pi50 NBS4 3/4 con- recognizing the cognate TALEs in Xoo.
REVIEW Liu and Wang 301

STV11, which confers durable resistance to RSV, ble for resistance to the cyst nematodes that attacks
was recently cloned by a map-based cloning strat- rice is urgently needed.
egy [18]. The gene encodes a sulfotransferase that Recently, many new resistance genes have
can catalyze the conversion of salicylic acid (SA) into been mapped via genome-wide association studies
sulphonated salicylic acid (SSA) in RSV-infected (GWASs) of large collections of rice germplasm.
plants, and SSA is more effective than SA in trigger- Wang et al., for example, investigated 366 diverse
ing RSV resistance and in inhibiting viral replication indica rice accessions using 0.8 million single-
[18]. Moreover, SSA may also serve as a signal to en- nucleotide polymorphisms (SNPs) and identified
hance SA biosynthesis through a positive feedback 30 loci that are significantly related to resistance to
mechanism after RSV infection; SA may contribute M. oryzae [86]. In that study, a new R gene locus
to the inhibition of viral replication in the RSV- was identified on chromosome 3 where no blast R

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infected plants [18]. STV11-R is prevalent in culti- gene had been previously reported [86]. Using 372
vated indica rice cultivars, whereas the susceptible diverse rice cultivars collected from 82 countries
allele STV11-S is prevalent in japonica cultivars. The and 700 000-SNP arrays, Kang et al. identified
cloning of STV11 will facilitate the breeding of RSV- 97 loci associated with blast resistance (LABRs)
resistant rice through molecular marker-assisted se- against five diverse isolates [87]. Among these loci,
lection; such resistance will greatly improve RSV 82 are new regions, and 15 are co-localized with
management in rice production. known blast resistance loci [87]. Further functional
Our understanding of rice resistance to nema- analysis of the candidate genes in the LABR 64
todes has lagged behind the soybean-nematode region via RNAi technology identified two new R
pathosystem. For instances, two soybean cyst ne- alleles at the Pi5 locus [87]. These results suggest
matode (SCN) resistance genes (Rhg1 and Rhg4) that GWAS is an efficient strategy for rapid allele
have been cloned through a map-based cloning strat- discovery and that GWAS, when coupled with RNAi
egy [83,84]. The Rhg1 gene encodes three proteins technology, will help researchers dissect complex
[an AA transporter (Glyma18g02580), an a-SNAP disease resistance in rice. Another recent study
protein (Glyma18g02590), and a WI12 (wound- investigated the function of 332 NLR genes that
inducible domain protein), (Glyma18g02610)], all were cloned from five blast-resistant rice cultivars
of which are essential for the resistance to SCN [83]. [88]. Strikingly, 98 of them confer resistance to one
A physical structure study revealed that the rhg1 lo- of the tested blast isolates, demonstrating that a
cus that encodes these three proteins is present in systemic approach can increase the efficiency of R
multiple copies (10 tandem copies) in SCN resistant gene cloning in rice.
lines, whereas only one copy is present in suscepti-
ble cultivars [83]. Overexpression of the individual
genes is ineffective, but overexpression of the three
PATHOGEN EFFECTORS AND THEIR HOST
genes together enhances SCN resistance [83]. These
results suggest that variation in the copy number of TARGETS
multiple genes at Rhg1 mediates SCN resistance in In a broad sense, effectors are pathogen proteins
soybean. Rhg4 encodes a ubiquitous enzyme (serine and small molecules that can alter host cell structure
hydroxymethyltransferase) that is responsible for in- and function [89]. Avr effectors are those molecules
terconversion of serine and glycine and that is impor- that are recognized by the cognate host R proteins
tant for cellular one-carbon metabolism [84]. Two directly or indirectly in plant cells; the recognition
genetic polymorphisms (R130P and Y358N) were triggers a rapid and robust hypersensitive reaction.
detected in the Rhg4 alleles of resistant versus sus- To date, a total of 21 Avr effector genes have been
ceptible cultivars, suggesting that these two AAs are cloned in rice pathogens, and these include 13 from
important for the regulatory function of this enzyme M. oryzae, 7 from Xoo, and 1 from Xoc (Table 3).
[84]. A linkage mapping study revealed a major re- The identification of these Avr genes has greatly fa-
sistance gene (Has-1Og ) against rice cyst nematode cilitated the investigation of the molecular basis of
caused by Heterodera sacchari and it was delimited to the interaction between Avr effectors and R proteins.
a 8.2 cM interval between the markers RM254 and The examples of direct and indirect interactions be-
RM206 on chromosome 11 in rice [85]. However, tween two types of proteins and host targets of the
the gene encodes Has-1Og have not been cloned. Be- Avr effectors have recently been reviewed [19,90].
cause another three species of cyst nematodes (H. AvrPib and AvrPi9 were recently cloned in M.
oryzicola, H. elachista, and H. oryzae) also frequently oryzae. AvrPib, the cognate Avr gene of the R gene
infect rice and cause significant annual yield lost, ad- Pib, was cloned using a map-based cloning strat-
ditional identification and cloning of genes responsi- egy. It encodes a 75-AA protein with no homology
302 Natl Sci Rev, 2016, Vol. 3, No. 3 REVIEW

to any protein in the database [43]. Phenotyping HORMONE-MEDIATED IMMUNITY IN

and genotyping of 60 M. oryzae isolates collected RICE
from five geographically distinct areas suggested that
Rice hormones such as SA (salicylic acid), JA
AvrPib has undergone host-driven selection [43].
(jasmonate acid), and ET (ethylene) are important
Resequencing of the AvrPib allele of 108 diverse iso-
regulators of immune responses [96–98]. Two ex-
lates revealed that transposable element (TE) inser-
cellent reviews summarized the advances in under-
tion (frequency 81.7%) is the prevalent mechanism
standing the functions of various hormones in rice
that leads to the loss of its avirulence function [43].
immunity in 2013 [99,100]. Here, we provide the
AvrPi9, the Avr gene of the R gene Pi9, was cloned
recent progress on hormone-mediated immunity in
using a comparative genomic approach with virulent
rice during the past few years.
mutant strains derived from a sequential planting

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SA, JA, and ET are three main hormones that
method [47]. The AvrPi9 protein is highly expressed
play important roles in plant immunity. SA is usually
at early stages of M. oryzae infection [47]. Moreover,
considered to regulate immunity against biotrophic
the AvrPi9 protein localizes in the biotrophic inter-
pathogens, whereas JA and ET are believed to be
facial complex and appears to be translocated into
involved in resistance to necrotrophic and insect
rice cells during infection [47]. Like AvrPib, TEs also
pests [101]. However, this dichotomy does not fully
play an important role in acquisition of virulence in
fit into the monocotyledonous plant rice [10]. Dif-
the AvrPi9 alleles in M. oryzae.
ferent from the dicot plant Arabidopsis, rice plants
Magnaporthe oryzae secretes various effectors
challenged by fungal and bacterial pathogens do not
that enter infected rice cells and then move to neigh-
show SA accumulation [102]. However, rice plants
boring cells, presumably targeting host proteins to
indeed respond to exogenous SA treatment [102].
prepare for infection [91]. Several host targets of Avr
These results suggest that rather than the endoge-
effectors have been recently characterized. For in-
nous SA level, the involvement of SA in rice defense
stance, the AvrPiz-t effector targets the rice RING E3
responses is more dependent on the SA signaling
ligase APIP6 and suppresses PTI [92]. Interestingly,
[99].
the interaction between AvrPiz-t and APIP6 leads
Accumulating evidence reveals that extensive
to their mutual degradation [92]. Transgenic rice
crosstalk between different hormones exists in rice
plants expressing the APIP6 RNAi construct have re-
plants in response to pathogen infections. For in-
duced PTI responses and reduced basal resistance to
stance, the rice DELLA protein SLR1 (slender
M. oryzae [92], suggesting that APIP6 positively reg-
rice1) represses the transcription of gibberellic acid
ulates rice innate immunity. A recent study showed
(GA)-responsive genes and functions as a key reg-
that APIP6 interacts with and degrades OsELF3-2
ulator of GA signaling [103]. Vleesschauwer et al.
(ortholog of Arabidopsis flowering and circadian reg-
recently found that SLR1 functions in resistance
ulator ELF3) [93]. The oself3-2 T-DNA mutant and
to hemibiotrophic but not necrotrophic pathogens
RNAi plant exhibit enhanced resistance to M. oryzae
[104]. Moreover, they demonstrated that SLR1 me-
[93], indicating that OsELF3-2 negatively regulates
diates resistance through integrating and amplifying
rice innate immunity against M. oryzae.
both SA- and JA-dependent defense signaling path-
The exocyst is an octameric protein complex that
ways in rice [104]. A recent transcriptome study of
functions in vesicle trafficking. Its subunits Exo70B2
root-knot nematode-infected rice plants reveals that
and Exo70H1 in Arabidopsis are involved in the re-
a number of well-identified marker genes involved
sponse to pathogens, with Exo70B2 having a more
in the SA/JA/ET pathways show significantly differ-
important role in cell wall apposition formation re-
ential expression patterns between susceptible and
lated to plant defense [94]. The Avr-Pii effector
resistant interactions [105]. These results indicate
targets two rice Exo70 proteins (OsExo70-F2 and
that various plant hormones are involved in the rice–
OsExo70-F3) to form a protein complex in rice cells
nematode interaction and further in-depth studies
[95]. Functional assays showed that OsExo70-F3
are needed to decipher the underlying mechanism of
but not OsExo70-F2 is specifically involved in Pii-
hormone-mediated resistance in this pathosystem.
dependent resistance [95]. Moreover, overexpres-
Plant hormone pathways are often targeted by
sion of Avr-Pii or silencing of OsExo70-F2 and -F3
pathogen effectors for suppression of hormone-
genes in rice did not affect the virulence to compati-
mediated immunity. For example, M. oryzae encodes
ble M. oryzae strains [95]. These results suggest that
an antibiotic biosynthesis monooxygenase (Abm)
the Avr-Pii targets OsExo70-F3 and the rice exocy-
that converts endogenous free JA into hydroxy-
tosis pathway are important for ETI and that Os-
lated JA (12OH-JA) to attenuate rice innate immu-
Exo70 functions as a decoy or helper in Pii/Avr-Pii
nity during fungal colonization [106]. The wild-type
interactions.
strain of M. oryzae secretes 12OH-JA during host
REVIEW Liu and Wang 303

penetration to avoid the defense response, whereas troscopy to determine the 3D structures of the M.
the Abm mutant of M. oryzae accumulates methyl oryzae effectors Avr1-CO39, Avr-Pia, and AvrPiz-t
JA (MeJA), which induces rice defense [106]. No- and of the Pyrenophora tritici-repentis (wheat tan
tably, M. oryzae also secretes Abm after invasion, and spot pathogen) effector ToxB [111]. The analysis
the secreted Abm appears to convert plant JA into showed that these effectors have very similar six
12OH-JA to facilitate host colonization [106], indi- β-sandwich structures that are stabilized by a
cating that Abm is an effector protein that is impor- disulfide bridge between two conserved cysteins
tant for M. oryzae pathogenicity. The host target of located in similar positions of the proteins. These
Abm remains to be identified. sequence unrelated but structurally similar fungal
In addition to inducing or manipulating host effectors were termed MAX effectors. Most M.
hormone biosynthesis, most plant pathogens are oryzae MAX effectors are highly expressed early

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producing hormones as virulence factors [107]. For during infection. Determining whether the MAX
example, rice bakanae disease pathogen Fusarium fu- effectors have similar functions in pathogenesis and
jikuroi produces chemically similar GA that probably whether they can target conserved host proteins will
functions as a suppressor of host defense responses require further investigation.
through modulating hormonal balance in plants Maqbool et al. recently used biochemical, struc-
[107]. Many gall-forming bacteria and biotrophic tural, and activity-based assays to study how the
fungi produce cytokinins (CKs) that are required rice NLR protein Pik directly interacts with the M.
for the establishment of diseases [107]. However, oryzae effector Avr-Pik [112]. Coexpression of Pikp-
the underlying mechanism of CKs produced by HMA and Avr-PikD and the analysis of the 3D crys-
plant pathogens during infection remains largely tal structure of their complex revealed that Avr-PikD
unknown. Recently, Chanclud et al. identified the has high affinity binding to the so-called integrated
gene CKS1 (cytokinin synthesis 1) that is required HMA domain in Pikp [112]; this binding initiates
for CK synthesis and full virulence in M. oryzae immunity responses. Furthermore, mutated Avr-
[108]. Moreover, they showed that the CKs pro- PikD compromises the interaction with the Pikp-
duced by M. oryzae are important for dampening HMA domain and therefore abolishes the Avr-PikD-
host defense and affecting plant nutrients (sugar and Pikp-triggered defense response in rice [112].
AAs) distribution that facilitate for fungal growth Finally, a recent copurification and crystal
in and around the infection site [108], indicating structure study revealed that the Xanthomonas type
this fungal-secreted CKs are key effectors that are III effector AvrRox1-ORF1 binds to a molecular
similar with the TALE from bacteria. Interestingly, chaperone AvrRox1-ORF2 to form a tetramer
Bockhaven et al. recently found that rice plants complex with a distinct fold containing a novel
treated with 2 mM silicon (si) significantly increase kinase-binding domain [113]; the AvrRox1-ORF2
resistance to the brown spot fungus Cochliobolus chaperone is structurally different from typical
miyabeanus [109]. Rather than suppressing rice ET effector-binding chaperones. This tetramer complex
signaling, Si application increases resistance to rice is structurally homologous to zeta toxin:epsilon
brown spot probably through interfering with the antitoxin [113]. AvrRox1-ORF1 encodes a T4
production and/or action of ET in C. miyabeanus polynucleotide kinase-like domain that might
[109]. These results suggest that impairment of hor- directly phosphorylate a host target [113].
mone production in pathogens is an efficient strat-
egy to control plant diseases resistance.

BREEDING OF DISEASE-RESISTANT RICE

Researchers have estimated that crop yields must be
STRUCTURAL INSIGHT INTO increased by150% before 2030 to meet the global
RICE/PATHOGEN SYSTEMS food demand [114]. This increase in yield will be
Advances in X-ray crystallography promise to difficult to achieve because of many limiting factors
deepen our understanding of the recognition including pathogens. During the past decades, the
between plant NLRs and pathogen effectors at breeding of disease-resistant rice cultivars has greatly
the molecular level. The technique has been re- increased yield in China and several Asian countries.
cently used to analyze the interaction between For example, many R genes against M. oryzae, Xoo,
rice NLRs and M. oryzae effectors. According to and RSV have been integrated into new rice cultivars
X-ray crystallography, the Avr effector AvrPiz-t through marker-assisted selection and genetic engi-
adopts a six-stranded β-sandwich-fold structure, neering breeding strategies in China [114]. Readers
and Cys62 forms a disulphide bond with Cys75 are referred to a recent comprehensive review on the
[110]. de Guillen et al. recently used NMR spec- progress of rice molecular breeding in China [114].
304 Natl Sci Rev, 2016, Vol. 3, No. 3 REVIEW

In addition to conventional approaches, novel cerns related to genetically modified plants [125].
strategies based on host-induced gene silencing With this new method, transgenic plants were gen-
(HIGS), Xanthomonas spp. transcription activator- erated from the protoplasts of Arabidopsis thaliana,
like effector nucleases (TALENs), and a bacterial tobacco, lettuce, and rice transfected with purified
monomeric DNA endonuclease CRISPR-associated Cas9 protein and guide RNA. These plants con-
protein 9 (CRISPR/Cas9) have been successfully tain only small insertions or deletions that are indis-
used to increase resistance against pathogens in tinguishable from naturally occurring genetic varia-
plants. The first successful application of HIGS tions. In the future, improvements in the application
in disease control was the expression of papaya of CRISPR/Cas9 technology will likely lead to novel
ringspot virus (PSRV) coat protein in transgenic pa- and broad-spectrum disease resistance in crops.
paya plants to inhibit PSRV infection [115]. Grow-

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ing evidence suggests that the expression of dsRNA
molecules that target important genes in nematodes, CONCLUSION AND PERSPECTIVES
fungi, and even insects might also generate resistant
During the last two decades, tremendous progress
plants [116]. For instance, transgenic plants express-
has been made in understanding the innate immune
ing fungal virulence gene constructs can specifically
receptor complex in rice. More than 40 rice PRR
silence host targets in the case of the pathogenic
and R genes have been identified and functionally
fungi Blumeria graminis, Fusarium species, and Puc-
characterized. These genes help regulate the defense
cinia striiformis f.sp. tritici [117–119]. The use of
responses to bacterial, fungal, and viral pathogens.
HIGS to control rice blast and sheath blight is be-
Breakthroughs have included the determination of
ing studied in several laboratories and may gen-
rice immune receptors and how such receptors rec-
erate transgenic lines with resistance to multiple
ognize fungal and bacterial ligands, the understand-
pathogens if the target pathogen DNA sequence is
ing of the structure of the rice immune receptor
highly conserved.
complex, and the development of novel strategies
Genome-editing technology has great potential
for rice diseases management. Research is needed in
for the engineering of plants that have a broad spec-
the following areas: (1) the connections and interac-
trum of resistance but are free of antibiotic mark-
tions between the signaling components of rice PRR
ers. TALENs encode artificial bipartite enzymes
and NLR-mediated resistance for defense activation,
that consist of a modular DNA-binding domain
(2) the function of transcriptional factors that re-
and the FokI nuclease domain [120]. The DNA-
ceive signals from PRRs and NLRs and that control
binding domain has been engineered to recognize
the downstream defense gene activation in the nu-
a specific DNA sequence. The ability to precisely
cleus, (3) the role of epigenetic regulations in rice
edit a specific host gene, such as the target of a
immunity, and (4) the application of our increas-
bacterial virulence gene, can result in the develop-
ing understanding of rice innate immunity to achieve
ment of transgenic crops that thwart the virulence
disease control in rice fields.
strategy of Xanthomonas spp. For example, resis-
tant and hygromycin-free rice plants have been gen-
erated with TALEN technology; the resistance of
these plants is based on the targeting of the bacterial
ACKNOWLEDGEMENTS
blight susceptibility gene Os11N3 (also called Os- We thank Drs Huanbin Zhou and Yuese Ning for critically read-
SWEET14) [121]. The CRISPR/Cas9-based gene- ing this manuscript. We apologize to the colleagues whose work
could not be included in this review because of space limitations.
editing tool is becoming increasingly important. This
technology simply uses engineered 20 base pair (bp)
RNA guide sequence that binds to its DNA tar-
get site of interests to cause DNA cleavage and FUNDING
mismatching repairing or homologous replacement This work was supported by grants from the National Natural
[122]. To date, CRISPR/Cas9-based gene editing Science Foundation of China (31422045 and 31272034), the
has been used for many organisms, including the National Transgenic Crop Initiative (2012ZX08009001), and
model crop plants rice, maize, and wheat [123]. USDA-National Institute of Food and Agriculture (2013-68004-
20378).
Simultaneous editing of three mildew resistance lo-
cus o (Mlo) genes in hexaploid bread wheat led to
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