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Contents lists available at ScienceDirect

Seminars in Cell & Developmental Biology

journal homepage: www.elsevier.com/locate/semcdb

Review

Current understanding of pattern-triggered immunity and

hormone-mediated defense in rice (Oryza sativa) in response to
Magnaporthe oryzae infection
Fahad Nasir a,b , Lei Tian b , Chunling Chang b , Xiujun Li b , Yingzhi Gao a,∗ ,
Lam-Son Phan Tran c,d,∗ , Chunjie Tian b,∗
a
Key Laboratory of Vegetation Ecology, Institute of Grassland Science, Northeast Normal University, Changchun 130024, Jilin Province, China
b
Key Laboratory of Mollisols Agroecology, Northeast Institute of Geography and Agroecology, Chinese Academy of Sciences, Changchun 130102, Jilin
Province, China
c
Institute of Research and Development, Duy Tan University, 03 Quang Trung, Da Nang, Viet Nam
d
Signaling Pathway Research Unit, RIKEN Center for Sustainable Resource Science, Yokohama, Kanagawa, Japan

a r t i c l e i n f o a b s t r a c t

Article history: Plant pathogens represent a huge threat to world food security, affecting both crop production and
Received 15 July 2017 quality. Although significant progress has been made in improving plant immunity by expressing key,
Received in revised form defense-related genes and proteins from different species in transgenic crops, a challenge remains
21 September 2017
for molecular breeders and biotechnologists to successfully engineer elite, transgenic crop varieties
Accepted 20 October 2017
with improved resistance against critical plant pathogens. Upon pathogen attack, including infection
Available online xxx
of rice (Oryza sativa) by Magnaporthe oryzae, host plants initiate a complex defense response at molec-
ular, biochemical and physiological levels. Plants perceive the presence of pathogens by detecting
Keywords:
Hormones microbe-associated molecular patterns via pattern recognition receptors, and initiate a first line of innate
Magnaporthe oryzae immunity, the so-called pattern-triggered immunity (PTI). This results in a series of downstream defense
Oryza sativa responses, including the production of hormones, which collectively function to fend off pathogen attacks.
Pattern-triggered immunity A variety of studies have demonstrated that many genes are involved in the defense response of rice to
Transgenic crops M. oryzae. In this review, the current understanding of mechanisms that improve rice defense response
to M. oryzae will be discussed, with special focus on PTI and the phytohormones ethylene, jasmonic acid,
salicylic acid, and abscisic acid; as well as on the mediation of defense signaling mechanisms by PTI
and these hormones. Potential target genes that may serve as promising candidates for improving rice
immunity against M. oryzae will also be discussed.
© 2017 Elsevier Ltd. All rights reserved.

Contents

1. Introduction . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 00
2. Infection strategies of M. oryzae . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 00
3. Defense strategies in rice against M. oryzae . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 00
3.1. Role of PTI signaling in host defense against M. oryzae in rice . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 00
3.1.1. Sensing of M. oryzae and activation of PTI signaling . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 00
3.1.2. Co-components and signaling events downstream of PRRs . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 00
3.1.3. MicroRNAs (miRNAs) regulate PTI against M. oryzae . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 00
3.2. Hormone-mediated defense responses to M. oryzae in rice . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 00
3.2.1. ET-mediated defense against M. oryzae . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 00
3.2.2. JA-mediated defense against M. oryzae . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 00
3.2.3. SA-mediated defense against M. oryzae . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 00

∗ Corresponding authors.
E-mail addresses: gaoyz108@nenu.edu.cn (Y. Gao), son.tran@riken.jp (L-S.P. Tran), tiancj@neigae.ac.cn (C. Tian).

https://doi.org/10.1016/j.semcdb.2017.10.020
1084-9521/© 2017 Elsevier Ltd. All rights reserved.

Please cite this article in press as: F. Nasir, et al., Current understanding of pattern-triggered immunity and hormone-mediated defense in
rice (Oryza sativa) in response to Magnaporthe oryzae infection, Semin Cell Dev Biol (2017), https://doi.org/10.1016/j.semcdb.2017.10.020
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3.2.4. ABA-mediated susceptibility to M. oryzae . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 00

4. Bio-engineering strategies for enhancing M. oryzae resistance in rice . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 00
5. Future perspectives . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 00
Conflict of interest . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 00
Acknowledgments . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 00
References . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 00

1. Introduction 2. Infection strategies of M. oryzae

Rice (Oryza sativa) blast disease, the most destructive disease of M. oryzae has evolved a hemibiotrophic life-style, exhibiting a
rice globally, is caused by a filamentous ascomycetous fungus, Mag- biotrophic phase during the early stages of infection, after gain-
naporthe oryzae [1]. This disease is of immense importance because ing entry into the host [26]. M. oryzae infects both roots and aerial
it causes enormous reduction (about 10–30%) in the yield of rice, parts of rice plants, such as leaves, stems, nodes and panicles. Dur-
a grain crop that feeds approximately 50% of the world popula- ing the initial stage of infection, M. oryzae conidia adhere to foliar
tion [2,3]. Different host-specific strains of M. oryzae also infect tissues of the host plant. Subsequently, germ tubes produced by
many other economically important crops, such as foxtail millet the conidia develop into melanized appressoria, and a penetra-
(Setaria italica), finger millet (Eleusine coracana), barley (Hordeum tion peg breaches the leaf cuticle by generating a massive turgor
vulgare), wheat (Triticum aestivum) and a variety of grasses (e.g. pressure via the accumulation of glycerol; thus, gaining entry into
Lerrsia hexandra and Panicum repens) [2–4]. Rice blast disease is the epidermal cells of the host [26,27]. M. oryzae also secretes
typically controlled by the use of different fungicides, such as tricy- cell-wall-degrading enzymes (CWDEs) that facilitate the infection
clazole, probenazole, azoxystrobin, propiconazole, and iprobenfos process. Genetic disruption of the cutinase2 (CUT2) gene encoding
[5,6]. In addition to problems with the efficacy of these fungicides, the CWDE CUT2 of M. oryzae confirmed its pivotal role in facilitat-
there has been a growing concern over the use, misuse, and overuse ing appressorium formation and penetration [28]. RNA interference
of chemical fungicides, which can lead to potentially hazardous (RNAi)-mediated silencing of genes encoding cellulases belonging
health and environmental issues [7,8]. The use of crop varieties to glycosyl hydrolase 6 and 7 families, and endoxylanases resulted
with “race-specific” resistance is another reliable method of disease in a reduced infection ability in M. oryzae due to the impaired activ-
management; however, in the case of rice blast disease, resistance ities of these enzymes [29,30]. After gaining access to the host
is not durable, only lasting about two or three years, due to the tissues, M. oryzae utilizes plasmodesmata to spread to neighbor-
occurrence of new bio-types of M. oryzae that constantly overcome ing cells without causing any visible alterations in the cell walls of
host defense [9,10]. Thus, there is a critical need to improve rice the host [26].
immunity against M. oryzae using a transgenic approach to manip- In order to prevent activation of PTI in the host, M. oryzae also
ulate potential gene targets that have the potential to provide a delivers virulence protein factors (effectors), such as a secreted
more durable resistance to rice blast disease. lysin motif (LysM)-containing protein1 (Slp1), into the host rice
In order to cope with pathogen infection, including that of cells being invaded. The LysM effector binds to chitin fragments
M. oryzae, rice has evolved a sophisticated innate immunity sys- released from the cell walls of M. oryzae hyphae, preventing
tem, which is divided into two layers [11]. The first layer of host recognition of the chitin fragments by host-generated, chitin
defense in plants is the detection of the plant pathogen by the elicitor-binding protein (CEBiP); thus suppressing PTI and facilitat-
perception of microbe-associated molecular patterns (MAMPs) via ing pathogenesis [31]. As a countermeasure, rice cells recognize the
plasma membrane-localized pattern recognition receptors (PRRs), effector proteins through intracellular receptor proteins, termed
which then activates pattern-triggered immunity (PTI) to inhibit disease resistance (R) proteins, which activate ETI or race-specific
or prevent the establishment of the pathogen. Effector-triggered resistance [11]. M. oryzae also secretes elicitor proteins that serve
immunity (ETI) is the second layer of the innate immunity system. as virulence factors. For instance, knockout mutants of the M.
ETI provides a robust defense response that is often accompanied oryzae snodprot1 homolog (MSP1) gene encoding MSP1, a homolog
by a hypersensitive response at the infection site. ETI, however, of snodprot1 protein of Stagonospora nodorum, and the M. oryzae
is race-specific and fragile. Thus, it is not a very effective form of alpha-N-arabinofuranosidaseB (MoAbfB) gene, encoding an MoAbfB
resistance against the rice blast disease. Phytohormones, such as protein, exhibited decreased pathogenicity [32,33]. In order to
ethylene (ET), jasmonic acid (JA), salicylic acid (SA), and abscisic achieve successful infection, M. oryzae also represses host immu-
acid (ABA), have also been demonstrated to play an important role nity by impairing or hijacking hormone-based defense signaling
in rice response to M. oryzae infection [12–16]. pathways. For example, after invading cells, M. oryzae secretes an
The advent of advanced high-throughput -omics technologies, antibiotic biosynthesis-related monooxygenase into the host that
and the resulting availability of various types of -omics data, have can alter host JA into a hydroxylated form (12OH-JA) which disrupts
allowed for the identification of a large number of novel genes, pro- the JA-dependent defense network in the host, thereby facilitating
teins, and metabolites that are associated with the plant response fungal colonization [34]. M. oryzae also synthesizes its own ABA
to environmental stresses [17–21]. Recently, a number of ‘omics’ and cytokinins, and then uses them as virulence factors to atten-
analyses have been used to investigate the interaction of rice uate host immune responsiveness [15,35,36]. Recently, published
with M. oryzae, in order to identify the biochemical and molecu- reviews have provided a comprehensive description of the molec-
lar mechanisms underlying disease resistance and susceptibility. ular mechanisms associated with the infection of host cells by M.
This information could provide the foundation for understanding oryzae [37,38]. Disease lesions, which are common symptoms of M.
the genetic basis for resistance to the disease and the develop- oryzae disease, usually become visible as a result of host cell death
ment of better control strategies [21–25]. The current review will after 72–96 h of a successful infection of host tissues [26]. Under
focus on recent findings on the mechanisms and strategies used by high humidity conditions, M. oryzae produces copious amounts of
rice plants to inhibit or prevent M. oryzae infection, and the poten- spores inside the host, which then spread the disease and act as a
tial use of genetic engineering to develop rice cultivars with stable source of secondary dispersal, spreading the disease to neighboring
resistance to M. oryzae. plants.

Please cite this article in press as: F. Nasir, et al., Current understanding of pattern-triggered immunity and hormone-mediated defense in
rice (Oryza sativa) in response to Magnaporthe oryzae infection, Semin Cell Dev Biol (2017), https://doi.org/10.1016/j.semcdb.2017.10.020
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Table 1
List of genes that confer resistance to Magnaporthe oryzae when ectopically expressed in transgenic rice plants.

Gene Encoding protein Function References

OsLYP4 Receptor-like protein Chitin and peptidoglycan receptor [42]

OsLYP6 Receptor-like protein Chitin and peptidoglycan receptor [42]
CRPi Chimeric receptor protein Acts as a chitin receptor [46]
OsWAK1 Wall-associated protein kinase Confers resistance to M. oryzae [49]
OsWAK25 Wall-associated protein kinase Biotic and abiotic stress responses [50]
BSR1 Receptor-like cytoplasmic kinase Chitin-derived defense signaling [53]
OsWRKY53(SD) WRKY53 transcription factor Confers resistance to M. oryzae [60]
OsWRKY22 WRKY22 transcription factor Confers resistance to M. oryzae [61]
OsWRKY30 WRKY30 transcription factor JA-dependent defense [62]
OsWRKY45 WRKY45 transcription factor SA-dependent defense [63,91]
OsNAC6 NAC6 transcription factor Biotic and abiotic stress tolerance [64]
OsNAC111 NAC111 transcription factor Confers resistance to M. oryzae [65]
OsEIN2 Ethylene-insensitive 2 ET signal transduction [79]
OsEIL1 Ethylene-insensitive-3-like 1 ET signal transduction [79]
OsACS2 1-aminocyclopropane-1-carboxylate synthase 2 ET biosynthesis [81]
OsAOS2 Allene oxide synthase 2 JA biosynthesis [83]
OsJAMyb JAMyb transcription factor JA-dependent biotic and abiotic stress responses [86]
OsNPR1 Nonexpressor of pathogenesis-related genes 1 SA-dependent defense [89]
OsWRKY13 WRKY13 transcription factor OsNPR1-dependent defense [90]
OsWRKY47 WRKY47 transcription factor Confers resistance to M. oryzae [97]
ChiC Chitinase C Antifungal [99]
Gns1 1,3;1,4-ˇ glucanase Antifungal [100]
RIXI Xylanase inhibitor protein 1 Prevents the activity of fungal endo-1,4- ˇ-d-xylanases [101]
AGL ␣-1,3-glucanase Removes ␣-1,3-glucan [103]
MoSM1 Cerato-platanin protein Host defense activator protein secreted by M. oryzae [104]
MoHrip1 Elicitor protein MoHrip 1 Host defense activator protein secreted by M. oryzae [105]
MoHrip2 Elicitor protein MoHrip 2 Host defense activator protein secreted by M. oryzae [105]
OsBBI1 RING finger protein-like Fortifies plant cell wall [106]

3. Defense strategies in rice against M. oryzae
PTI and hormone-mediated defense responses are the most
effective defense strategies used by rice plants to cope with M.
oryzae (Figs. 1 and 2). Due to considerations regarding the length
of the current review, this section will only discuss recent progress
in understanding the regulation and molecular mechanisms of PTI
signaling in response to M. oryzae infection. Readers are referred to
two excellent reviews for understanding molecular mechanisms of
ETI in rice against M. oryzae disease [11,39].
3.1. Role of PTI signaling in host defense against M. oryzae in rice
3.1.1. Sensing of M. oryzae and activation of PTI signaling
Plants sense the presence of pathogens by their ability to detect
conserved MAMPs, such as fungal chitin, bacterial flagellin and
peptidoglycan via PRRs, which then activate PTI [40]. Activation
of PTI leads to various defense responses that include the induc-
tion of an oxidative burst, activation of mitogen-activated protein
kinase (MAPK or MPK) cascades, biosynthesis of hormones, accu-
mulation of antimicrobial compounds or enzymes, and callose
deposition (involved in the fortification of cell wall); which, as a
result, inhibits or prevent pathogen proliferation. Rice cells rec-
ognize M. oryzae chitin fragments through transmembrane LysM
receptor-like proteins (LysM-RLPs), such as CEBiP and its paralogs
lysin motif-containing proteins OsLYP4 and OsLYP6 [41,42]. CEBiP,
OsLYP4 and OsLYP6 have been shown to have the capacity to bind to
the rice chitin elicitor receptor kinase1 (OsCERK1) to make recep-
tor complexes that transmit chitin-derived signals (Fig. 1) [43,44].
In rice, RNAi-mediated silencing of either CEBiP, OsLYP4 or OsLYP6
resulted in increased susceptibility to M. oryzae [42,45]. In contrast,
overexpression of either CRPi, a chimeric gene possessing CEBiP and
Pi-d2 (coding for a ˇ-lectin receptor-like kinase) domains, or OsLYP4
or OsLYP6, improves resistance to M. oryzae in transgenic rice plants
(Table 1) [42,46]. In support of these results, OsCERK1-silenced
rice mutants exhibit suppressed levels of chitin-mediated defense
responses, including callose deposition, induction of immunity-
related genes, and the increase in the production of reactive oxygen
species (ROS) [43]. Thus, it is evident that chitin-derived signal-
ing initiated by LysM-RLPs–OsCERK1 receptor complexes plays an
essential role in disease resistance againt M. oryzae in rice.
In addition to MAMPs, various elicitor molecules, referred to as
host damage-associated molecular patterns (DAMPs), are released
from plant cell walls. These include the release of oligogalatur-
onides (OGs) in response to adverse biotic stress conditions, which
trigger a defense response [47]. For example, wall-associated
kinase1 (WAK1) serves as a DAMP receptor during an Arabidopsis-
Botrytis cinerea interaction, recognizing OGs released by the host,
resulting in increased resistance to B. cinerea [48]. What DAMPs
are released from rice plants during M. oryzae infection, and how
rice senses these DAMPs, however, are currently unresolved ques-
tions. It should be noted that overexpression of either OsWAK1
or OsWAK25 in transgenic rice increased resistance to M. oryzae
(Table 1) [49,50], raising an interesting question as to whether
or not the WAK cluster in rice contains the same functional OG-
binding domain found in Arabidopsis. Resolving this question may
identify OG receptor(s), as well as DAMP-based immune signals, in
rice that play an important role in its interaction with M. oryzae and
other pathogens.
3.1.2. Co-components and signaling events downstream of PRRs
Plants contain receptor-like cytoplasmic kinases (RLCKs) that
function downstream of PRRs, and play a central role in linking
PRRs to the downstream components for the activation of defense
responses [51]. For example, two independent studies have demon-
strated that chitin applications can elicit OsCERK1 in rice, and that
OsCERK1 then directly activates both OsRLCK185 and OsRLCK176
(Fig. 1) [43,52]. On the other hand, silencing of either OsRLCK185
or OsRLCK176 gene in rice compromised chitin-mediated defense
responses, including phosphorylation of the OsMPK3/OsMPK6,
expression of immunity-related genes, and ROS production [43,52].
The compromised ROS generation observed in both OsRLCK185-
and OsRLCK176-silenced mutants [43,52], suggests an interaction
of these RLCKs with ROS; however, the underlying details of such an
interaction have not been elucidated. Transgenic rice plants over-
expressing the broad-spectrum resistance1 (BSR1) gene, encoding

Please cite this article in press as: F. Nasir, et al., Current understanding of pattern-triggered immunity and hormone-mediated defense in
rice (Oryza sativa) in response to Magnaporthe oryzae infection, Semin Cell Dev Biol (2017), https://doi.org/10.1016/j.semcdb.2017.10.020
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Fig. 1. Diagrammatic representation of pattern-triggered immunity (PTI) signaling in rice in response to Magnaporthe oryzae infection. Chitin fragments released from M.
oryzae act as a microbe-associated molecular pattern (MAMP). MAMP is sensed by three LysM-RLPs: CEBiP; OsLYP4; and OsLYP6. Activated CEBiP, OsLYP4, and OsLYP6 bind
to the co-receptor OsCERK1 to form chitin-receptor complexes that regulate chitin signaling. Upon chitin perception, LysM-RLP–OsCERK1 complexes initiate two distinct (A)
OsRLCKs- and (B) OsRacGEF1-dependent chitin signaling pathways in rice, both of which are important for activation of PTI against M. oryzae. (A) The OsRLCKs (OsRLCK185,
OsRLCK176, and perhaps BSR1)-dependent pathway transduces the defense signal to downstream components, such as a MAPK cascade and perhaps H2 O2 . OsRLCK185 directly
individually interacts with and phosphorylates OsMAPKKK18 and OsMAPKKK␧ to activate OsMKK4. Activated OsMKK4 then phosphorylates OsMPK3/OsMPK6, which induces
the biosynthesis of phytoalexins, which are antimicrobial compounds. In addition, phosphorylated OsMPK4–OsMPK3/OsMPK6 activates OsWRKY53, which may upregulate
defense- and phytoalexin biosynthesis-related genes. (B) Upon chitin elicitation, LysM-RLP–OsCERK1 complexes mediate phosphorylation of OsRacGEF1, which in turn
activates OsRac1. Activated OsRac1 then phosphorylates OsMKK4. Phosphorylated OsMKK4 phosphorylates and thus activates OsMPK3/OsMPK6, which then phosphorylates
the OsRAI1 transcription factor. Activated OsRAI1 subsequently upregulates the expression of defense-related genes, leading to disease resistance. Phosphorylated OsRac1
also induces the production of lignin (a compound that strengthens and fortifies host cell walls) and H2 O2 through cooperation with OsCCR1 and OsRBOH, respectively. Upon
chitin treatment, LyM-RLP–OsCERK1-dependent activation of OsMKK4–OsMPK3/OsMPK6 leads to the production of phytoalexins. It remains to be determined, however,
whether or not phytoalexin production is OsRLCKs- and/or OsRacGEF1-dependent. Several rice microRNAs, such as miR160a and miR398b increase resistance to M. oryzae by
inducing the expression of defense-related genes. In contrast, Osa-miR169 negatively regulates resistance to the rice blast pathogen, M. oryzae by suppressing the expression of
defense-related genes. (C) Host damage-associated molecular pattern (DAMP) molecules such as OGs released during the rice-blast fungus interaction and DAMP receptor(s)
remain to be identified. (D) The RLPs, OsLYP4 and OsLYP6, as well as OsCERK1, function in callose deposition. The pathway responsible for callose deposition, however, has
not been characterized. Solid arrows indicate positive regulation and bars indicate inhibition. Dotted arrows indicate hypothetical or unidentified downstream signaling
components, and a dotted eclipse indicates an unidentified substrate. Abbreviations: BSR1, broad-spectrum resistance1; CEBiP, chitin elicitor-binding protein; GTP, guanosine
triphosphate; H2 O2 , hydrogen peroxide; LysM-RLPs, lysine motif-containing receptor-like proteins; MAPK, mitogen-activated protein kinase; MAPKK, MAPK kinase; MAPKKK,
MAPK kinase kinase; OGs, oligogalaturonides; OsCCR1, cinnamoyl-CoA reductase1; OsCERK1, chitin elicitor receptor kinase1; OsLYP, lysin motif-containing protein; OsRac1,
Rac/Rop protein; OsRacGEF1, Rac guanine nucleotide exchange factor1; OsRBOH, respiratory burst oxidase homolog; OsRLCKs, receptor-like cytoplasmic kinases; RAI1, Rac
immunity1; WAK(s), wall-associated kinase(s).

a RLCK, exhibited significantly enhanced resistance to M. oryzae
(Table 1) [53]. In contrast, a knockout mutation of BSR1 in rice sig-
nificantly suppressed chitin-triggered defense responses [54]. How
BSR1 conveys chitin-triggered signal to downstream components
for activation of defense responses to M. oryzae; however, remains
an open question.
The MAPK cascades in plants consist of a MAPK kinase
kinase (MAPKKK), a MAPK kinase (MAPKK or MKK), and a
MAPK that are present downstream of RLCKs; which perceive
and transmit MAMP-driven signals from RLCKs to downstream
components, leading to the activation of immune responses
[55]. For example, chitin elicitation in rice leads to the activa-
tion of OsMKK4–OsMPK3/OsMPK6, subsequently triggering the
accumulation of diterpenoid phytoalexins (DPs) that have antimi-
crobial activity [56]. Upon chitin recognition in Arabidopsis,
the phosphorylation of PBL27 (an ortholog of rice OsRLCK185)
by CERK1 phosphorylates AtMAPKKK5. Subsequently, phospho-
rylated AtMAPKKK5 then activates AtMKK4/MKK5–MPK3/MPK6
[57], suggesting that AtMAPKKK5 is involved in receiving and
propagating the chitin-induced signal from CERK1-PBL27 to MAPK

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Fig. 2. Schematic illustration of the ethylene (ET), jasmonic acid (JA), salicylic acid (SA) and abscisic acid (ABA) signaling pathways in rice regulating defense responses
against Magnaporthe oryzae. M. oryzae attack increases the production and signaling of ET by triggering the expression of ET biosynthesis- (OsACS2/6) and signaling-related
(OsEIN2 and OsEIL1) genes. Sensing of M. oryzae cell wall-derived MAMP(s) by rice also activates ET biosynthetic pathway. Activation of ET signaling positively regulates
callose deposition. M. oryzae-induced ET signaling also enhances the synthesis of H2 O2 and JA through OsEIL1 activation of OsRBOHa/b and JA biosynthesis-related OsPR4
genes, respectively. The accumulation of OsEIN2-dependent JA also activates the biosynthesis of diterpenoid phytoalexins (DPs). M. oryzae inoculation also activates the
production of JA and JA-isoleucine (JA-Ile) by inducing the expression of the genes involved, resulting in enhanced production of flavonoid phytoalexin (sakuranetin),
ultimately disease resistance to M. oryzae. The SA-mediated defense pathway in rice is divided into OsNPR1- and OsWRKY45-dependent pathways. Both signaling pathways
positively regulate defense responses against M. oryzae. OsWRKY13 acts upstream of OsNPR1 and induces OsNPR1 expression. Upon BTH treatment, the OsWRKY45-dependent
pathway positively regulates defense-related genes including DP biosynthetic genes by acting upstream of OsWRKY62 and downstream of the OsMKK10-2–OsMPK6 cascade.
In order to avoid autoimmune regulation of OsWRKY45-dependent defense signaling in the absence of defense signals (-SA/BTH), UPS constantly degrades OsWRKY45.
The ABA signaling pathway, which is induced by abiotic stresses, suppresses both ET- and SA-dependent defense pathways, and thus increases the susceptibility of rice
to M. oryzae. OsMPK5 and OsPTP1/2 are the convergence points through which ET-ABA and WRKY45-dependent SA-ABA crosstalk is mediated. M. oryzae also produces
ABA, which may be involved in regulating ABA signaling in the host, and consequently regulate SA- and ET-mediated defense response. Solid arrows indicate positive
regulation and bars indicate inhibition. Abbreviations: BTH, benzo (1,2,3) thiadiazole-7-carbothioic acid S-methyl ester; H2 O2 , hydrogen peroxide; MAMP(s), microbe-
associated molecular pattern(s); OsACS2/6, 1-aminocyclopropane-1-carboxylate synthase2/6; OsAOC, allene oxide cyclase; OsAOS2, allene oxide synthase2; OsEIL1, OsEIN3-LIKE1;
OsEIN2, ethylene insensitive2; OsNPR1, nonexpressor of pathogenesis-related genes1; OsOPR4, 12-oxo-phytodienoic acid reductase4; OsPTP1/2, protein tyrosine phosphatases1/2;
OsRBOH, respiratory burst oxidase homolog; UPS, ubiquitin–proteasome system.

cascade. Yamada et al. [58] recently reported that silencing of
OsMAPKKK18 (an ortholog of AtMAPKKK5) also suppressed chitin-
based OsMPK3/OsMPK6 activation in rice, indicating that the
chitin-activated MAPK signaling pathway is conserved in both rice
and Arabidopsis. OsRLCK185 was also confirmed to directly phos-
phorylate OsMAPKKK18, which then phosphorylates OsMKK4. In
turn, the phosphorylated OsMKK4 then activates OsMPK3/OsMPK6
by its phosphorylation [58]. This study also demonstrated that
OsRLCK176 did not cooperate with OsMAPKKK18, thus it is plausi-
ble that OsRLCK176 regulates the activation of OsMAPKs through
other OsMAPKKKs; however, this still needs to be confirmed. A
more recent study revealed that OsMAPKKKε-silenced rice lines
exhibited suppressed chitin-based OsMPK3/OsMPK6 activation, as
well as reduced resistance to M. oryzae [59]. In contrast, over-
expression of the OsMAPKKKε-kinase domain (OsMAPKKKε-KD) in
transgenic rice plants increased chitin-based OsMPK3/OsMPK6
activation, and upregulated defense-related genes. Furthermore,
OsRLCK185 has been shown to activate OsMAPKKK␧ by inter-
acting with its C-terminal domain, and activated OsMAPKKK␧
subsequently phosphorylates OsMKK4. Phosphorylated OsMKK4

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then induces phosphorylation of OsMPK3/OsMPK6, transmitting
the chitin-based immune signal [59]. Based on the above reports,
it is clear that OsMAPKKK18 and OsMAPKKK␧ are the first sig-
naling components in rice that are known to activate the MAPK
cascade and its downstream components by receiving and trans-
mitting chitin-driven immune signals from OsCERK1–OsRLCK185
to OsMKK4, and then to OsMPK3/OsMPK6 (Fig. 1). Further inves-
tigations are needed to examine how various OsMAPKs respond
to M. oryzae attack, and whether additional OsMAPKs are involved
in receiving and transmitting chitin-induced immune signals that
result in the activation of MAMP-mediated defense.
Upon pathogen infection, sequential activation of MAPKs leads
to the activation of various downstream transcription factors (TFs),
resulting in a reprogramming of immunity-related genes, and
consequently activation of immune responses [55]. For instance,
activation of the chitin-responsive OsMKK4–OsMPK3/OsMPK6 cas-
cade was reported to lead to the phosphorylation of OsWRKY53
TF [60], suggesting that OsWRKY53 is a downstream member
of the OsMKK4–OsMPK3/OsMPK6 cascade (Fig. 1). Further-
more, transgenic rice lines overexpressing a phospho-mimic
mutated version of OsWRKY53 (OsWRKY53SD) exhibited signif-
icantly increased resistance against M. oryzae (Table 1), along
with the upregulation of defense and phytoalexin (momilactone)
biosynthesis-related genes. In transgenic rice, ectopic overexpres-
sion of either OsWRKY22 or OsWRKY30 also improved resistance
to M. oryzae (Table 1) [61,62]. Importantly, overexpression
of pathogen-responsive OsWRKY45, under the control of the
pathogenesis-related protein1b (PR1b) promoter in combination
with the rice alcohol dehydrogenase (ADH) 5 -untranslated region
(5 -UTR), increased resistance to M. oryzae in transgenic rice under
field conditions, without yield penalties (Table 1) [63]. Trans-
genic rice plants overexpressing the NAC (NAM/ATAF/CUC) TF gene,
OsNAC6 or OsNAC111, also displayed increased resistance to M.
oryzae (Table 1) [64,65]. More recently, a novel, natural allele bsr-d1
of Bsrd-1, encoding a C2 H2 -type TF, was identified which promotes
a broad-spectrum resistance to M. oryzae by preventing the degra-
dation of hydrogen peroxide (H2 O2 ) [66]. Moreover, only 10% of
the rice varieties possess this novel allele. Thus, the bsr-d1 allele
can be utilized in breeding programs for developing rice varieties
with durable resistance to M. oryzae. The molecular mechanisms
underlying the activation of various TFs by M. oryzae infection are
largely unknown; and thus, require further investigations.
Upon chitin elicitation, OsCERK1 also rapidly activated the
downstream Rac guanosine triphosphate (GTP) exchange factor1
(OsRacGEF1) by phosphorylating its C-terminal S549, leading to
increased resistance to M. oryzae (Fig. 1) [67]. Activated OsRacGEF1
cooperates with and activates Rac/Rop protein (OsRac1), which
then phosphorylates OsMKK4–OsMPK3/OsMPK6 and subsequently
activates the Rac immunity1 (RAI1) TF; leading to induced
expression of defense-associated genes, such as OsWRKY19 and
phenylalanine ammonia lyase1 (OsPAL1) [67,68]. Furthermore,
activated OsRac1 also induces the production of H2 O2 and
cinnamoyl-CoA reductase1 (OsCCR1) (involved in lignin biosyn-
thesis) by interacting with the respiratory burst oxidase homolog
(OsRBOH) and OsCCR1 (Fig. 1) [67,69]. Based on current studies,
it is evident that after rice cells detect M. oryzae via LysM-
RLPs–OsCERK1 receptor complexes, the host plants trigger PTI
responses. The LysM-RLPs–OsCERK1-dependent chitin-induced
signal disseminates into RLCKs- and OsRacGEF1-dependent path-
ways. Both of these pathways are critical for the positive regulation
of PTI responses which are used to inhibit or prevent infection by
M. oryzae.
3.1.3. MicroRNAs (miRNAs) regulate PTI against M. oryzae
Emerging evidence has indicated that diverse pathogen-
inducible host miRNAs function as central regulators of gene
Please cite this article in press as: F. Nasir, et al., Current understanding of pattern-triggered immunity and hormone-mediated defense in
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expression, contributing to the regulation of PTI responses in rice
[70]. Deep sequencing of miRNA libraries from resistant and vul-
nerable rice varieties inoculated with M. oryzae has demonstrated
that a variety of miRNAs are differentially induced in response
to M. oryzae [71,72]. Recently, nine novel M. oryzae elicitor-
responsive miRNAs were identified in rice using high-throughput
Illumina sequencing [73]. Importantly, ectopic overexpression of
either miR160a or miR398b in transgenic rice resulted in enhanced
resistance to M. oryzae infection, concomitant with upregulated
expression of immunity-related genes and enhanced production of
H2 O2 at the infection site [71], indicating that they act as positive
regulators of rice defense against M. oryzae. In contrast, constitutive
overexpression of Osa-miR169 in rice increased its susceptibility
to M. oryzae by negatively regulating the expression of defense-
associated genes and compromising production of H2 O2 at the
infection site [74], suggesting that Osa-miR169 acts as a negative
regulator of rice defense responses to M. oryzae. How M. oryzae
infection or chitin application induces various miRNAs, and how the
induced miRNAs mediate PTI signaling remain to be determined.
3.2. Hormone-mediated defense responses to M. oryzae in rice
Upon infection, the biosynthesis of hormones and related sig-
naling pathways are activated in rice. ET, JA, and SA have been
known as positive signaling molecules involved in rice defense
against M. oryzae [12–14,75]. In contrast, ABA acts as a negative
modulator of host defense response to M. oryzae in rice [15,16]. This
section of the current review provides a discussion of recent find-
ings related to the role and signaling mechanism of ET, JA, SA, and
ABA in regulating host defense against M. oryzae. The roles of other
hormones, such as cytokinins, gibberellins, and auxins have been
discussed in detail in two recent reviews [75,76]. The function of the
newly identified phytohormone, strigolactone, in defense against
rice pathogens, including M. oryzae, has not been examined. Molec-
ular studies in Arabidopsis, however, have shown that strigolactone
can act as a positive regulator of both immunity and abiotic stress
responses [77,78].
3.2.1. ET-mediated defense against M. oryzae
M. oryzae challenge activates ET production and signaling
in rice by upregulating the expression of the genes involved
(Fig. 2) [12,79]. Besides, application of M. oryzae cell wall elicitors
also induces ET biosynthetic pathway in rice [12]. Rice ethy-
lene insensitive2ab (OsEIN2ab), and EIN3-LIKE1 (OsEIL1) mutants
altered in ET signaling, have exhibited attenuated resistance to
M. oryzae, and a reduction in callose deposition [12]. Silencing of
ET-biosynthetic 1-aminocyclopropane-1-carboxylic acid synthase2
(OsACS2) also showed susceptibility to M. oryzae but at less severe
level than the ET signaling mutants [12]. Consistent with this
premise, a recent report demonstrated that altering ET signaling,
by mutation in OsEIN2, markedly increased disease susceptibility of
rice to M. oryzae. The susceptibility was associated with a reduction
in ROS generation and a decrease in biosynthesis of DPs, e.g. momi-
lactone A and phytocassanes A, D and E [79]. In contrast, ectopic
overexpression of either OsEIN2 or OsEIL1 in transgenic rice plants
increased disease resistance to M. oryzae (Table 1). Furthermore,
it was shown that OsEIL1 is responsible for the upregulation of JA
biosynthesis-related 12-oxo-phytodienoic acid reductase4 (OsOPR4)
and OsRBOHa/b genes by interacting with their promoters [79].
These findings suggest that activation of ET signaling in the host
by M. oryzae results in JA accumulation, leading to increased DPs
production, as well as an induction of ROS. The exogenous applica-
tion of either cyanide (a co-product of the ET biosynthetic pathway)
or the ET precursor 1-aminocyclopropane-1-carboxylic acid, also
improved the resistance of susceptible rice lines to M. oryzae [80].
Moreover, OsACS2 transgenic rice plants exhibit increased ET pro-
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duction, and enhance host resistance to both M. oryzae and sheath [92]. Genetic and in vitro kinase studies have confirmed that the
blight (caused by Rhizoctonia solani), without causing a reduction in OsMKK10-2–OsMPK6 cascade acts upstream of OsWRKY45, and
growth and yield (Table 1) [81]. Collectively, these reports suggest receives SA-derived defense signals that it subsequently conveys to
that ET biosynthesis and ET signaling are critical to the positive reg- OsWRKY45; thereby activating defense responses against M. oryzae
ulation of rice resistance to M. oryzae. It would be of great interest (Fig. 2) [93]. A recent study also demonstrated that knockdown rice
to elucidate how M. oryzae-derived MAMPs trigger ET biosynthesis mutants of OsWRKY62 were highly susceptible to both M. oryzae and
and signaling. Xanthomonas oryzae pv. oryzae. This susceptibility was also accom-
panied with the suppression of defense-related genes, including DP
3.2.2. JA-mediated defense against M. oryzae biosynthetic genes [94]. In addition, BTH treatment induces the for-
JA enhances disease resistance to M. oryzae through its abil- mation of OsWRKY45–OsWRKY62 heterodimers, and upregulates
ity to promote the synthesis and accumulation of antimicrobial the DP factor (DPF) TF [94]. This TF positively regulates the expres-
compounds (Fig. 2) [13,82]. M. oryzae infection induces the expres- sion of DP biosynthetic genes, and consequently directly affects
sion of JA and JA-isoleucine (JA-Ile) biosynthesis-related genes, the production of DPs (Fig. 2) [94,95]. Collectively, these findings
resulting in enhanced production of JA and JA-Ile [79,83,84]. demonstrate that the SA defense signaling network in rice consists
It has been reported that coleoptile photomorphogenesis2 (cpm2) of two OsWRKY13–OsNPR1- and OsMPK6–OsWRKY45-dependent
and hebiba mutants lacking JA-biosynthetic allene oxide cyclase pathways that act together to inhibit or prevent M. oryzae infection
(OsAOC) exhibiting reduced levels of both endogenous JA and in rice.
M. oryzae-inducible phytoalexins display increased vulnerability
to M. oryzae [13]. Similarly, either JA-resistant1 (OsJAR1) Tos17
3.2.4. ABA-mediated susceptibility to M. oryzae
mutants or coronatine insensitive1 (OsCOI1) knockdown rice lines
Inoculation of rice with a compatible race of M. oryzae
with reduced stress-inducible JA-Ile biosynthesis and impaired JA
induces the expression of ABA-responsive genes in host cells
signaling, respectively, are hypersusceptible to M. oryzae [75,85].
[15]. Exogenous ABA treatment of rice inhibits the expression of
Notably, upon M. oryzae challenge the accumulation of flavonoid
defense-related genes, such as OsWRKY45 and OsNPR1, which play
phytoalexin (sakuranetin) but not DP was suppressed in OsJAR1
critical roles in SA-based defense; thus attenuating resistance to
Tos17 mutants compared to wild-type, suggesting that the sus-
M. oryzae (Fig. 2) [15]. Exogenously administered ABA has been
ceptibility of the OsJAR1 Tos17 mutants were especially due to the
recently shown to inactivate/dephosphorylate OsMPK6 in rice by
reduced accumulation of sakuranetin [85]. In contrast, transgenic
protein tyrosine phosphatases OsPTP1 and OsPTP2, resulting in the
rice plants overexpressing JA-biosynthetic allene oxide synthase2
suppression of OsWRKY45-dependent SA defense and decreased
(OsAOS2) showing elevated levels of JA and induced expression
resistance to M. oryzae, even after application of BTH [93]. Further-
of PR-genes are highly resistant to M. oryzae (Table 1) [83]. In
more, it was revealed that abiotic stresses such as high salinity and
rice, overexpression of a JA-responsive myeloblastosis (MYB) gene,
low temperature also suppress an OsWRKY45-dependent signal-
OsJAMyb, conferred a significant increase in resistance to M. oryzae
ing pathway in rice probably via ABA-dependent inactivation of
in transgenic lines (Table 1) [86]. The underlying molecular mech-
OsMPK6 through OsPTP1 and OsPTP2 [93]. In contrast, OsPTP1/2
anism of OsJAMyb-mediated defense against M. oryzae, however,
double knockdown rice mutants exhibit strong resistance to M.
remains to be elucidated. The combined findings of these reports
oryzae, even when cold or salt stress is present, suggesting that host
indicate that JA synthesis, and thus JA-mediated signaling, plays an
plants prioritize abiotic stress response over defense response by
important positive regulatory role in the rice defense response to
switching off OsWRKY45-dependent SA defense signaling through
M. oryzae.
crosstalk of ABA and SA via the activation of OsPTP1 and OsPTP2
(Fig. 2) [93].
3.2.3. SA-mediated defense against M. oryzae
An earlier study demonstrated that ABA treatment reduces ET
M. oryzae does not induce SA production in rice plants to any
production and markedly increases susceptibility of ABA-treated
significant degree [76,87]. Transgenic rice plants overexpressing
rice plants to M. oryzae (Fig. 2) [16]. In addition, impairment of
NahG, which encodes a salicylate hydroxylase, are SA-deficient
ET signaling by silencing of OsEIN2b results in hypersensitivity to
and hypersusceptible to the oxidative stress induced by M. oryzae
ABA and reduced resistance to M. oryzae [16]. In contrast, RNAi-
infection [88]. This suggests that SA modulates redox balance and
mediated silencing of ABA-inducible OsMPK5 in rice increases ET
defends host cells from the oxidative damage induced by M. oryzae
levels and reduces ABA accumulation, while concomitantly increas-
[88]. Silencing of the SA-responsive marker gene, OsNPR1 (nonex-
ing rice resistance to M. oryzae [16]. These findings suggest that
pressor of PR genes1), results in suppression of PR-genes (coding
OsMPK5 is the convergent point, which regulates the crosstalk
for PR-proteins) and increased vulnerability to M. oryzae in rice
between ABA and ET signaling pathways in rice. Interestingly, a
[89]. In contrast, overexpression of OsNPR1 triggers the expression
considerable amount of ABA has been found in both M. oryzae
of PR-genes in transgenic rice plants, and confers resistance to M.
hyphae and its culture filtrates. This source of ABA may play a
oryzae (Table 1) [89]. Related to this finding, ectopic overexpression
role in the regulation of host ABA signaling, and consequently
of OsWRKY13 in transgenic rice plants results in improved dis-
defense responses [15]. In addition, disruption of ABA production
ease resistance to M. oryzae (Table 1), by upregulating OsNPR1 [90],
in M. oryzae by deletion of the ABA biosynthesis-related ABA4 gene
suggesting that OsNPR1 is a downstream substrate of OsWRKY13
resulted in reduced pathogenicity in M. oryzae [36]. In summary,
(Fig. 2).
ABA decreases host resistance to M. oryzae by impairing SA and
In addition, treatment of rice plants with the SA analog,
ET defense-signaling pathways in plants. In contrast, it increases
benzo (1,2,3) thiadiazole-7-carbothioic acid S-methyl ester (BTH),
virulence in M. oryzae.
induces the expression of different OsWRKY genes, including
OsWRKY45 [91]. Silencing of OsWRKY45 in rice compromised
BTH-induced resistance to M. oryzae infection, suggesting that 4. Bio-engineering strategies for enhancing M. oryzae
OsWRKY45 is a crucial component for BTH-mediated defense resistance in rice
responses to M. oryzae [91]. Moreover, during the absence
of defense signals (-SA/BTH), the ubiquitin–proteasome system Advancements in -omics technologies have provided a better
(UPS) negatively regulates OsWRKY45 by constant degradation understanding of the molecular and genetic aspects of plant-
of OsWRKY45 as a mechanism to avoid autoimmune regulation pathogen interactions, and thus enabled the development of

Please cite this article in press as: F. Nasir, et al., Current understanding of pattern-triggered immunity and hormone-mediated defense in
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novel disease management strategies [96]. High-throughput -
omics studies, including genomics, transcriptomics, proteomics
and metabolomics, are tools that can be used to dissect the molec-
ular mechanisms underlying rice-M. oryzae interactions, and have
provided an expanding list of disease resistance-related genes
which can be potentially used to develop cultivars with broad, sta-
ble resistance through conventional breeding and biotechnology.
For example, transcriptome analyses have revealed the importance
of various MAPK and WRKY genes in the rice-M. oryzae interaction
[24,97]. Subsequently, some of these genes, including OsWRKY47,
have been shown, as summarized in Table 1, to confer enhanced
resistance to M. oryzae when they are overexpressed in transgenic
rice plants [97].
Genomics studies of M. oryzae led to the identification of a large
number of CWDEs, some of which have been functionally char-
acterized [98]. M. oryzae uses CWDEs, e.g. cutinases, cellulases,
and endoxylanases, as virulence factors. Besides, chitin and ˇ-1,3
glucan are crucial cell wall components of M. oryzae. Thus, the
dependence of M. oryzae on CWDEs and cell wall components can
be manipulated to engineer effective resistance of rice against M.
oryzae infection. For example, transgenic rice lines overexpress-
ing the chitinase C (chiC) gene from Streptomyces griseus HUT6037
not only exhibited an increased hydrolyzing activity against glycol
chitin, but also this resulted in enhanced resistance to M. oryzae in
the transgenic rice (Table 1) [99]. Similarly, ectopic overexpression
of Gns1, encoding a 1,3;1,4-ˇ glucanase, in transgenic rice plants
resulted in the production of resistant-type lesions in response
to M. oryzae inoculation (Table 1) [100]. Additionally, transgenic
rice plants overexpressing rice xylanase inhibitor (RIXI), coding for
a xylanase inhibitor protein (which inhibits the activity of fun-
gal endo-1,4-␤-D-xylanases), exhibited increased resistance to M.
oryzae (Table 1) [101]. M. oryzae covers the surface of its own
cell walls with a ␣-1,3-glucan polysaccharide, which not only pro-
tects the M. oryzae cell wall from hydrolyzing activities induced
by the host digestive enzymes, but also prevents host PRRs from
detecting PAMPs to avoid the activation of host innate defense
[102]. Notably, transgenic rice plants overexpressing a Bacillus
circulans ˛-1,3-glucanase gene (AGL) exhibit the production of bac-
terial ␣-1,3-glucanase 9, an enzyme which functions in the removal
of fungal ␣-1,3-glucan. These transgenic plants displayed a high
level of resistance to M. oryzae, Rhizoctonia solani, and Cochlioborus
miyabeanus (Table 1) [103].
Controlling the elicitor proteins secreted by M. oryzae may
also be a useful approach for preventing M. oryzae infection.
Overexpression of genes encoding M. oryzae-derived elicitor pro-
teins in transgenic rice can activate plant defense responses and
increase resistance to M. oryzae [104,105]. For example, transgenic
rice plants overexpressing MoSM1 (also called MoMSP1) exhibit
increased resistance to two different races of M. oryzae without
any reductions in yield or abiotic stress tolerance (Table 1) [104].
Ectopic overexpression of either M. oryzae hypersensitive response-
inducing protein elicitor1 (MoHrip1) or MoHrip2 in transgenic rice
conferred strong resistance to M. oryzae, as well as high tolerance
to drought stress; along with improved agronomic traits (Table 1)
[105].
Rice cells fortify their cell walls in order to impede the penetra-
tion of M. oryzae. The fortified cell walls serve as a physical barrier
to M. oryzae invasion, and such fortification may potentially be
strengthened using genetic engineering. For instance, overexpres-
sion of blast and BTH-induced1 (OsBBI1), coding for a RING finger
protein with E3 ligase activity, enhanced resistance to M. oryzae
by strengthening the cell wall defense system in transgenic rice
(Table 1) [106]. Identification and characterization of the upstream
and downstream components of OsBBI1 may help to better under-
stand the relevant cell wall-mediated defense pathways in rice
plants. Increasing experimental evidence has indicated that phy-
Please cite this article in press as: F. Nasir, et al., Current understanding of pattern-triggered immunity and hormone-mediated defense in
rice (Oryza sativa) in response to Magnaporthe oryzae infection, Semin Cell Dev Biol (2017), https://doi.org/10.1016/j.semcdb.2017.10.020
toalexin accumulation is a principle and critical defense response.
For example, rice produces a considerable amount of phytoalexins
in response to M. oryzae challenge [107]. Moreover, rice Syn-copalyl
diphosphate synthase4 (OsCPS4)-tos knockdown mutants exhibit
reduced levels of the phytoalexins momilactones and oryzalexin
S, and are less resistant to M. oryzae [108]. Thus, OsCPS4 represents
a potential candidate gene that can be used in the future in genet-
ically engineered plants to provide durable resistance against M.
oryzae, and perhaps other pathogens.
The collective evidence supports the premise that engineering
resistance to critical pathogens using transgenic approaches is an
efficient and environmentally sound strategy for providing disease
resistance to M. oryzae in rice at a commercial level. The genes listed
in Table 1 represent promising candidates but require additional
in-depth functional studies prior to their use in developing rice vari-
eties with enhanced resistance to M. oryzae without any reduction
in yield under field conditions.
5. Future perspectives
Long-lasting resistance, durable resistance to rice blast disease,
caused by M. oryzae, is dependent on PTI and hormone-associated
immunity. Although a basic model of PTI and hormone-based
defense signaling in rice in response to M. oryzae has been estab-
lished, the whole picture is not yet complete. The identification of
the host DAMP molecules that are released in rice in response to M.
oryzae, as well as their corresponding recognition receptor(s), are
still unknown. The mechanism by which various RLCKs transduce
MAMP-derived immune signals and activate downstream compo-
nents, such as MAPKs and ROS, also requires further investigation.
The molecular mechanisms responsible for the activation of dif-
ferent TF-encoding genes also deserve further investigation. How
M. oryzae inoculation triggers host hormone biosynthesis and sig-
naling is another interesting topic for future in-depth analyses.
While many host resistance mechanisms against M. oryzae are
well-documented, how host plants tolerate M. oryzae is poorly
understood. Further studies in all of these mentioned areas of
research will help scientists better understand the defense signal-
ing events and mechanisms that occur in rice in response to the
presence of M. oryzae and subsequent infection. A precise under-
standing of the rice-M. oryzae host-pathogen interaction is essential
due the potential impact that M. oryzae can have on global rice
production. Therefore, there is a great need for plant scientists
around the world to work together to determine the molecular
components of defense-related signaling pathways using differ-
ent modern −omics technologies, and forward and reverse genetic
screening techniques. Such a communal effort will enable the sci-
entific community to precisely identify and characterize defense-
and infection-related genes, proteins and metabolites, as well as
their signaling components. This information, in turn, will allow
for the development of strategies to genetically engineer durable
resistance to M. oryzae in rice plants, and thus will enable us to
achieve the ultimate goal of ensuring sustainable food security.
Conflict of interest
The authors declare no conflict of interest.
Acknowledgments
This work was supported in part by the Chinese Academic
Project B (XDB1503010), the National Project (2016YFC0501202),
the National Natural Science Foundation of China (41571255,
31370144), the National Key Basic Research Program of China
G Model
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F. Nasir et al. / Seminars in Cell & Developmental Biology xxx (2017) xxx–xxx
(2016YFC0500703), and the National Natural Science Foundation
of China (31670446, 31270444).
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Please cite this article in press as: F. Nasir, et al., Current understanding of pattern-triggered immunity and hormone-mediated defense in
rice (Oryza sativa) in response to Magnaporthe oryzae infection, Semin Cell Dev Biol (2017), https://doi.org/10.1016/j.semcdb.2017.10.020