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Arms and ammunitions: effectors at the interface of rice and it’s pathogens and pests

December 2021
Rice 14(1)

DOI:10.1186/s12284-021-00534-4

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CC BY 4.0

Authors:

Sohini Deb

University of Copenhagen

Vishnu Narayanan Madhavan

University of Southern Denmark

Gokulan C.G.

Centre for Cellular and Molecular Biology

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The plant immune system has evolved to resist attack by pathogens and pests. However, successful phytopathogens deliver effector proteins into plant cells where they hijack the host cellular machinery to suppress the plant immune responses and promote infection. This manipulation of the host cellular pathways is done by the pathogen using various enzymatic activities, protein- DNA or protein- protein interactions. Rice is one the major economically important crops and its yield is affected by several pathogens and pests. In this review, we summarize the various effectors at the plant- pathogen/ pest interface for the major pathogens and pests of rice, specifically, on the mode of action and target genes of the effector proteins. We then compare this across the major rice pathogens and pests in a bid to understand probable conserved pathways which are under attack from pathogens and pests in rice. This analysis highlights conserved patterns of effector action, as well as unique host pathways targeted by the pathogens and pests.

Overview of rice-Xoo interaction with a focus on effectors during pathogenesis. The Xoo-rice interaction is an example of a complex multi-layered arms race between the pathogen and host with effectors playing remarkable roles in determining the pathogenicity. Xoo gains access to the plant cellular contents through digesting the cell wall. This is achieved via secreting an array of cell wall degrading enzymes (CWDEs, shown as different coloured pie shapes) through the type II secretion system (1). The damage-associated molecular patterns (DAMPs) from degradation products of CWDEs and pathogen-associated molecular patterns (PAMPs) are sensed by specific receptors at the plasma membrane (2). This activates downstream signalling cascades (3) such as MAPK signalling leading to activation of transcription factors and upregulation of defense genes, resulting in defense responses such as callose deposition, programmed cell death, and release of ROS (4). The effector proteins secreted via the type III secretion system are directly delivered into the plant cell cytoplasm (5). These effectors consist of transcription activator-like (TAL) effectors, which are DNA binding proteins that upregulate plant genes leading to further susceptibility (6) (Classical example is SWEET gene upregulation in Xoo-rice interaction). Another class of T3S effectors—non-TAL effectors -are involved in dampening the immune responses by targeting defense signalling pathways, working directly or indirectly by binding to plant proteins (7). The plant counters these effectors using multiple mechanisms. This involves the executor R genes whose transcription is activated by TAL effectors leading to strong immune response and thus resistance (8), and by resistance proteins that target effectors directly or indirectly (9)

…

The infection strategy of M. oryzae. The spore of the fungi germinates and generates an appressorium. The appressorium penetrates the barriers of cuticle and cell wall, extending the invasive hyphae (IH), invaginating the plant plasma membrane. This plant plasma membrane covering the IH is known as the extrainvasive hyphal membrane (EIHM) and the matrix between the plant and fungal plasma membranes forms the extrainvasive hyphal matrix (EIHMx). The first bulbous IH forms in the biotrophic invasion complex (BIC), which is the specialised region of EIHMx for fungal secretions. EIHMx forms the interface for interactions between the plant and fungi. The fungal IH continue to grow in the plant invading new cells and forming new BIC regions through plasmodesmata

…

Effector secretory routes of M. oryzae. The fungal effector secretion takes place via vesicles and follows two routes. The BFA-insensitive vesicle secretion from endoplasmic reticulum (ER) which forms the BIC (1), which is destined for the plant cell cytoplasm, and the BFA-sensitive effector secretion, via Golgi apparatus, which is directed to the EIHMx (2). The effectors secreted to the EIHMx are the apoplastic effectors (violet pie shapes) and secretions from BIC are the cytoplasmic effectors (yellow pie shapes). The cytoplasmic effectors further localise to specific cell compartments such as the nucleus or plasmodesmata (3) or bind their target proteins (4), or have enzymatic activity, to compromise the plant cell and enable fungal growth. The plant cell cytoplasm is shown in green, bright yellow region represents BIC and BIC along with violet represents EIHMx or apoplasm

…

Schematic representation of BPH-Rice interaction. Using its stylet, the insect pierces the rice tissue and reaches the phloem to suck the sap. During this process, both gelling and watery saliva are secreted by the insect, which contain various molecules that elicit or act against plant defense. Proteins like catalase, endoglucanase, and Ca²⁺-binding proteins might be involved in suppressing the plant defense while proteins like Mucin-like proteins, Apolipophorins, and Protein disulfide isomerase elicit immune responses. Some of these proteins were found to induce callose deposition, cell death and SA or JA- associated defense gene expression

…

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Debetal. Rice (2021) 14:94

https://doi.org/10.1186/s12284-021-00534-4

REVIEW

Arms andammunitions: eectors

attheinterface ofrice andit’s pathogens

andpests

Sohini Deb1,2, Vishnu Narayanan Madhavan1, C. G. Gokulan1, Hitendra K. Patel1* and Ramesh V. Sonti1,3*

Abstract

The plant immune system has evolved to resist attack by pathogens and pests. However, successful phytopathogens

deliver eﬀector proteins into plant cells where they hijack the host cellular machinery to suppress the plant immune

responses and promote infection. This manipulation of the host cellular pathways is done by the pathogen using vari-

ous enzymatic activities, protein- DNA or protein- protein interactions. Rice is one the major economically important

crops and its yield is aﬀected by several pathogens and pests. In this review, we summarize the various eﬀectors at the

plant- pathogen/ pest interface for the major pathogens and pests of rice, speciﬁcally, on the mode of action and tar-

get genes of the eﬀector proteins. We then compare this across the major rice pathogens and pests in a bid to under-

stand probable conserved pathways which are under attack from pathogens and pests in rice. This analysis highlights

conserved patterns of eﬀector action, as well as unique host pathways targeted by the pathogens and pests.

Keywords: Rice, Eﬀectors, Immunity, Pathogen, Pest, Disease

permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the

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to the material. If material is not included in the article’s Creative Commons licence and your intended use is not permitted by statutory

regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this

licence, visit http:// creat iveco mmons. org/ licen ses/ by/4. 0/.

Background

e growing global population necessitates increased

food production even as resources such as water and

land are becoming limiting and environmental concerns

dictate lesser use of inputs such as fertilizers and pesti-

cides. To ensure food security and sustainable agricul-

tural practices, the development of newer crop varieties

is necessary. is involves addressing various aspects,

such as yield and tolerance to biotic and abiotic stresses.

e biotic stresses include plant diseases caused by bac-

teria, fungi and viruses as well as damage caused by nem-

atodes and insect pests. Understanding the molecular

intricacies of these plant-pathogen/pest interactions can

be an important aid in developing disease tolerant plant

varieties. A major role in the success of these pathogens

and pests is played by the class of molecules, known as

“eﬀectors”. Eﬀectors secreted by pathogens/pests can

function in gaining entry into the plant, obtaining access

to its nutrients, to suppress host defense responses and

to eventually multiply in or on the plant. ese eﬀectors

can either be proteins or metabolites. Because of their

importance in promoting infection/infestation, a better

understanding of eﬀector biology can potentially help in

conceptualizing newer strategies for developing biotic

stress tolerant plant varieties. Numerous reviews have

extensively covered eﬀector biology from the perspec-

tive of the pathogens (Franceschetti et al. 2017; Dean

etal. 2012; Toruno etal. 2016; Varden etal. 2017; Dou

and Zhou 2012). is article aims to review eﬀectors

deployed by the pathogens and pests of rice and identify

any common strategies that they may be targeting.

Oryza sativa, or rice, is the staple food for nearly half

of the global population and is an economically impor-

tant crop across nations (Khush 2005). Its production

is constantly threatened by many diﬀerent diseases/

pests. On an average, farmers lose an estimated 37% of

their rice crop to diseases and pests every year (http://

Open Access

*Correspondence: hkpatel@ccmb.res.in; sonti@ccmb.res.in

1 CSIR-Centre for Cellular and Molecular Biology (CSIR-CCMB),

Hyderabad 500007, India

Full list of author information is available at the end of the article

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Page 2 of 21

Debetal. Rice (2021) 14:94

www. knowl edgeb ank. irri. org). Various pathogens and

pests have been described in rice, although the biology

of their eﬀectors has been explored only in a few of the

major pathogens. Two members of the bacterial genus

Xanthomonas cause the serious bacterial blight (BB) and

bacterial leaf streak (BLS) diseases. Magnaporthe ory-

zae causes blast of rice and is a well-established fungal

disease model in rice. Other emerging rice- pathogen

disease models among ﬁlamentous pathogens include

the fungus Rhizoctonia solani and Pythium oomycetes

species. About 20 species of insects are known to cause

signiﬁcant economic damage in rice (http:// www. knowl

edgeb ank. irri. org). Some important pests of the rice plant

include brown plant hopper (BPH), gall midge and yellow

stem borer.

Research on rice-pathogen/pest interaction at the

molecular level is a very active ﬁeld and warrants more

investigation. is review seeks to highlight the informa-

tion available for rice in a comprehensive manner, also

emphasizing on the need for further characterisation of

the host targets of eﬀectors secreted by pathogens and

pests.

Main Text

Bacterial Pathogens: Microscopic butDevastating

Xanthomonas includes a large group of plant pathogenic

Gram- negative bacteria which infect more than 200 dif-

ferent plant species (Boch and Bonas 2010; Buttner and

Bonas 2010). Depending on the host range, and symp-

tomology on a host, they have been grouped into diﬀer-

ent pathovars (pv.) (Dye etal. 1980). e primary mode

of entry for Xanthomonas bacteria into rice plants are

natural openings like stomata and hydathodes. X. oryzae

pv. oryzae (Xoo) causes bacterial blight (BB) and X. ory-

zae pv. oryzicola (Xoc) causes bacterial leaf streak (BLS)

in rice. Infection sites are characterised by water-soaked

lesions and chlorosis, and often become necrotic. Xoo

and Xoc use eﬀectors secreted through diﬀerent types

of protein secretion systems, such as the type II secre-

tion system (T2SS) and the type III secretion system

(T3SS) (Fig. 1). Eﬀectors can thus be divided into two

broad groups: those acting in the extracellular spaces of

host tissues (apoplastic) or those acting within host cells

(cytoplasmic) (Carella et al. 2018). Apoplastic eﬀectors

are secreted via the T2SS of bacterial pathogens (Chang

et al. 2014). ese molecules are typically involved in

the enzymatic degradation of plant cell walls, immune

evasion, or the suppression of host proteolytic activ-

ity (Toruno etal. 2016; Wang and Wang 2018). e cell

wall degrading enzymes secreted by Xoo serve to breach

the cell wall, but the damage that they cause also triggers

host immune responses (Fig.1). To suppress and evade

host immune responses, Xoo secretes eﬀector proteins

into plant cells via its T3SS. e T3SS apparatus is a

needle-like structure spanning both the bacterial mem-

branes which injects the eﬀectors directly into the plant

cell (Weber etal. 2005). Hence these eﬀectors are termed

as “cytoplasmic eﬀectors”, their site of action being inside

the plant cell (Khan etal. 2018). Xanthomonas type III

eﬀector proteins are classiﬁed either as Transcription

activator-like (TAL) eﬀectors which have a DNA bind-

ing domain or non-TAL eﬀectors (also known as Xan-

thomonas outer proteins or Xops) which lack the same

(Buttner and Bonas 2010; White and Yang 2009).

Apoplastic Eectors: The Two‑Edged Swords

As part of its virulence strategy, Xoo secretes a bat-

tery of plant cell wall– degrading enzymes (CWDEs)

using its T2SS (Jha et al. 2005, 2007). e Xoo genome

contains a single gene cluster encoding for proteins of

the type II secretion system (Lee etal. 2005). e T2SS

secreted CWDEs are important virulence determinants

of the pathogen (Ray etal. 2000; Tayi etal. 2016a, 2016b;

Rajeshwari etal. 2005). Action of these CWDEs on the

rice cell wall results in damage that is sensed by the host

and leads to induction of immune responses.

Proteins secreted by the T2SS include CWDEs such

as xylanase (Ray etal. 2000; Rajeshwari etal. 2005; Qian

et al. 2013), cellulase/endoglucanase (Sun et al. 2005;

Furutani etal. 2004), putative cysteine protease (Furu-

tani etal. 2004), cellobiosidase (Tayi etal. 2016a, 2018),

lipase/esterase (Aparna etal. 2009), an extracellular pro-

tease EcpA (Zou etal. 2012), endoglucanase EglXoB (Hu

etal. 2007), etc. A number of these CWDEs have been

shown to be required for full virulence on rice and some

of them have also been shown to be involved in eliciting

host immune responses inplanta (Tayi etal. 2016a; Jha

et al. 2005). ese immune responses are further sup-

pressed by the type III secreted eﬀectors, or the cytoplas-

mic eﬀectors.

Cytoplasmic Eectors: The Tale oftheTALEs

e cytoplasmic eﬀectors consist of TAL eﬀector pro-

teins (TALEs) and non-TAL eﬀector proteins. e TAL

eﬀector proteins enter the nucleus and execute their role

as transcription factors by activating the expression of

plant susceptibility genes (Boch and Bonas 2010). TAL

eﬀector family proteins typically consist of an N-terminal

secretion signal and a variable number of near- identi-

cal repeats of a 34–amino acid sequence (Mudgett 2005;

Bonas etal. 1989; Hopkins etal. 1992). ey also have at

least one nuclear localisation signal (NLS), and an acidic

activation domain (AAD) at the C- terminus (Gurlebeck

etal. 2006). Both Xoo and Xoc express a large number of

TAL eﬀectors, exceeding eight in Xoo isolates and over

twenty in Xoc isolates (Wilkins etal. 2015; Salzberg etal.

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Page 3 of 21

Debetal. Rice (2021) 14:94

2008; Bogdanove et al. 2011). Some of the most con-

served TAL eﬀectorsgenes are avrXa7, pthXo1, pthXo2

and pthXo3 (Yang and White 2004). Loss of these four

eﬀectors from Xoo results in highly reduced virulence

and aﬀects symptom development (Bai etal. 2000; Yang

and White 2004). e target genes of these eﬀectors are

commonly referred to as susceptibility genes. Mutations

in the promoters of these genes render these host genes

non-responsive to TAL eﬀectors and they function as

recessive resistance genes. An alternate response of the

plant is a strong suppression of disease development in

response to diverse TAL eﬀectors, such as what is medi-

ated by the Xo1 resistance locus (Triplett etal. 2016).

e target genes of the TAL eﬀectors are a diverse class

of genes, the major targets being transcription factors,

receptor kinases or SWEET genes (Mücke etal. 2019).

Fig. 1 Overview of rice-Xoo interaction with a focus on eﬀectors during pathogenesis. The Xoo-rice interaction is an example of a complex

multi-layered arms race between the pathogen and host with eﬀectors playing remarkable roles in determining the pathogenicity. Xoo gains

access to the plant cellular contents through digesting the cell wall. This is achieved via secreting an array of cell wall degrading enzymes (CWDEs,

shown as diﬀerent coloured pie shapes) through the type II secretion system (1). The damage-associated molecular patterns (DAMPs) from

degradation products of CWDEs and pathogen-associated molecular patterns (PAMPs) are sensed by speciﬁc receptors at the plasma membrane

(2). This activates downstream signalling cascades (3) such as MAPK signalling leading to activation of transcription factors and upregulation of

defense genes, resulting in defense responses such as callose deposition, programmed cell death, and release of ROS (4). The eﬀector proteins

secreted via the type III secretion system are directly delivered into the plant cell cytoplasm (5). These eﬀectors consist of transcription activator-like

(TAL) eﬀectors, which are DNA binding proteins that upregulate plant genes leading to further susceptibility (6) (Classical example is SWEET gene

upregulation in Xoo-rice interaction). Another class of T3S eﬀectors—non-TAL eﬀectors -are involved in dampening the immune responses by

targeting defense signalling pathways, working directly or indirectly by binding to plant proteins (7). The plant counters these eﬀectors using

multiple mechanisms. This involves the executor R genes whose transcription is activated by TAL eﬀectors leading to strong immune response and

thus resistance (8), and by resistance proteins that target eﬀectors directly or indirectly (9)

Content courtesy of Springer Nature, terms of use apply. Rights reserved.

Page 4 of 21

Debetal. Rice (2021) 14:94

e well- characterised R-genes that confer tolerance

against Xoo are Xa1, xa5, Xa7, Xa10, xa13, Xa21, Xa23,

Xa27, and Xa3/Xa26 (Song etal. 1995; Yoshimura etal.

1998; Iyer and McCouch 2004; Sun etal. 2004; Chu etal.

2006b; Gu etal. 2005; Xiang etal. 2006; Wang etal. 2015;

Tian etal. 2014; Chen etal. 2021) (Table1). e Xa21

gene encodes a leucine rich repeat (LRR)-type recep-

tor kinase and interacts with the E3 ligase XB3 (Xa21

Binding Protein 3) (Wang etal. 2006; Song etal. 1995).

e elicitor of Xa21 mediated resistance is a sulphated-

tyrosine containing peptide secreted by Xoo called RaxX

(da Silva et al. 2004; Shen and Ronald 2002; Burdman

et al. 2004; Pruitt etal. 2015). xa13 encodes a plasma

membrane protein (Chu et al. 2006b), Xa1 encodes a

nucleotide-binding site–LRR protein (Yoshimura et al.

1998) and Xa3/Xa26 encodes an LRR receptor kinase-

like protein (Sun etal. 2004; Xiang etal. 2006). Another

class of R-genes, called executor R-genes, have also been

cloned and characterised. is class include the genes

Xa7, Xa10, Xa23, and Xa27. Common features of these

genes are (i) their expression is observed only in the

presence of a cognate TAL eﬀector in the infecting Xoo

strain, (ii) the gene induction occurs only in resistant

cultivars, (iii) induction of these genes results in hyper-

sensitive response (HR) and thus resistance to Xoo. Xa7,

Xa10, Xa23, and Xa27 were shown to be respectively

induced by their cognate TAL eﬀectors and leading to

HR and resistance to Xoo (Gu et al. 2005; Wang etal.

2015; Tian etal. 2014; Chen etal. 2021). Further, Xa10

has been shown to be localised in endoplasmic reticulum

(ER) as a hexamer and could trigger cell death by ER Ca2+

depletion via a conserved mechanism (Tian etal. 2014).

Xa7 was shown to be highly induced at high tempera-

ture regime (35℃) and is proposed as a suitable source

for resistance to Xoo considering the global tempera-

ture changes. Notably, among all the TAL eﬀectors that

induce executor R-genes, only AvrXa7 has been shown to

be essential for Xoo virulence (Chen etal. 2021).

Many of the TALEs target a class of sugar transport-

ers known as the SWEET genes, eg., PthXo1, PthXo6

and PthXo7. e TAL eﬀector PthXo1 binds to the pro-

moter region of OsSWEET11 (also called Os8N3 or

Xa13), which is a sucrose transporter gene to induce its

expression and promote bacterial pathogenicity. e

rice gene xa13 is a recessive resistance allele of Os8N3

(Yang etal. 2006; Antony etal. 2010; Chu etal. 2006a)

and is not induced by PthXo1, whereas the susceptible

gene Xa13 is pathogen inducible. is recessive allele,

however, can be overcome by strains of Xoo producing

any one of the type III TAL eﬀectorsAvrXa7, PthXo2, or

PthXo3. Both AvrXa7 and PthXo3 induce the expression

of Os11N3/ OsSWEET14, another SWEET gene which

apparently compensates for the inability of Xoo to induce

xa13 (Antony etal. 2010; Yuan and Wang 2013). e TAL

eﬀector PthXo2 also induces OsSWEET13 (also known as

xa25 in the rice cultivar Minghui 63) (Zhou etal. 2015).

us, TALEs target multiple sugar transporters in the

SWEET gene family, likely facilitating sugar export for

bacterial consumption (Chen etal. 2010). is has been

directly demonstrated for PthXo2 wherein heterologous

expression ofits target OsSWEET13inNicotiana bentha-

miana leaf cells elevated sucrose concentrations in the

leaf apoplasm (Zhou etal. 2015).

Table 1 TAL eﬀectors of Xoo

TAL eector Target gene Target gene family References

TalB OsTFX1 OsERF#123 bZIP transcription factor

AP2/ERF transcription factor Tran et al. (2018)

TalC OsSWEET14 Plasma membrane protein (sucrose transporter) Streubel et al. (2013)

AvrXa7 OsSWEET14/ Os11N3

Xa7

Plasma membrane protein (sucrose transporter)

Executor R-gene (of unknown function) Antony et al. (2010), Yuan and

Wang (2013) and Chen et al.

(2021)

AvrXa10 Xa10 Trans-membrane protein localised to the endoplasmic

reticulum membrane (Executor R-gene) Tian et al. (2014)

AvrXa23 Xa23 Trans-membrane protein (Executor R-gene) Wang et al. (2014)

AvrXa27 Xa27 Executor R-gene (of unknown function) Gu et al. (2005)

PthXo1 OsSWEET11/Os8N3 Plasma membrane protein (sucrose transporter) Yang et al. (2006)

PthXo2 OsSWEET13/xa25 Plasma membrane protein (sucrose transporter) Zhou et al. (2015)

PthXo3JXOV CDS1, CDS2, CDS3

OsSWEET14

Unknown

Plasma membrane protein (sucrose transporter) Li et al. (2018a)

PthXo3PXO99A OsSWEET14/Os11N3 Plasma membrane protein (sucrose transporter) Antony et al. (2010)

PthXo6 OsTFX1 bZIP transcription factor Sugio et al. (2007)

PthXo7 OsTFIIAɣ1Small subunit of the transcription factor IIA Sugio et al. (2007)

Content courtesy of Springer Nature, terms of use apply. Rights reserved.

Page 5 of 21

Debetal. Rice (2021) 14:94

Other targets of Xoo TAL eﬀectors include OsTFX1 and

OsTFIIAɣ1, the small subunit of the transcription factor

IIA (Sugio etal. 2007). e resistant allele of OsTFIIAɣ5

is encoded by xa5 (Iyer and McCouch 2004; Blair etal.

2003). In order to overcome the resistance mediated

by xa5, PthXo7 is used by the bacteria to increasethe

expression of OsTFIIAɣ1 (Ma etal. 2018).

More recently, "truncTALEs," for "truncated TAL

eﬀectors", alternatively known as interfering TALEs, or

iTALEs, have been described in the Xoo strain PXO99A

as well as in Xoc BLS256, which suppress disease resist-

ance. As compared to typical TALEs, these proteins lack

a transcription activation domain and are expressed

from genes that were previously considered pseudogenes

(Read etal. 2016; Ji etal. 2016, 2020a).

The Xoo Non‑TAL Eectors

In Xoo, 16 non-TAL eﬀectors were initially identiﬁed. Out

of these, nine eﬀectors shared homology with previously

identiﬁed T3S eﬀectors in other plant-pathogenic bacte-

ria whereas seven eﬀectors appeared to be Xoo speciﬁc

(Furutani etal. 2009). Expression of the type III eﬀectors

is regulated by genes that regulate the hrp cluster (hyper-

sensitive response and pathogenicity), speciﬁcally, hrpG

and hrpX (Song and Yang 2010). Many of these eﬀectors,

were shown to be required for the full virulence of the

strain (Gupta etal. 2015; Song and Yang 2010; Zhao etal.

2013; Mondal etal. 2016).

True to their putative function, the type III eﬀectors

were shown to suppress immune responses. XopZPXO99A

suppressed callose deposition induced by treatment of a

T3SS– strain (Song and Yang 2010). XopRXoo enhances

the growth of Xanthomonas campestris pv. campestris

T3SS− in Arabidopsis, probably by suppression of PAMP

(pathogen-associated molecular pattern) -triggered

early-defense genes, for example, a leucine-rich repeat

protein kinase, a cysteine/histidine-rich C1 domain

family protein, Flg22-induced receptor-like kinase 1

(FRK1) and a member of CYP81F, induced by the T3SS−

mutant (Akimoto-Tomiyama etal. 2012). Furthermore,

XopRPXO99A suppresses PAMP-triggered stomatal closure

in transgenic Arabidopsis expressing XopRPXO99A (Wang

et al. 2016b). Expression of XopPXoo in rice strongly

suppresses peptidoglycan (PGN)- and chitin-triggered

immunity and tolerance to X. oryzae (Ishikawa et al.

2014). XopQBXO43, as well as XopX BXO43 were shown

to suppress plant defense responses by targeting 14-3-3

proteins of rice, which are adapter proteins in signalling

pathways (Deb etal. 2019, 2020).

Interestingly, these eﬀectors seem to be targeting a var-

ied number of pathways, indicating towards the involve-

ment of these pathways in immune responses (Table2).

XopNKXO85 was shown to interact with a thiamine

synthase (OsXNP) and OsVOZ2 (a transcription factor)

(Cheong etal. 2013). Since treatment with thiamine was

shown to enhance resistance to pathogen invasion in rice

(Ahn etal. 2005, 2007), XopN seems to suppress immune

responses by blocking thiamine synthesis. Another type

III non-TAL eﬀector, XopY was shown to inhibit the

phosphorylation of the receptor kinase OsRLCK185

and the downstream MAPK signalling, and hence pro-

mote pathogenesis (Yamaguchi etal. 2013b). Later it was

further shown that this receptor kinase is involved in

theperception of both peptidoglycan (PGN) as well as

chitin signalling, indicatingfor its possible involvement

in response to bacterial and fungal pathogens (Wang

etal. 2017). Another eﬀector which may have a role in

interfering with peptidoglycan and chitin induced signal-

ling is the Xoo eﬀector XopPXoo, which targets OsPUB44,

a rice ubiquitin E3 ligase. XopPXoo was shown to directly

interact with the U-box domain of OsPUB44 and inhibit

ligase activity. Silencing ofOsPUB44suppressed PGN-

and chitin-triggered immunity (Ishikawa etal. 2014). On

the other hand, XopL itself exhibits E3 ubiquitin ligase

activity and interacts with ferredoxin (NbFd), to target

it for ubiquitination and ubiquitin-mediated degrada-

tion, thereby increasing reactive oxygen species (ROS)

production (Ma etal. 2020). XopI has also been shown

to act as a F-box adapter and interacts with a thioredoxin

protein, OsTrxh2, to strongly inhibit the host’s OsNPR1-

dependent resistance to Xoo (Ji etal. 2020b).

XopAA strongly inhibited host resistance to X. oryzae,

possibly by interaction with OsBAK1 (BRI1—associ-

ated kinase). OsBAK1 interacts with FLS2, the receptor

kinase sensor of the PAMP ﬂg22, in the initial steps of

its signalling, making it an essential component of sig-

nalling responses induced by PAMPs (Chinchilla et al.

2007). OsBAK1 is also a co- receptor of the hormone

brassinosteroid (BR) (Wang etal. 2008), suggesting that

the virulence promoting activity of XopAA is mediated

by the inhibition of OsBAK1 (Yamaguchi etal. 2013a).

Similarly, XopRPXO99A was shown to interact with BIK1, a

receptor-like cytoplasmic kinase (RLCK) and appears to

be phosphorylated by it. BIK1 mediates PAMP-triggered

stomatal immunity. In addition, XopR was seen to associ-

ate with other RLCKs as well apart from BIK1 and thus

may suppress plant immunity by targeting RLCKs (Wang

etal. 2016b; Akimoto-Tomiyama etal. 2012).

Eectors Employed byFilamentous Pathogens ofRice

e ﬁlamentous pathogens such as fungi and oomycetes

are known to cause devastating plant diseases leading

to signiﬁcant yield losses worldwide. Some of the fungal

diseases of rice include rice blast caused by Magnaporthe

oryzae (M. oryzae), rice sheath blight caused by Rhizoc-

tonia solani, false smut of rice caused by Ustilaginoidea

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Page 6 of 21

Debetal. Rice (2021) 14:94

virens, sheath rot of rice caused by Sarocladium ory-

zae and bakanae disease caused by Gibberella fujikuroi

(Elazegui and Islam 2003). In addition, the oomycete

genus Pythium is also known to cause diseases in rice

(Van Buyten and Hofte 2013).

e ﬁlamentous pathogens have evolved a large rep-

ertoire of secreted eﬀectors of various functions, which

play a major role in disease progression. With respect to

rice-ﬁlamentous pathogen biology, the most well-studied

pathogen is M. oryzae (Dean etal. 2012; Pennisi 2010).

us, the scope of this review would primarily be refer-

ring to theeﬀectors of M. oryzae.

The ‘Blast’ byMagnaporthe oryzae

e ascomycete fungus M. oryzae, causative agent of

rice blast, is classiﬁed as one of the most devastating

plant pathogens (Pennisi 2010; Dean etal. 2012). Dur-

ing the infection cycle, the fungal spore attaches to the

leaf surface, germinates and the germ tube forms a spe-

cialised cell called appressorium, which develops the

fungal hyphae and uses turgor pressure to insert the

hyphae into the plant cell. e fungal hyphae invade

plant tissues and cause necrotrophy, leading to disease

lesions. M. oryzae gains access into the plant cytoplasm

by inserting the invasive hyphae (IH) through the cell

wall. e infection strategy of M. oryzae is outlined in

Fig.2.

e growing tips of primary IH and ﬁrst bulbous IH

retain the biotrophic invasion complex (BIC) which is the

specialised region at primary IH for secretion of eﬀec-

tors (Khang etal. 2010; Yan and Talbot 2016). e BIC

is a plant membrane-derived structure formed upon the

invasion by fungus (Giraldo etal. 2013). Eﬀector secre-

tion at the BIC continues as the IH grow and branch in

the plant cell. rough plasmodesmata the IH enter-

ing the neighbouring cell forms the BIC again. e BIC

structure is a feature of successful infection and is not

observed in resistant plants (Mosquera etal. 2009; Khang

etal. 2010; Jones etal. 2016; Shipman etal. 2017).

Recently the fungal MAP Kinase, Pathogenicity MAP-

Kinase 1 (PMK1) was shown to control the constriction

of IH at the plasmodesmata to invade the neighbouring

cells and regulate the expression of various eﬀectors to

suppress rice immune responses (Sakulkoo et al. 2018;

Table 2 Non-TAL eﬀectors of Xoo

Eector Localisation Pathway inhibited/relevant information

XopC Cytoplasmic (Wang et al. 2016b)

XopF Chloroplast (predicted) (Zhao et al. 2013)

XopG Suppression of XopQ- XopX mediated immune responses (Deb et al. 2020)

XopI Acts as a F-box adapter and interacts with a thioredoxin protein, OsTrxh2, to strongly inhibit the

host’s OsNPR1-dependent resistance to Xoo

Required for complete virulence in rice (Ji et al. 2020b)

XopL Cytoplasmic (Wang et al. 2016b) Exhibits E3 ubiquitin ligase activity and interacts with ferredoxin (NbFd), to target it for ubiquit-

ination and ubiquitin-mediated degradation, thereby increasing reactive oxygen species (ROS)

production (Ma et al. 2020)

XopN Thiamine synthesis (Cheong et al. 2013)

Suppresses PGN- triggered MAPK activation (Long et al. 2018)

XopP Chloroplast (predicted) (Zhao et al. 2013) Suppresses PGN- and chitin-triggered immunity and resistance and targets OsPUB44, a rice

ubiquitin E3 ligase (Ishikawa et al. 2014)

Suppression of XopQ- XopX mediated immune responses (Deb et al. 2020)

XopQ Nucleo- cytoplasmic (Deb et al. 2019) 14-3-3 mediated suppression of rice immune responses (Deb et al. 2019)

Required for complete virulence in rice (Gupta et al. 2015)

XopR Plasma membrane (Zhao et al. 2013) Receptor kinase interaction (Wang et al. 2016b)

Immune response suppression (Akimoto-Tomiyama et al. 2012)

Required for complete virulence in rice (Zhao et al. 2013)

XopU Suppression of XopQ- XopX mediated immune responses (Deb et al. 2020)

XopV Cytoplasmic (Wang et al. 2016b) Suppresses PGN- triggered MAPK activation (Long et al. 2018)

Suppression of XopQ- XopX mediated immune responses (Deb et al. 2020)

XopW Cytoplasmic (Wang et al. 2016b)

XopX Nucleo- cytoplasmic (Deb et al. 2020) 14-3-3 mediated suppression of rice immune responses (Deb et al. 2020)

XopY Chitin & PG induced MAPK signalling (Yamaguchi et al. 2013b)

XopZ Suppresses PGN- triggered MAPK activation (Long et al. 2018)

XopAA Receptor kinase interaction & Brassinosteroid signalling (Yamaguchi et al. 2013a)

XopAE Chloroplast (predicted) (Zhao et al. 2013)

AvrBs2 Suppression of XopQ- XopX mediated immune responses (Deb et al. 2020)

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Page 7 of 21

Debetal. Rice (2021) 14:94

Eseola etal. 2021). is secretion of a repertoire of eﬀec-

tors in a co-ordinated manner and with spatio-temporal

dynamics plays a major role in M. oryzae infection.

Apoplastic Eectors: ‘The Players atthePeriphery’

e eﬀectors that remain in and are targeted to plant

apoplast are known as apoplastic eﬀectors. e apo-

plastic eﬀectors follow a classical Golgi-dependant

secretory pathway, which is sensitive to treatment by

Brefeldin A (BFA). e apoplastic eﬀectors are mostly

localised in the extrainvasive hyphal matrix (EIHMx)

lining the fungal cell (Giraldo etal. 2013) (Fig.3). For

example, among the apoplastic eﬀectors, the biotro-

phy associated secreted (BAS) proteins have been

described, which are a class of small cysteine-rich

secreted proteins (Giraldo etal. 2013), some of which

have been shown to localise in the EIHMx as well as at

cell wall crossing points of IH (Mosquera et al. 2009;

Khang etal. 2010).

Among the apoplastic eﬀectors of M. oryzae, one

functionally well-described eﬀector is the secreted

LysM (lysine motif) protein 1 (SLP1). Being an apoplas-

tic eﬀector, SLP1 accumulates in the EIHMx and com-

petes with the rice pattern recognition receptor protein

LysM protein, chitin elicitor binding protein (OsCE-

BiP), to bind chitin oligosaccharides and suppress

chitin-induced immunity (Mentlak etal. 2012; Giraldo

et al. 2013). Another apoplastic eﬀector found to be

competing with the OsCEBiP is MoAa91, a M. oryzae

Fig. 2 The infection strategy of M. oryzae. The spore of the fungi germinates and generates an appressorium. The appressorium penetrates

the barriers of cuticle and cell wall, extending the invasive hyphae (IH), invaginating the plant plasma membrane. This plant plasma membrane

covering the IH is known as the extrainvasive hyphal membrane (EIHM) and the matrix between the plant and fungal plasma membranes forms

the extrainvasive hyphal matrix (EIHMx). The ﬁrst bulbous IH forms in the biotrophic invasion complex (BIC), which is the specialised region of EIHMx

for fungal secretions. EIHMx forms the interface for interactions between the plant and fungi. The fungal IH continue to grow in the plant invading

new cells and forming new BIC regions through plasmodesmata

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Page 8 of 21

Debetal. Rice (2021) 14:94

homolog of the auxiliary activity family 9 protein (Aa9)

(Li etal. 2020).

Cytoplasmic Eectors: ‘The Internal Intruders’

e cytoplasmic eﬀectors have primarily been shown to

be secreted and concentrated at the BIC and are even-

tually translocated to the plant cell cytoplasm. Some of

the cytoplasmic eﬀectors are also known to translocate

Fig. 3 Eﬀector secretory routes of M. oryzae. The fungal eﬀector secretion takes place via vesicles and follows two routes. The BFA-insensitive vesicle

secretion from endoplasmic reticulum (ER) which forms the BIC (1), which is destined for the plant cell cytoplasm, and the BFA-sensitive eﬀector

secretion, via Golgi apparatus, which is directed to the EIHMx (2). The eﬀectors secreted to the EIHMx are the apoplastic eﬀectors (violet pie shapes)

and secretions from BIC are the cytoplasmic eﬀectors (yellow pie shapes). The cytoplasmic eﬀectors further localise to speciﬁc cell compartments

such as the nucleus or plasmodesmata (3) or bind their target proteins (4), or have enzymatic activity, to compromise the plant cell and enable

fungal growth. The plant cell cytoplasm is shown in green, bright yellow region represents BIC and BIC along with violet represents EIHMx or

apoplasm

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Debetal. Rice (2021) 14:94

into neighbouring cells via plasmodesmata (Khang etal.

2010). e cytoplasmic eﬀectors follow a Golgi- inde-

pendent secretory pathway involving the exocyst (Exo70

and Sec5) and t-SNARE (Sso1) complexes, via the endo-

plasmic reticulum. Hence, cytoplasmic eﬀector secretion

is BFA-insensitive (Giraldo etal. 2013) (Fig.3).

Some examples include PWL2, Avr-Piz-t, and some

BAS proteins (Mosquera etal. 2009; Khang etal. 2010).

e cytoplasmic eﬀector BAS107 has been shown to

localise to the plant cell nucleus, suggesting a compart-

mental specialisation for the eﬀectors. BAS1 and BAS2

were shown to preferentially localise to theBIC (Mos-

quera etal. 2009), and BAS107 and BAS1 translocated to

uninvaded neighbouring plant cells via plasmodesmata

(Khang etal. 2010). Among the small glycine-rich PWL

(Pathogenicity toward Weeping Lovegrass) proteins, the

cytoplasmic PWL1 and PWL2 have beenshown to accu-

mulate at theBIC, and PWL2 has been demonstrated

to move from cell-to-cell via plasmodesmata (Sweigard

etal. 1995; Kang etal. 1995; Khang etal. 2010).

One of the functionally well-characterised cytoplasmic

eﬀectors is Avr-Piz-t, which has been shown to interact

with multiple proteins in the host (Li etal. 2009). Avr-

Piz-t has been shown to interact with a RING-domain E3

ubiquitin ligase, Avr-Piz-t Interacting Protein 6 (APIP6).

e interaction leads to the ubiquitination of Avr-Piz-t

and degradation of both Avr-Piz-t and APIP6, resulting

in the suppression of PAMP-triggered immunity and

increased susceptibility of rice (Park etal. 2012). e R

gene, Piz-t, surprisingly does not have any direct inter-

action with the eﬀector. Meanwhile, Piz-t is targeted

for degradation by a second RING-domain E3 ubiqui-

tin ligase, APIP10. APIP10 also interacts with Avr-Piz-t

leading to its ubiquitination and degradation of both

APIP10 and Avr-Piz-t. is degradation of APIP10 leads

to stabilization of Piz-t and initiation of ETI (Park etal.

2016). e interaction of Avr-Piz-t with a bZIP transcrip-

tion factor, APIP5, suppresses the function of APIP5 to

promote eﬀector-triggered necrotrophic cell death in

rice (Wang etal. 2016a). A virulence target of Avr-Piz-t

is the protein APIP12, a homologue of nucleoporin pro-

tein, Nup80, with which it interacts and reduces the basal

resistance against M. oryzae (Tang etal. 2017). APIP4, a

Bowman-Birk-type trypsin Inhibitor (BBI), interacts with

Avr-Piz-t leading toa reduction in its trypsin inhibitor

activity (Zhang etal. 2020). Avr-Piz-t also interacts with

the Potassium (K+) channel protein OsAKT1, to suppress

the rice innate immunity (Shi etal. 2018), and with the

rice homologue of human small GTPase, OsRac1, to sup-

press the reactive oxygen species (ROS) production by

the host (Bai etal. 2019).

Like Avr-Piz-t, another cytoplasmic eﬀector Avr-Pii

also interacts with more than one host protein and plays

distinct roles in promoting pathogenesis. e interaction

of rice exocyst complex protein OsExo70-F3 with Avr-

Pii is necessary for immunity triggered by the cognate R

protein, Pii (Fujisaki etal. 2015). Like other cytoplasmic

eﬀectors, Avr-Pii accumulates atthe BIC and in rice cells,

it interacts and inhibits the rice NADP-malic enzyme2

(Os-NADP-ME2). Inhibition of Os-NADP-ME2 reduces

the NADPH levels, reducing the host ROS burst (Singh

etal. 2016).

A family of structurally conserved fungal eﬀectors

has been described to share a conserved sixβ-sandwich

structures with no signiﬁcant sequence similarity.ese

eﬀectors were named as MAX-eﬀectors (Magnaporthe

Avrs and ToxB-like), and include Avr-CO39, Avr-Pia,

Avr-Piz-t, and ToxB (an eﬀector of the wheat tan spot

pathogen) (de Guillen etal. 2015). e Avr-CO39 eﬀec-

tor has been shown to localise to the endoplasmic retic-

ulum in the rice protoplast (Ribot et al. 2013), and is

recognised by the NB-LRR protein pair, RGA4 & RGA5

(R-gene analog), which also recognize Avr-Pia. Both Avr-

CO39 and AvrPia were shown to bind RGA5 (Cesari etal.

2013).

M. oryzae eﬀectors have been found to aﬀect multi-

ple hormone signalling pathways as well. e M. oryzae

hypothetical eﬀector, MoHEG16 was shown to be neces-

sary for thesuppression of cell death caused by M. oryzae

necrosis- and ethylene-inducing protein 1 (Nep1)-like

proteins (MoNLPs) (Mogga etal. 2016). e interaction

of M. oryzae cytoplasmic eﬀector NIS1 with the rice

receptor like kinase, OsBAK1, inhibits the kinase activ-

ity to suppress PTI (Irieda etal. 2019). IUG6 and IUG9

were identiﬁed as novel eﬀectors, among other candidate

genes in a new isolate of M. oryzae, showing a BIC locali-

sation and suppression of salicylic acid and ethylene sig-

nalling (Dong etal. 2015).

Other than functional proteins, various metabolites or

hormones have been shown to support theinfection of

M. oryzae. e enzyme, antibiotic biosynthesis monooxy-

genase (Abm), was shown to convert free jasmonic acid

(JA) to Hydroxylated JA (12OH-JA), which helps the fun-

gus to evade the rice immune responses. Abm localises

to the fungal endoplasmic reticulum and BIC, indicating

that Abm could be a secreted protein. us, both fungal

derived enzymes and products of their activity together

impart their action as eﬀectors (Patkar etal. 2015). e

avirulence conferring enzyme 1(ACE1), an appressoria-

localised eﬀector protein, produces a secondary metab-

olite, which is the eﬀector rather than the protein itself

(Bohnert etal. 2004; Collemare etal. 2008). Like ACE1,

the TAS1 enzyme has been shown to produce the well-

characterised mycotoxin Tenuazonic acid (TeA) (Yun

etal. 2015). Similarly, another enzyme, cytokinin synthe-

sis 1, CSK1, was shown to be involved in active cytokinin

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Page 10 of 21

Debetal. Rice (2021) 14:94

production by M. oryzae. e cytokinin from fungus was

shown to be involved in increasing metabolic availability,

reducing defense responses and altering gene expression,

thus suggesting that the cytokinin secreted by M. oryzae

could be a classical eﬀector (Chanclud etal. 2016). ese

studies implicate that the fungal secondary metabolites

function as eﬀectors and play key roles in disease pro-

gression. Table3 summarises all the discussed M. oryzae

eﬀectors.

Insect Pests

Rice is infested by a wide range of insect pests. e major

insect pests include planthoppers, namely brown plan-

thopper (BPH; Nilaparvata lugens), whitebacked plan-

thopper (WBPH; Sogatella furcifera), smaller brown

planthopper (SBPH; Laodelphax striatellus) and green

rice leafhopper (GRH; Nephotettix cincticeps). Stembor-

ers and Asian rice gall midge (Orseolia oryzae) are other

major pests of rice (Bentur etal. 2016). Apart from dam-

aging the crop by ingesting the phloem sap, many of

these insects also transmit viruses that cause diseases in

rice (Huang etal. 2019b).

Diﬀerent insects have diﬀerent ways of obtaining their

food. Among the piercing-sucking insects, BPH shows

intracellular probing while GRH shows intercellular

probing (Sōgawa 1982). e chewing insects access nutri-

ents by causing mechanical damage to the host, whereas

in piercing-sucking insects, the insect saliva forms the

interface between the host and the insect. It has been

shown that the insect saliva is composed of a diverse

array of molecules. Majority of the studies on rice-

insect interactions have been carried out with respect to

the piercing-sucking insects like BPH and GRH. ese

insects probe the host tissue using their stylets in order

to ﬁnd a proper feeding site (Fig.4). During this process,

they secrete two types of saliva, the gelling saliva and the

watery saliva. e gelling saliva is believed to aid in the

production of asalivary sheath that might be helpful in

providing mechanical strength to the stylet of the insect.

Watery saliva is secreted into the plant tissue and might

play a role in establishing proper conditions for accessing

the nutrients, as has been established by various studies

(Huang etal. 2019b). Hence, insect saliva is becoming an

attractive area of study. Studies on plant- aphid interac-

tions have demonstrated that the salivary components

of the insect have the ability to alter the host physiology

and also elicit the host response against the insect attack

(Rodriguez and Bos 2013; Elzinga and Jander 2013).

Until now, many studies have demonstrated the global

proﬁle of the secretome of insects that attack rice, includ-

ing BPH, WBPH, and GRH. Transcriptomics and prot-

eomics approaches were used to proﬁle the salivary gland

transcriptome and the insect secretome, respectively.

is section summarises these ﬁndings.

Insect Saliva: ARepertoire ofDiverse Set ofMolecules

e role of insect saliva in the plant–insect interface has

been known since the 1960s (Sogawa 1967). Studies on

plant–insect interaction have revealed the ability of the

insect saliva or oral secretions to induce and alter the

host defense response (Rodriguez and Bos 2013; Acevedo

etal. 2015). In rice, it was shown that theapplication of

salivary gland extract of BPH causes rice transcriptional

changes (Petrova and Smith 2015). Also, oral secretion

of two chewing insects, viz., Mythimna loreyi and Par-

nara guttata were shown to elicit immune responses in

rice (Shinya etal. 2016). ese studies suggest that the

salivary components of insects have the ability to alter

the host physiology. Most of the studies in rice have

been carried out with respect to the rice-planthopper

interaction. Such studies have analysed the transcrip-

tome or secretome of the insectsalivary glands or saliva,

respectively.

Transcriptomics studies of the salivary glands of BPH

and GRH have established the global proﬁle of the genes

that are expressed in the insect salivary glands. Two dif-

ferent studies have identiﬁed 352 and 76 genes that

encode secretory proteins in BPH and GRH, respectively

(Ji etal. 2013; Matsumoto etal. 2014). Results from both

these studies suggest that there are a large number of

proteins that are salivary gland-secreted, which func-

tion as enzymes. Among various predicted genes, those

coding for serine protease, disulﬁde isomerase, lipase,

and dehydrogenase were common with other piercing-

sucking insects. In addition, the same study found that 45

out of the 68 salivary gland-speciﬁc transcripts code for

unknown proteins (Matsumoto etal. 2014).

Other predicted genes encode for plant cell wall

degrading enzymes, β-glucanases, β-glucosidases, gly-

cosylases, trypsin-like proteins, lipases and α-amylase.

Besides enzymes, genes encoding chemosensory pro-

teins (CSPs) and odorant-binding proteins (OBPs) were

alsoidentiﬁed. It was previously shown in other systems

that, CSPs and OBPs have host physiology altering abil-

ity (Ji etal. 2013). In addition, Ji etal. (2013) had identi-

ﬁed a set of 67 salivary gland genes that are diﬀerentially

expressed between two biotypes of BPH that diﬀer in

virulence. Another transcriptomics study identiﬁed 19

secretory proteins that might play a role in plant defense

suppression and detoxiﬁcation and digestion of theplant

cellwall (Miao etal. 2018a).

Proteomics studies were crucial in establishing the

truly secreted components of insect saliva. Approaches

like 2D-PAGE and LC–MS/MS were used to study the

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Debetal. Rice (2021) 14:94

Table 3 Eﬀectors of M. oryzae

Eector Known function/related information References

Apoplastic eectors

SLP1 Competes with plant OsCEBiP to bind chitin oligosaccharides

and helps the fungus suppress chitin-induced immunity in host;

outlines IH, i.e. localised to EIHMx

Mentlak et al. (2012), Giraldo et al. (2013)

BAS3 focused point localisation in EIHMx & accumulates in the

regions where IH cross at the cell wall to neighbouring cells Mosquera et al. (2009)

BAS4 Outlines IH, i.e. localised to EIHMx Mosquera et al. (2009)

BAS113 Outlines IH, i.e. localised to EIHMx Giraldo et al. (2013)

MC69 Targeted gene disruption aﬀects the pathogenicity of M. oryzae Saitoh et al. (2012)

MSP1 Secreted into apoplasm; induces cell death & elicits immune

responses Wang et al. (2016c)

Cytoplasmic eectors

PWL1 Accumulate at BIC, translocate to rice cytoplasm Khang et al. (2010)

PWL2 Accumulate at BIC, translocate to rice cytoplasm, and move

from cell to cell Khang et al. (2010)

BAS1 Accumulate at BIC Khang et al. (2010), Mosquera et al. (2009)

BAS2 Translocate to rice cytoplasm, and accumulate at cell wall cross-

ing points Mosquera et al. (2009)

BAS107 Accumulates at BIC, translocates and localises to rice cell

nucleus, also moves from cell to cell Giraldo et al. (2013)

Avr-Piz-t Translocates to rice cells; interacts with Avr-Piz-t Interacting

Protein 6 (APIP6, RING E3 ubiquitin ligase), APIP10 (RING E3

ubiquitin ligase), APIP5(bZIP transcription factor), APIP12 (homo-

logue of nucleoporin protein, Nup80), OsAKT1 (Potassium

(K+) channel protein) and OsRac1(homologue of human small

GTPase) to suppress PTI

Park et al. (2012, 2016), Wang et al. (2016a),

Tang et al. (2017), Shi et al. (2018), Bai et al.

(2019)

Avr-Pii Interact with OsExo70-F3 (exocyst complex protein) and

Os-NADP-ME2 (NADP-malic enzyme2) Fujisaki et al. (2015), Singh et al. (2016)

Avr-CO39 Translocates to rice cells; puriﬁed protein directly localises to

protoplast without aid from fungal components, RAG5 interac-

tion leads to recognition by RAG4/RAG5 R pair proteins

Ribot et al. (2013), Cesari et al. (2013)

Avr-Pia RAG5 interaction leads to recognition by RAG4/RAG5 R pair

proteins Cesari et al. (2013)

MoHEG13 Suppresses the cell death caused by MoNLP proteins Mogga et al. (2016)

MoHEG16 Necessary for successful virulence of M. oryzae Mogga et al. (2016)

IUG6 BIC localisation and suppression of salicylic acid & ethylene

signalling Dong et al. (2015)

IUG9 BIC localisation and suppression of salicylic acid & ethylene

signalling Dong et al. (2015)

Avr-Pita Predicted metalloprotease domain; binds to cognate R protein

Pita directly; accumulates at BIC Jia et al. (2000)

Avr-Pik/km/kp The diﬀerent alleles are pathogen race speciﬁc; have cognate

functional R gene pair of NB-LRR with a set of Pik alleles in rice Yoshida et al. (2009), Kanzaki et al. (2012)

Avr-Pi9 Localises to BIC and translocate to rice cells Wu et al. (2015)

Avr-Pib Zhang et al. (2015)

Avr-Pi54 Interacts directly with the R protein Pi54 Devanna et al. (2014)

Avr-Pi12 Li et al. (2018b)

Secondary metabolites as eector

Hydroxylated Jasmonic acid (12OH-JA) antibiotic biosynthesis monooxygenase (Abm) converts free

jasmonic acid (JA) to Hydroxylated JA (12OH-JA) Patkar et al. (2015)

Unknown secondary metabolite Synthesis involves avirulence conferring enzyme 1, ACE1 an

appressoria localised eﬀector protein; the corresponding R gene

is identiﬁed to be Pi33

Bohnert et al. (2004), Collemare et al. (2008)

Tenuazonic acid (TeA) TAS1 is involved in the synthesis of TeA Yun et al. (2015)

Cytokinin Known protein involved is cytokinin synthesis 1, CSK1 Chanclud et al. (2016)

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Debetal. Rice (2021) 14:94

insect saliva. All these studies used the saliva secretions

of insects that were fed on artiﬁcial diet. In common, all

the studies identiﬁed a wide variety of enzymes and pro-

teins with diverse functions to be present in the saliva

of BPH, WBPH, and GRH (Konishi etal. 2009; Liu etal.

2016; Huang etal. 2016; Hattori etal. 2015; Miao etal.

2018b).Proteins involved in Ca2+-binding, ATP-binding,

cytoskeletal, DNA- or RNA-binding, chromatin binding,

transporters, apolipoproteins, ubiquitin, and heat shock

proteins were also identiﬁed in the saliva (Liu etal. 2016).

Details of the studies are shown in Table4. ese stud-

ies have established the components of insect saliva and

laid the foundation for further studies on the molecular

aspects of plant–insect interaction.

Insect Eectors: The Players attheInterface

Knockdown ofinsect genes using dsRNA has proved to

be a valuable approach for functional characterisation of

genes (Gu and Knipple 2013). Certain salivary proteins

were found to be essential for the ﬁtness of the insect.

Knockdown of BPH NlMul (Nilaparvata lugens Mucin-

like protein)has resulted in short and single-branched

stylets. NlMul gene codes for a mucin-like protein that

is present in abundance in the insect saliva. Mucins are

highly glycosylated proteins and are important for the

cell-environment communication (Huang et al. 2017).

Knockdown of another salivary protein-encoding gene in

BPH, NlShp (Nl Sheath protein)was shown to inhibit the

formation of salivary ﬂanges and salivary sheath. NlShp

was annotated as an unknown protein (Huang et al.

2015). Another study revealed that three protein cod-

ing genes, including an annexin-like protein (ANX-like

5), a salivary sheath protein (salivap-3) and a carbonic

anhydrase (CA), are essential for the survival of BPH in

rice. Further ANX-like 5 and salivap-3 were shown to be

indispensable for the feeding behaviour of BPH wherein

the knockdown of these genes showed negative eﬀects

on phloem sap-feeding time and honeydew excretion

by BPH (Huang etal. 2016). ese studies support the

notion that proper salivary sheath formation is essen-

tial for BPH virulence in rice. In GRH, knockdown of

NcSP75, (Nephotettix cincticepsSalivary Protein 75kDa)

encoding a salivary protein of unknown function, was

shown to cause poor performance of the insect on rice,

while no such eﬀects were seen in insects raised on arti-

ﬁcial diet (Matsumoto and Hattori 2018). As the knock-

down of these genes led to lesser virulence of the insect,

it is possible that these gene products aid in the interac-

tion between the host and the pest.

In order to reach the vascular bundle, the insect uses

its stylet to probe and pierce through the plant tissue.

During this process, the insect has to break the cellwall

components of the plant cell. e expression of genes

coding for plant cellwall degrading proteins in the BPH

salivary gland was described previously (Ji et al. 2013).

NlEG1, a predicted endo-β-1,4-glucanase, was shown to

have in-vitro endoglucanase activity and the knockdown

of NlEG1 reduced the insect’s ability to reach the phloem

and also had negative impacts on food intake, mass, sur-

vival, and fecundity of the insect on rice plants. Addition-

ally, only a small eﬀect on survival was seen in the insects

that were raised on artiﬁcial diet. Hence, it is speculated

that NlEG1 might act as an eﬀector which alters the host

structures and enables the stylet to reach the phloem (Ji

etal. 2017).

Further, catalase gene named Kat-1 was shown to be

secreted into the rice tissue and possess catalase activ-

ity (Petrova and Smith 2014). It is speculated that Kat-1

might be helpful in scavenging the hydrogen perox-

ide (H2O2) molecules released by the plant post insect

attack. A mucin-like protein, NlMLP was alsoshown to

be important for insect performance and salivary sheath

formation. In addition, NlMLP was found to induce cell

death when transiently expressed in either rice proto-

plasts or Nicotiana benthamiana leaves. e induction of

cell death was found to be calcium-dependent and act-

ingthrough theMEK2-dependent MAPK pathway. Also,

NlMLP was shown to induce callose deposition and trig-

ger jasmonic acid-related defense gene expression in N.

benthamiana (Shangguan etal. 2018).

Calcium signalling is known to be an immedi-

ate response by plants after insect attack. It results in

the occlusion of sieve elements, thereby preventing

the insects from ingesting the sap (Rodriguez and Bos

2013). But the insects are mostly successful in overcom-

ing this block. Studies had shown that insect saliva pos-

sesses Ca2+-binding proteins. NlSEF1 is an EF-hand

Ca2+-binding protein present in the saliva of BPH and

is secreted into the rice tissue. Also, it was shown that

NlSEF1 reduces the cytosolic Ca2+ levels in rice and sup-

presses wound-induced H2O2 production. Moreover, the

knockdown of NlSEF1 decreased the survival and feed-

ing of the insects (Ye etal. 2017). A similar protein was

also characterised in GRH. NcSP84 was found to be a

(See ﬁgure on next page.)

Fig. 4 Schematic representation of BPH-Rice interaction. Using its stylet, the insect pierces the rice tissue and reaches the phloem to suck the

sap. During this process, both gelling and watery saliva are secreted by the insect, which contain various molecules that elicit or act against plant

defense. Proteins like catalase, endoglucanase, and Ca2+-binding proteins might be involved in suppressing the plant defense while proteins like

Mucin-like proteins, Apolipophorins, and Protein disulﬁde isomerase elicit immune responses. Some of these proteins were found to induce callose

deposition, cell death and SA or JA- associated defense gene expression

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Page 13 of 21

Debetal. Rice (2021) 14:94

Fig. 4 (See legend on previous page.)

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Page 14 of 21

Debetal. Rice (2021) 14:94

salivary protein that exhibits in-vitro Ca2+-binding activ-

ity and is secreted into the rice tissue (Hattori etal. 2012).

e putative eﬀectors thus far identiﬁed have been tabu-

lated in Table5. ese studies support the possible role

of insect-associated molecules in suppressing the plant

defense response.

In order to identify the eﬀector properties of a candi-

date protein, transient transformation of N. benthamiana

followed by cell death assays is widely used. Using such

a strategy, six putative eﬀectors were identiﬁed in BPH

after screening 64 candidates. e six putative eﬀectors

include protein disulﬁde isomerase (PDI; N112), apoli-

pophorin (N116), small secreted cysteine-rice protein

Table 4 Studies that established the secretome of various rice pests

BPH Brown planthopper, GRH Green riceleafhopper, WBPH Whitebacked planthopper, LC MS/MS Liquid Chromatography–Tandem Mass Spectrometry, SG salivary gland,

2D-PAGE two-dimensional polyacrylamide gel electrophoresis

Insect Source material Approach Number of proteins/genes identied References

BPH SG 2D-PAGE and Edman

Degradation 52 proteins Konishi et al. (2009)

BPH Secreted Saliva LC–MS/MS 202—Watery Saliva Proteins

18—Gelling Saliva Proteins Huang et al. (2016)

BPH Secreted Saliva LC–MS/MS 107—Watery Saliva Proteins Liu et al. (2016)

BPH SG Transcriptome 1140 genes coding secretory proteins Rao et al. (2019)

BPH SG Transcriptome 352 genes coding secretory proteins Ji et al. (2013)

BPH SG Transcriptome 19—SG Speciﬁc secreted protein encoding genes Miao et al. (2018a)

GRH Secreted Saliva LC–MS/MS 71—Proteins Hattori et al. (2015)

GRH SG Transcriptome 76 genes coding secretory proteins Matsumoto et al. (2014)

WBPH Secreted Saliva LC–MS/MS 161—Watery saliva proteins Miao et al. (2018b)

Table 5 Insect associated molecules that are characterised

BPH Brown Planthopper, GRH Green Rice Leafhopper, SBPH Small Brown Planthopper, RGM Rice Gall Midge

Insect Protein Description Activity and localisation in rice References

BPH NlMLP Mucin-like protein Cell death and callose deposition

Cytoplasm Shangguan et al. (2018)

BPH NlSEF1 EF-hand Ca2+-binding protein Suppression of wound-induced H2O2 and reduction in

cytosolic Ca2+ level Ye et al. (2017)

BPH NlEG1 endo-β-1,4-glucanase Possesses in vitro endoglucanase activity Ji et al. (2017)

BPH NlMul Mucin-like protein – Huang et al. (2017)

BPH Kat-1 Catalase In vitro catalase activity Petrova and Smith, (2014)

BPH salivap-3 Salivary Protein – Huang et al. (2016)

BPH CA Carbonic Anhydrase – Huang et al. (2016)

BPH ANX-like 5 Annexin-like protein 5 – Huang et al. (2016)

BPH N112 Protein disulﬁde isomerase Cell death/Nucleo-cytoplasmic Rao et al. (2019)

BPH N116 Apolipophorin-III Cell death/Nucleo-cytoplasmic Rao et al. (2019)

BPH N128 Small secreted cysteine-rich protein Cell death/Nucleo-cytoplasmic Rao et al. (2019)

BPH N132 Chemosensory protein Nucleo-cytoplasmic Rao et al. (2019)

BPH N140 Unknown Protein – Rao et al. (2019)

BPH N143 Unknown protein Cell death/Nucleus Rao et al. (2019)

GRH NcSP75 Unknown Protein – Matsumoto and Hattori, (2018)

GRH NcSP84 EF-hand Ca2+-binding protein In vitro Ca2+ binding activity Hattori et al. (2012)

GRH β-glucosidase β-glucosidase In vitro hydrolysis of p-nitrophenyl-b-

-glucopyranoside Nakamura and Hattori, (2013)

GRH NcLac1S Laccase In vitro laccase activity Hattori et al. (2010)

SBPH DNaseII Deoxyribonuclease II In vitro DNAse activity; suppression of insect-induced

callose and H2O2 accumulation Huang et al. (2019a)

RGM OoNDPK Nucleoside diphosphate kinase Secreted into the host cells; causes elongation of rice

coleoptile cells Sinha et al. (2012)

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Debetal. Rice (2021) 14:94

(SSCP; N128), chemosensory protein (CSP; N132), and

two proteins with no predicted functions (N140 and

N143). ese proteins were found to induce cell death,

chlorosis, or dwarf phenotype in N. benthamiana. In

addition, the proteins also induced defense responses

including callose deposition and defense gene expression

(Rao etal. 2019). Cellular damage could occur during the

penetration of insect stylet which in turn would result

in the release of cellular components. e presence of

deoxyribonucleic acid (DNA) in the extracellular region

is alsoknown to trigger plant defense responses by act-

ing as a damage-associated molecular pattern (DAMP)

(Quintana-Rodriguez etal. 2018). Previous studies have

reported the presence of deoxyribonuclease II (DNase

II) in the saliva of planthoppers (Liu et al. 2016; Miao

etal. 2018b). e DNase II in small brown planthopper

saliva suppresses induction of plant defense responses

including H2O2 accumulation and callose deposition. In

addition, it was shown that the exogenous application of

DNase II slightly reduced those responses (Huang etal.

2019a).

Another pest, the rice gall midge (RGM), causes gall

formation in susceptible rice varieties and is a major

threat for crop production. RGM induces gall formation

in rice apical meristem by altering the rice metabolic

pathways in order to facilitate its own survival (Sinha

etal. 2011). Although a serious pest of rice, the studies

on the pest eﬀectors that are involved in establishing

gall formation are somewhat limited. In one study, gene

expression analysis of RGM maggots identiﬁed a nucleo-

tide diphosphate kinase (NDPK), that is highly expressed

in compatible interaction than in incompatible inter-

action (Sinha et al. 2012). NDPK was identiﬁed to be

secreted into rice during RGM feeding and theapplica-

tion of recombinant NDPK resulted in theelongation of

rice coleoptile cells. is study suggested a possible role

of NDPK in facilitating the alteration of host machinery

to establish gall formation by RGM.

Many rice resistance genes have been identiﬁed against

the major rice pests including the planthoppers and the

gall midge. Like many disease resistance genes, the insect

resistance genes also encode Nucleotide binding-site-

Leucine rich repeat-containing proteins (NBS-LRRs),

among others (Bentur etal. 2016; Fujita etal. 2013). is

suggests that a direct recognition of the pest-associated

molecules may be occuring in the cytoplasm of plant

cells.

Conclusions: Diverse Attackers—Common

Pathways

e pathogens and pests discussed in this review rep-

resent a diverse group of organisms but with rice as

a common host. e ﬁrst striking diﬀerence between

the diﬀerent pathogens and pests is the mode of eﬀec-

tor secretion. In bacteria, dedicated type II and type III

secretion systems are involved in the secretion of eﬀector

proteins, whereas fungal pathogens employ the BFA- sen-

sitive or BFA- insensitive vesicular pathways for eﬀector

secretion (Jha etal. 2007; Giraldo etal. 2013). Insects,

on the other hand, secrete saliva, which contains the

complete repertoire of eﬀectors (Shangguan etal. 2018).

Pathogenesis begins by the invasion of the plant cell. is

is accomplished by the apoplastic eﬀectors, which breach

the plant cell wall and facilitate entry into the host cel-

lular system. Most of these apoplastic eﬀectors have

deﬁned enzymatic activity, the majority of which are

directed towards disruption of cell wall barriers leading

to nutrient availability (Ji etal. 2013, 2017; Jha etal. 2005;

Tayi et al. 2016b; Rajeshwari et al. 2005; Aparna etal.

2009; Zou etal. 2012).

However, for suppression of plant immune responses,

these diﬀerent pathogens and pests seem to target com-

mon nodes in plant defense. Some of the common

pathways targeted by the pathogens and pests include

well-characterised immune response components, such

as the MAPK pathway, ubiquitination pathway, cal-

cium signalling, and hormone signalling. For example,

both bacterial peptidoglycan and fungal chitin are rec-

ognised by the OsCERK1 receptor complex, which fur-

ther phosphorylates the cytoplasmic receptor kinase

OsRLCK185 and activates MAPK cascades (Akamatsu

etal. 2013; Wang etal. 2017; Yamaguchi etal. 2013b; Ao

etal. 2014). is seems to be a critical step inthe induc-

tion of defense responses against multiple pathogens,

and hence is also a target for suppression of immune

responses by the pathogens, eg., by XopYXoo, XopPXoo,

MoSLP1, and Avr-Piz-t (Yamaguchi etal. 2013b; Mentlak

etal. 2012; Giraldo etal. 2013; Bai etal. 2019; Ishikawa

etal. 2014). e MAPK signalling pathway ampliﬁes the

plant immune responses, thus making it another nodal

point for suppression. Numerous eﬀector proteins tar-

get the MAPK signalling events, hence modulating the

plant immune responses (Long et al. 2018; Mentlak

etal. 2012; Giraldo et al. 2013). In parallel, some of the

pathways which are activated early on during pathogen

infection and pest infestation include calcium signalling

and the oxidative burst (Akamatsu et al. 2013), which

pathogens and pests have evolved to suppress in order to

cause infection (Giraldo etal. 2013; Mentlak etal. 2012;

Bai etal. 2019; Singh etal. 2016). For instance, an eﬀec-

tor from BPH, NlSEF1, suppresses cytosolic Ca2+ levels

and wound- induced H2O2 (Ye etal. 2017), whereas the

Magnaporthe eﬀectors Avr-Piz-t and Avr-Pii were shown

to suppress ROS levels (Bai etal. 2019; Singh etal. 2016).

Another important molecular cascade that is targeted by

pathogens to evade immune activation is regulation via

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Page 16 of 21

Debetal. Rice (2021) 14:94

ubiquitination, speciﬁcally, by targeting the E3 Ubiquitin

ligases, which regulate the ﬁnal step of ubiquitin conjuga-

tion (Ishikawa etal. 2014; Park etal. 2016, 2012).

e hormone signalling pathways are important targets

for host defense manipulation. Eﬀectors from pathogens

and pests modulate components of hormone pathways

to suppress the plant defenses. Eﬀectors from Xoo have

been shown to suppress immune responses by target-

ing brassinosteroid signalling (Yamaguchi et al. 2013a;

Wang etal. 2008), whereas Magnaporthe eﬀectors mod-

ulate cytokinin and active jasmonic acid levels inplanta

(Chanclud etal. 2016; Patkar etal. 2015).

Yet another common feature among eﬀector proteins is

functional compartmentalisation. Some of the bacterial

non-TAL eﬀectors as well as the TAL eﬀectors are known

to translocate to the nucleus in plant cells. Although the

precise functions have not been elucidated for fungal

and pest eﬀectors, nuclear localisation is observed, sug-

gesting that nuclear localisation is possibly important for

the function of several eﬀectors (Gurlebeck et al. 2006;

Mosquera etal. 2009; Giraldo etal. 2013; Deb etal. 2019,

2020; Rao etal. 2019). In bacterial pathogens, some TAL

eﬀectors speciﬁcally target and regulate gene expression

of susceptibility factors like SWEET genes (Yang etal.

2006; Antony etal. 2010; Yuan etal. 2009). is seems

to be crucial in Xoo since geographically distant strains

of Xoo were shown to upregulate the same or diﬀerent

SWEET genes through diﬀerent TAL eﬀectors (Streubel

etal. 2013).

e primary requirement of the pathogen and pest is

immune evasion in order to establish itself in the host.

For this, they target multiple pathways in rice. e con-

vergence of eﬀector functions could be attributed in part

to the common host pathways which are involved in

defense against multiple pathogens and pests. e char-

acterisation of such key components of the plant immune

system would lead to a more comprehensive understand-

ing of plant resistance responses to pathogens and pests.

Future Perspectives

Although numerous studies have been focused on

understanding the mechanism of host- pathogen/pest

interactions in rice, there is a lot that remains to be

explored. Gaps in our knowledge exist regarding the

molecular mechanisms of eﬀector action in rice. It is

established that diﬀerent pathotypes of a pathovar or

biotypes of an insect possess an eﬀectome repertoire

speciﬁc for causing disease in a plant genotype in a

particular geographical location. How this diversity in

eﬀectome and the crosstalk between the eﬀectors helps

in disease development remains to be determined.

Studies on hub proteins in immune signalling path-

ways are also crucial to understand immune response

functioning. Ultimately, this knowledge should be

leveraged to develop crop varieties that are resistant

tomultiple pathogens and pests, thus helping to meet

the increasing demand of global rice production.

Abbreviations

12OH-JA: Hydroxylated JA; 2D-PAGE: Two-dimensional polyacrylamide gel

electrophoresis; BAS: Biotrophy associated secreted; BB: Bacterial Blight; BBI:

Bowman-Birk-type trypsin Inhibitor; BFA: Brefeldin A; BIC: Biotrophic invasion

complex; BLS: Bacterial Leaf Streak; BPH: Brown planthopper; CWDE: Cell

Wall Degrading Enzymes; DAMP: Damage-Associated Molecular Pattern;

DNA: Deoxyribonucleic acid; EIHM: Extrainvasive hyphal membrane; EIHMx:

Extrainvasive hyphal matrix; ETI: Eﬀector triggered immunity; GRH: Green

rice leafhopper; IH: Invasive hyphae; JA: Jasmonic acid; LC MS/MS: Liquid

Chromatography–Tandem Mass Spectrometry; M. oryzae: Magnapor the oryzae;

NADPH: Nicotinamide adenine dinucleotide phosphate; NBS-LRR: Nucleotide-

Binding Site-Leucine Rich Repeats; PAMP: Pathogen-Associated Molecular

Pattern; PGN: Peptidoglycan; pv.: Pathovar; PWL: Pathogenicity toward

Weeping Lovegrass; RGA : R-gene analog; R-gene: Resistance gene; RGM:

Rice Gall Midge; RNA: Ribonucleic acid; ROS: Reactive oxygen species; SBPH:

Small Brown planthopper; SG: Salivary Gland; T2SS: Type 2 Secretion System;

T3SS: Type 3 Secretion System; TALE: Transcription-activator like eﬀector; TeA`:

Tenuazonic acid; WBPH: White-backed planthopper; Xoc: Xanthomonas or yzae

pv. oryzicola; Xoo: Xanthomonas oryzae p v. oryzae; Xop: Xanthomonas outer

protein.

Acknowledgements

We apologize to those authors whose work was omitted or not emphasized

due to space limitations.

Authors’ contributions

SD, VNM and GCG wrote the manuscript. HKP and RVS ﬁnalized the manu-

script, which was approved by all the authors. All authors read and approved

the ﬁnal manuscript.

Funding

This work was supported by grants to RVS from the Plant–Microbe and Soil

Interaction (PMSI) project of the Council of Scientiﬁc and Industrial Research

(CSIR), Government of India (Project Code: BSC0117) and the J. C. Bose

fellowship to RVS from the Department of Science and Technology (DST),

Government of India (Project Code: GAP0444). This work was also supported

by grants to HKP from the Council of Scientiﬁc and Industrial Research (CSIR),

Government of India (Project Code: MLP0121). SD acknowledges the Council

of Scientiﬁc and Industrial Research (CSIR), Government of India for fellowship.

CGG acknowledges the Council of Scientiﬁc and Industrial Research (CSIR),

Government of India for Ph.D. fellowship. VNM acknowledges Ph.D. scholar-

ship funding from UGC, Govt. of India.

Availability of data and materials

Data sharing is not applicable to this article as no datasets were generated

during this study.

Declarations

Ethics approval and consent to participate

Not applicable.

Consent for publication

Not applicable.

Competing interests

The authors declare that they have no competing interests.

Author details

1 CSIR-Centre for Cellular and Molecular Biology (CSIR-CCMB),

Hyderabad 500007, India. 2 Present Address: Department of Plant and Environ-

mental Sciences, University of Copenhagen, 1871 Frederiksberg C, Denmark.

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Page 17 of 21

Debetal. Rice (2021) 14:94

3 Present Address: Indian Institute of Science Education and Research (IISER)

Tirupati, Tirupati 517507, India.

Received: 13 July 2021 Accepted: 6 November 2021

References

Acevedo FE, Rivera-Vega LJ, Chung SH, Ray S, Felton GW (2015) Cues from

chewing insects—the intersection of DAMPs, HAMPs, MAMPs and

eﬀectors. Curr Opin Plant Biol 26:80–86

Ahn IP, Kim S, Lee YH (2005) Vitamin B1 functions as an activator of plant

disease resistance. Plant Physiol 138:1505–1515

Ahn IP, Kim S, Lee YH, Suh SC (2007) Vitamin B1-induced priming is dependent

on hydrogen peroxide and the NPR1 gene in Arabidopsis. Plant Physiol

143:838–848

Akamatsu A, Wong HL, Fujiwara M, Okuda J, Nishide K, Uno K, Imai K,

Umemura K, Kawasaki T, Kawano Y, Shimamoto K (2013) An OsCEBiP/

OsCERK1-OsRacGEF1-OsRac1 module is an essential early component

of chitin-induced rice immunity. Cell Host Microbe 13:465–476

Akimoto-Tomiyama C, Furutani A, Tsuge S, Washington EJ, Nishizawa Y, Minami

E, Ochiai H (2012) XopR, a type III eﬀector secreted by Xanthomonas

oryzae pv. oryzae, suppresses microbe-associated molecular pattern-

triggered immunity in Arabidopsis thaliana. Mol Plant Microbe Interact

25:505–514

Antony G, Zhou J, Huang S, Li T, Liu B, White F, Yang B (2010) Rice xa13

recessive resistance to bacterial blight is defeated by induction of the

disease susceptibility gene Os-11N3. Plant Cell 22:3864–3876

Ao Y, Li Z, Feng D, Xiong F, Liu J, Li JF, Wang M, Wang J, Liu B, Wang HB (2014)

OsCERK1 and OsRLCK176 play important roles in peptidoglycan and

chitin signaling in rice innate immunity. Plant J 80:1072–1084

Aparna G, Chatterjee A, Sonti RV, Sankaranarayanan R (2009) A cell wall-

degrading esterase of Xanthomonas oryzae requires a unique substrate

recognition module for pathogenesis on rice. Plant Cell 21:1860–1873

Bai J, Choi SH, Ponciano G, Leung H, Leach JE (2000) Xanthomonas oryzae

pv. oryzae avirulence genes contribute diﬀerently and speciﬁcally to

pathogen aggressiveness. Mol Plant Microbe Interact 13:1322–1329

Bai P, Park CH, Shirsekar G, Songkumarn P, Bellizzi M, Wang GL (2019) Role of

lysine residues of the Magnaporthe oryzae eﬀector AvrPiz-t in eﬀector-

and PAMP-triggered immunity. Mol Plant Pathol 20:599–608

Bentur JS, Rawat N, Divya D, Sinha DK, Agarrwal R, Atray I, Nair S (2016) Rice-

gall midge interactions: battle for survival. J Insect Physiol 84:40–49

Blair MW, Garris AJ, Iyer AS, Chapman B, Kresovich S, McCouch SR (2003) High

resolution genetic mapping and candidate gene identiﬁcation at the

xa5 locus for bacterial blight resistance in rice (Oryza sativa L.). Theor

Appl Genet 107:62–73

Boch J, Bonas U (2010) Xanthomonas AvrBs3 family-type III eﬀectors: discovery

and function. Annu Rev Phytopathol 48:419–436

Bogdanove AJ, Koebnik R, Lu H, Furutani A, Angiuoli SV, Patil PB, van Sluys

MA, Ryan RP, Meyer DF, Han SW, Aparna G, Rajaram M, Delcher AL,

Phillippy AM, Puiu D, Schatz MC, Shumway M, Sommer DD, Trapnell C,

Benahmed F, Dimitrov G, Madupu R, Radune D, Sullivan S, Jha G, Ishi-

hara H, Lee SW, Pandey A, Sharma V, Sriariyanun M, Szurek B, Vera-Cruz

CM, Dorman KS, Ronald PC, Verdier V, Dow JM, Sonti RV, Tsuge S, Bren-

del VP, Rabinowicz PD, Leach JE, White FF, Salzberg SL (2011) Two new

complete genome sequences oﬀer insight into host and tissue speciﬁc-

ity of plant pathogenic Xanthomonas spp. J Bacteriol 193:5450–5464

Bohnert HU, Fudal I, Dioh W, Tharreau D, Notteghem JL, Lebrun MH (2004) A

putative polyketide synthase/peptide synthetase from Magnaporthe

grisea signals pathogen attack to resistant rice. Plant Cell 16:2499–2513

Bonas U, Stall RE, Staskawicz B (1989) Genetic and structural characterization

of the avirulence gene avrBs3 from Xanthomonas campestris pv. vesica-

toria. Mol Gen Genet MGG 218:127–136

Burdman S, Shen Y, Lee SW, Xue Q, Ronald P (2004) RaxH/RaxR: a two-compo-

nent regulatory system in Xanthomonas oryzae pv. oryzae required for

AvrXa21 activity. Mol Plant Microbe Interact 17:602–612

Buttner D, Bonas U (2010) Regulation and secretion of Xanthomonas virulence

factors. FEMS Microbiol Rev 34:107–133

Carella P, Evangelisti E, Schornack S (2018) Sticking to it: phytopathogen eﬀec-

tor molecules may converge on evolutionarily conserved host targets

in green plants. Curr Opin Plant Biol 44:175–180

Cesari S, Thilliez G, Ribot C, Chalvon V, Michel C, Jauneau A, Rivas S, Alaux L,

Kanzaki H, Okuyama Y, Morel JB, Fournier E, Tharreau D, Terauchi R, Kroj

T (2013) The rice resistance protein pair RGA4/RGA5 recognizes the

Magnaporthe oryzae eﬀectors AVR-Pia and AVR1-CO39 by direct bind-

ing. Plant Cell 25:1463–1481

Chanclud E, Kisiala A, Emery NR, Chalvon V, Ducasse A, Romiti-Michel C, Gravot

A, Kroj T, Morel JB (2016) Cytokinin Production by the Rice Blast Fungus

Is a Pivotal Requirement for Full Virulence. PLoS Pathog 12:e1005457

Chang JH, Desveaux D, Creason AL (2014) The ABCs and 123s of bacte-

rial secretion systems in plant pathogenesis. Annu Rev Phytopathol

52:317–345

Chen L-Q, Hou B-H, Lalonde S, Takanaga H, Hartung ML, Qu X-Q, Guo W-J,

Kim J-G, Underwood W, Chaudhuri B, Chermak D, Antony G, White FF,

Somerville SC, Mudgett MB, Frommer WB (2010) Sugar transporters for

intercellular exchange and nutrition of pathogens. Nature 468:527–532

Chen X, Liu P, Mei L, He X, Chen L, Liu H, Shen S, Ji Z, Zheng X, Zhang Y, Gao Z,

Zeng D, Qian Q, Ma B (2021) Xa7, a new executor R gene that confers

durable and broad-spectrum resistance to bacterial blight disease in

rice. Plant Commun 2:100143

Cheong H, Kim CY, Jeon JS, Lee BM, Sun Moon J, Hwang I (2013) Xanthomonas

oryzae pv. oryzae type III eﬀector XopN targets OsVOZ2 and a putative

thiamine synthase as a virulence factor in rice. PLoS ONE 8:e73346

Chinchilla D, Zipfel C, Robatzek S, Kemmerling B, Nurnberger T, Jones JD, Felix

G, Boller T (2007) A ﬂagellin-induced complex of the receptor FLS2 and

BAK1 initiates plant defence. Nature 448:497–500

Chu Z, Fu B, Yang H, Xu C, Li Z, Sanchez A, Park YJ, Bennetzen JL, Zhang Q,

Wang S (2006a) Targeting xa13, a recessive gene for bacterial blight

resistance in rice. Theor Appl Genet 112:455–461

Chu Z, Yuan M, Yao J, Ge X, Yuan B, Xu C, Li X, Fu B, Li Z, Bennetzen JL, Zhang

Q, Wang S (2006b) Promoter mutations of an essential gene for

pollen development result in disease resistance in rice. Genes Dev

20:1250–1255

Collemare J, Pianfetti M, Houlle AE, Morin D, Camborde L, Gagey MJ, Barbisan

C, Fudal I, Lebrun MH, Bohnert HU (2008) Magnaporthe grisea aviru-

lence gene ACE1 belongs to an infection-speciﬁc gene cluster involved

in secondary metabolism. New Phytol 179:196–208

da Silva FG, Shen Y, Dardick C, Burdman S, Yadav RC, de Leon AL, Ronald PC

(2004) Bacterial genes involved in type I secretion and sulfation are

required to elicit the rice Xa21-mediated innate immune response. Mol

Plant Microbe Interact 17:593–601

de Guillen K, Ortiz-Vallejo D, Gracy J, Fournier E, Kroj T, Padilla A (2015) Struc-

ture analysis uncovers a highly diverse but structurally conserved eﬀec-

tor family in phytopathogenic fungi. PLoS Pathog 11:e1005228

Dean R, van Kan JA, Pretorius ZA, Hammond-Kosack KE, di Pietro A, Spanu

PD, Rudd JJ, Dickman M, Kahmann R, Ellis J, Foster GD (2012) The top

10 fungal pathogens in molecular plant pathology. Mol Plant Pathol

13:414–430

Deb S, Gupta MK, Patel HK, Sonti RV (2019) Xanthomonas oryzae pv. oryzae

XopQ protein suppresses rice immune responses through interaction

with two 14-3-3 proteins but its phospho-null mutant induces rice

immune responses and interacts with another 14-3-3 protein. Mol Plant

Pathol 20:976–989

Deb S, Ghosh P, Patel HK, Sonti RV (2020) Interaction of the Xanthomonas

eﬀectors XopQ and XopX results in induction of rice immune

responses. Plant J 104:332–350

Devanna NB, Vijayan J, Sharma TR (2014) The blast resistance gene Pi54of

cloned from Oryza oﬃcinalis interacts with Avr-Pi54 through its novel

non-LRR domains. PLoS ONE 9:e104840

Dong Y, Li Y, Zhao M, Jing M, Liu X, Liu M, Guo X, Zhang X, Chen Y, Liu Y, Liu

Y, Ye W, Zhang H, Wang Y, Zheng X, Wang P, Zhang Z (2015) Global

genome and transcriptome analyses of Magnaporthe oryzae epidemic

isolate 98-06 uncover novel eﬀectors and pathogenicity-related genes,

revealing gene gain and lose dynamics in genome evolution. PLoS

Pathog 11:e1004801–e1004801

Dou D, Zhou JM (2012) Phytopathogen eﬀectors subverting host immunity:

diﬀerent foes, similar battleground. Cell Host Microbe 12:484–495

Dye DW, Bradbury J, Goto M, Hayward AC, Lelliott RA, Schroth MN (1980)

International standards for naming pathovars of phytopathogenic

Content courtesy of Springer Nature, terms of use apply. Rights reserved.

Page 18 of 21

Debetal. Rice (2021) 14:94

bacteria and a list of pathovar names and pathotype strains. Rev Plant

Pathol 59(4):153–168

Elazegui F, Islam Z (2003) Diagnosis of common diseases of rice

Elzinga DA, Jander G (2013) The role of protein eﬀectors in plant-aphid interac-

tions. Curr Opin Plant Biol 16:451–456

Eseola AB, Ryder LS, Osés-Ruiz M, Findlay K, Yan X, Cruz-Mireles N, Molinari

C, Garduño-Rosales M, Talbot NJ (2021) Investigating the cell and

developmental biology of plant infection by the rice blast fungus

Magnaporthe oryzae. Fungal Genet Biol 154:103562

Franceschetti M, Maqbool A, Jimenez-Dalmaroni MJ, Pennington HG, Kamoun

S, Banﬁeld MJ (2017) Eﬀectors of ﬁlamentous plant pathogens: com-

monalities amid diversity. Microbiol Mol Biol Rev 81:e00066-16

Fujisaki K, Abe Y, Ito A, Saitoh H, Yoshida K, Kanzaki H, Kanzaki E, Utsushi H,

Yamashita T, Kamoun S, Terauchi R (2015) Rice Exo70 interacts with a

fungal eﬀector, AVR-Pii, and is required for AVR-Pii-triggered immunity.

Plant J 83:875–887

Fujita D, Kohli A, Horgan FG (2013) Rice resistance to planthoppers and leaf-

hoppers. Crit Rev Plant Sci 32:162–191

Furutani A, Tsuge S, Ohnishi K, Hikichi Y, Oku T, Tsuno K, Inoue Y, Ochiai H,

Kaku H, Kubo Y (2004) Evidence for HrpXo-dependent expression of

type II secretory proteins in Xanthomonas oryzae pv. oryzae. J Bacteriol

186:1374–1380

Furutani A, Takaoka M, Sanada H, Noguchi Y, Oku T, Tsuno K, Ochiai H, Tsuge S

(2009) Identiﬁcation of novel type III secretion eﬀectors in Xanthomonas

oryzae pv. oryzae. Mol Plant Microbe Interact 22:96–106

Giraldo MC, Dagdas YF, Gupta YK, Mentlak TA, Yi M, Martinez-Rocha AL, Saitoh

H, Terauchi R, Talbot NJ, Valent B (2013) Two distinct secretion systems

facilitate tissue invasion by the rice blast fungus Magnaporthe oryzae.

Nat Commun 4:1996

Gu L, Knipple DC (2013) Recent advances in RNA interference research in

insects: implications for future insect pest management strategies. Crop

Prot 45:36–40

Gu K, Yang B, Tian D, Wu L, Wang D, Sreekala C, Yang F, Chu Z, Wang GL, White

FF, Yin Z (2005) R gene expression induced by a type-III eﬀector triggers

disease resistance in rice. Nature 435:1122–1125

Gupta MK, Nathawat R, Sinha D, Haque AS, Sankaranarayanan R, Sonti RV

(2015) Mutations in the predicted active site of Xanthomonas oryzae

pv. oryzae XopQ diﬀerentially aﬀect virulence, suppression of host

innate immunity, and induction of the HR in a nonhost plant. Mol Plant

Microbe Interact 28:195–206

Gurlebeck D, Thieme F, Bonas U (2006) Type III eﬀector proteins from the plant

pathogen Xanthomonas and their role in the interaction with the host

plant. J Plant Physiol 163:233–255

Hattori M, Tsuchihara K, Noda H, Konishi H, Tamura Y, Shinoda T, Nakamura

M, Hasegawa T (2010) Molecular characterization and expression

of laccase genes in the salivary glands of the green rice leafhopper,

Nephotettix cincticeps (Hemiptera: Cicadellidae). Insect Biochem Mol

Biol 40:331–338

Hattori M, Nakamura M, Komatsu S, Tsuchihara K, Tamura Y, Hasegawa T (2012)

Molecular cloning of a novel calcium-binding protein in the secreted

saliva of the green rice leafhopper Nephotettix cincticeps. Insect Bio-

chem Mol Biol 42:1–9

Hattori M, Komatsu S, Noda H, Matsumoto Y (2015) Proteome analysis of

watery saliva secreted by green rice leafhopper, Nephotettix cincticeps.

PLoS ONE 10:e0123671

Hopkins CM, White F, Choi S, Guo A, Leach J (1992) Identiﬁcation of a family

of avirulence genes from Xanthomonas oryzae pv. oryzae. Mol Plant-

Microbe Interact 5:451–459

Hu J, Qian W, He C (2007) The Xanthomonas oryzae pv. oryzae eglXoB endo-

glucanase gene is required for virulence to rice. FEMS Microbiol Lett

269:273–279

Huang HJ, Liu CW, Cai YF, Zhang MZ, Bao YY, Zhang CX (2015) A salivary sheath

protein essential for the interaction of the brown planthopper with rice

plants. Insect Biochem Mol Biol 66:77–87

Huang HJ, Liu CW, Huang XH, Zhou X, Zhuo JC, Zhang CX, Bao YY (2016)

Screening and functional analyses of Nilaparvata lugens salivary pro-

teome. J Proteome Res 15:1883–1896

Huang HJ, Liu CW, Xu HJ, Bao YY, Zhang CX (2017) Mucin-like protein, a saliva

component involved in brown planthopper virulence and host adapta-

tion. J Insect Physiol 98:223–230

Huang H-J, Cui J-R, Xia X, Chen J, Ye Y-X, Zhang C-X, Hong X-Y (2019a) Salivary

DNase II from Laodelphax striatellus acts as an eﬀector that suppresses

plant defence. New Phytol 224:860–874

Huang HJ, Zhang CX, Hong XY (2019b) How does saliva function in planthop-

per-host interactions? Arch Insect Biochem Physiol 100:e21537

Irieda H, Inoue Y, Mori M, Yamada K, Oshikawa Y, Saitoh H, Uemura A, Terauchi

R, Kitakura S, Kosaka A, Singkaravanit-Ogawa S, Takano Y (2019) Con-

served fungal eﬀector suppresses PAMP-triggered immunity by target-

ing plant immune kinases. Proc Natl Acad Sci USA 116:496–505

Ishikawa K, Yamaguchi K, Sakamoto K, Yoshimura S, Inoue K, Tsuge S, Kojima C,

Kawasaki T (2014) Bacterial eﬀector modulation of host E3 ligase activ-

ity suppresses PAMP-triggered immunity in rice. Nat Commun 5:5430

Iyer AS, McCouch SR (2004) The rice bacterial blight resistance gene xa5

encodes a novel form of disease resistance. Mol Plant Microbe Interact

17:1348–1354

Jha G, Rajeshwari R, Sonti RV (2005) Bacterial type two secretion system

secreted proteins: double-edged swords for plant pathogens. Mol Plant

Microbe Interact 18:891–898

Jha G, Rajeshwari R, Sonti RV (2007) Functional interplay between two Xan-

thomonas oryzae pv, oryzae secretion systems in modulating virulence

on rice. Mol Plant Microbe Interact 20:31–40

Ji R, Yu H, Fu Q, Chen H, Ye W, Li S, Lou Y (2013) Comparative transcriptome

analysis of salivary glands of two populations of rice brown planthop-

per, Nilaparvata lugens, that diﬀer in virulence. PLoS ONE, 8, e79612

Ji Z, Ji C, Liu B, Zou L, Chen G, Yang B (2016) Interfering TAL eﬀectors of Xan-

thomonas oryzae neutralize R-gene-mediated plant disease resistance.

Nat Commun 7:13435

Ji R, Ye W, Chen H, Zeng J, Li H, Yu H, Li J, Lou Y (2017) A salivary endo-beta-1,4-

glucanase acts as an eﬀector that enables the brown planthopper to

feed on rice. Plant Physiol 173:1920–1932

Ji C, Ji Z, Liu B, Cheng H, Liu H, Liu S, Yang B, Chen G (2020a) Xa1 allelic R genes

activate rice blight resistance suppressed by interfering TAL eﬀectors.

Plant Commun 1:100087

Ji H, Liu D, Zhang Z, Sun J, Han B, Li Z (2020b) A bacterial F-box eﬀector sup-

presses SAR immunity through mediating the proteasomal degrada-

tion of OsTrxh2 in rice. Plant J 104:1054–1072

Jia Y, McAdams SA, Bryan GT, Hershey HP, Valent B (2000) Direct interaction of

resistance gene and avirulence gene products confers rice blast resist-

ance. Embo J 19:4004–4014

Jones K, Kim DW, Park JS, Khang CH (2016) Live-cell ﬂuorescence imaging to

investigate the dynamics of plant cell death during infection by the rice

blast fungus Magnaporthe oryzae. BMC Plant Biol 16:69

Kang S, Sweigard JA, Valent B (1995) The PWL host speciﬁcity gene family

in the blast fungus Magnaporthe grisea. Mol Plant Microbe Interact

8:939–948

Kanzaki H, Yoshida K, Saitoh H, Fujisaki K, Hirabuchi A, Alaux L, Fournier E,

Tharreau D, Terauchi R (2012) Arms race co-evolution of Magnaporthe

oryzae AVR-Pik and rice Pik genes driven by their physical interactions.

Plant J 72:894–907

Khan M, Seto D, Subramaniam R, Desveaux D (2018) Oh, the places they’ll

go! A survey of phytopathogen eﬀectors and their host targets. Plant J

93:651–663

Khang CH, Berruyer R, Giraldo MC, Kankanala P, Park SY, Czymmek K, Kang

S, Valent B (2010) Translocation of Magnaporthe oryzae eﬀectors into

rice cells and their subsequent cell-to-cell movement. Plant Cell

22:1388–1403

KHUSH, G. S. (2005) What it will take to feed 5.0 billion rice consumers in 2030.

Plant Mol Biol 59:1–6

Konishi H, Noda H, Tamura Y, Hattori M (2009) Proteomic analysis of the salivary

glands of the rice brown planthopper, Nilaparvata lugens (Stål) (Hom-

optera: Delphacidae). Appl Entomol Zool 44:525–534

Lee BM, Park YJ, Park DS, Kang HW, Kim JG, Song ES, Park IC, Yoon UH, Hahn JH,

Koo BS, Lee GB, Kim H, Park HS, Yoon KO, Kim JH, Jung CH, Koh NH, Seo

JS, Go SJ (2005) The genome sequence of Xanthomonas oryzae patho-

var oryzae KACC10331, the bacterial blight pathogen of rice. Nucleic

Acids Res 33:577–586

Li W, Wang B, Wu J, Lu G, Hu Y, Zhang X, Zhang Z, Zhao Q, Feng Q, Zhang H,

Wang Z, Wang G, Han B, Wang Z, Zhou B (2009) The Magnaporthe ory-

zae avirulence gene AvrPiz-t encodes a predicted secreted protein that

triggers the immunity in rice mediated by the blast resistance gene

Piz-t. Mol Plant Microbe Interact 22:411–420

Content courtesy of Springer Nature, terms of use apply. Rights reserved.

Page 19 of 21

Debetal. Rice (2021) 14:94

Li R, Wang S, Sun R, He X, Liu Y, Song C (2018a) Xanthomonas oryzae pv. oryzae

type III eﬀector PthXo3JXOV suppresses innate immunity, induces

susceptibility and binds to multiple targets in rice. FEMS Microbiol Lett.

https:// doi. org/ 10. 1093/ femsle/ fny037

Li T, Wen J, Zhang Y, Correll J, Wang L, Pan Q (2018b) Reconstruction of an

SSR-based Magnaporthe oryzae physical map to locate avirulence gene

AvrPi12. BMC Microbiol 18:47

Li Y, Liu X, Liu M, Wang Y, Zou Y, You Y, Yang L, Hu J, Zhang H, Zheng X, Wang P,

Zhang Z (2020) Magnaporthe oryzae auxiliary activity protein MoAa91

Functions as chitin-binding protein to induce Appressorium Formation

on artiﬁcial inductive surfaces and suppress plant immunity. Mbio

11:e03304-19

Liu X, Zhou H, Zhao J, Hua H, He Y (2016) Identiﬁcation of the secreted watery

saliva proteins of the rice brown planthopper, Nilaparvata lugens (Stal)

by transcriptome and Shotgun LC-MS/MS approach. J Insect Physiol

89:60–69

Long J, Song C, Yan F, Zhou J, Zhou H, Yang B (2018) Non-TAL eﬀectors from

Xanthomonas oryzae pv. oryzae suppress peptidoglycan-triggered

MAPK activation in rice. Front Plant Sci 9:1857

Ma W, Zou L, Zhiyuan JI, Xiameng XU, Zhengyin XU, Yang Y, Alfano JR, Chen G

(2018) Xanthomonas oryzae pv. oryzae TALE proteins recruit OsTFIIAg-

amma1 to compensate for the absence of OsTFIIAgamma5 in bacterial

blight in rice. Mol Plant Pathol 19:2248–2262

Ma W, Xu X, Cai L, Cao Y, Haq F, Alfano JR, Zhu B, Zou L, Chen G (2020) A

Xanthomonas oryzae type III eﬀector XopL causes cell death through

mediating ferredoxin degradation in Nicotiana benthamiana. Phyto-

pathol Res 2:16

Matsumoto Y, Hattori M (2018) The green rice leafhopper, Nephotettix cincti-

ceps (Hemiptera: Cicadellidae), salivary protein NcSP75 is a key eﬀector

for successful phloem ingestion. PLoS ONE 13:e0202492

Matsumoto Y, Suetsugu Y, Nakamura M, Hattori M (2014) Transcriptome

analysis of the salivary glands of Nephotettix cincticeps (Uhler). J Insect

Physiol 71:170–176

Mentlak TA, Kombrink A, Shinya T, Ryder LS, Otomo I, Saitoh H, Terauchi R,

Nishizawa Y, Shibuya N, Thomma BP, Talbot NJ (2012) Eﬀector-mediated

suppression of chitin-triggered immunity by Magnaporthe oryzae is

necessary for rice blast disease. Plant Cell 24:322–335

Miao Y, Jia H, Li Z, Liu Y, Hou M (2018a) Transcriptomic and expression analysis

of the salivary glands in Brown Planthoppers, Nilaparvata lugens

(Hemiptera: Delphacidae). J Econ Entomol 111:2884–2893

Miao YT, Deng Y, Jia HK, Liu YD, Hou ML (2018b) Proteomic analysis of watery

saliva secreted by white-backed planthopper, Sogatella furcifera. PLoS

ONE 13:e0193831

Mogga V, Delventhal R, Weidenbach D, Langer S, Bertram PM, Andresen K,

Thines E, Kroj T, Schaﬀrath U (2016) Magnaporthe oryzae eﬀectors

MoHEG13 and MoHEG16 interfere with host infection and MoHEG13

counteracts cell death caused by Magnaporthe-NLPs in tobacco. Plant

Cell Rep 35:1169–1185

Mondal KK, Verma G, Junaid MA, Mani C (2016) Rice pathogen Xanthomonas

oryzae pv oryzae employs inducible hrp-dependent XopF type III

eﬀector protein for its growth, pathogenicity and for suppression of PTI

response to induce blight disease. Eur J Plant Pathol 144:311–323

Mosquera G, Giraldo MC, Khang CH, Coughlan S, Valent B (2009) Interac-

tion transcriptome analysis identiﬁes Magnaporthe oryzae BAS1-4 as

Biotrophy-associated secreted proteins in rice blast disease. Plant Cell

21:1273–1290

Mücke S, Reschke M, Erkes A, Schwietzer CA, Becker S, Streubel J, Morgan RD,

Wilson GG, Grau J, Boch J (2019) Transcriptional reprogramming of rice

cells by Xanthomonas oryzae TALEs. Front Plant Sci 10:162

Mudgertt MB (2005) New insights to the function of phytopathogenic bacte-

rial type III eﬀectors in plants. Annu Rev Plant Biol 56:509–531

Nakamura M, Hattori M (2013) Puriﬁcation of β-glucosidase from the salivary

glands of the green rice leafhopper, Nephotettix cincticeps (Uhler)

(Hemiptera: Cicadellidae), and its detection in the salivary sheath. Appl

Entomol Zool 48:489–497

Park CH, Chen S, Shirsekar G, Zhou B, Khang CH, Songkumarn P, Afzal AJ, Ning

Y, Wang R, Bellizzi M, Valent B, Wang GL (2012) The Magnaporthe oryzae

eﬀector AvrPiz-t targets the RING E3 ubiquitin ligase APIP6 to suppress

pathogen-associated molecular pattern-triggered immunity in rice.

Plant Cell 24:4748–4762

Park CH, Shirsekar G, Bellizzi M, Chen S, Songkumarn P, Xie X, Shi X, Ning Y,

Zhou B, Suttiviriya P, Wang M, Umemura K, Wang GL (2016) The E3

ligase APIP10 connects the eﬀector AvrPiz-t to the NLR receptor Piz-t in

rice. PLoS Pathog 12:e1005529

Patkar RN, Benke PI, Qu Z, Chen YY, Yang F, Swarup S, Naqvi NI (2015) A fungal

monooxygenase-derived jasmonate attenuates host innate immunity.

Nat Chem Biol 11:733–740

Pennisi A (2010) Armed and dangerous. Science 327:804–805

Petrova A, Smith CM (2014) Immunodetection of a brown planthopper

(Nilaparvata lugens Stal) salivary catalase-like protein into tissues of rice,

Oryza sativa. Insect Mol Biol 23:13–25

Petrova A, Smith CM (2015) Application of Brown Planthopper salivary gland

extract to rice plants induces systemic host mRNA patterns associated

with nutrient remobilization. PLoS ONE 10:e0141769

Pruitt RN, Schwessinger B, Joe A, Thomas N, Liu F, Albert M, Robinson MR, Chan

LJG, Luu DD, Chen H, Bahar O, Daudi A, de Vleesschauwer D, Caddell D,

Zhang W, Zhao X, Li X, Heazlewood JL, Ruan D, Majumder D, Chern M,

Kalbacher H, Midha S, Patil PB, Sonti RV, Petzold CJ, Liu CC, Brodbelt JS,

Felix G, Ronald PC (2015) The rice immune receptor XA21 recognizes

a tyrosine-sulfated protein from a Gram-negative bacterium. Sci Adv

1:e1500245

Qian G, Zhou Y, Zhao Y, Song Z, Wang S, Fan J, Hu B, Venturi V, Liu F (2013)

Proteomic analysis reveals novel extracellular virulence-associated

proteins and functions regulated by the diﬀusible signal factor (DSF) in

Xanthomonas oryzae pv. oryzicola. J Proteome Res 12:3327–3341

Quintana-Rodriguez E, Duran-Flores D, Heil M, Camacho-Coronel X (2018)

Damage-associated molecular patterns (DAMPs) as future plant vac-

cines that protect crops from pests. Sci Hortic 237:207–220

Rajeshwari R, Jha G, Sonti RV (2005) Role of an in planta-expressed xylanase

of Xanthomonas oryzae pv. oryzae in promoting virulence on rice. Mol

Plant Microbe Interact 18:830–837

Rao W, Zheng X, Liu B, Guo Q, Guo J, Wu Y, Shangguan X, Wang H, Wu D, Wang

Z, Hu L, Xu C, Jiang W, Huang J, Shi S, He G (2019) Secretome analysis

and in planta expression of salivary proteins identify candidate eﬀectors

from the Brown Planthopper Nilaparvata lugens. Mol Plant Microbe

Interact 32:227–239

Ray SK, Rajeshwari R, Sonti RV (2000) Mutants of Xanthomonas oryzae pv. ory-

zae deﬁcient in general secretory pathway are virulence deﬁcient and

unable to secrete xylanase. Mol Plant Microbe Interact 13:394–401

Read AC, Rinaldi FC, Hutin M, He YQ, Triplett LR, Bogdanove AJ (2016) Sup-

pression of Xo1-mediated disease resistance in rice by a truncated,

non-DNA-binding TAL eﬀector of Xanthomonas oryzae. Front Plant Sci

7:1516

Ribot C, Cesari S, Abidi I, Chalvon V, Bournaud C, Vallet J, Lebrun MH, Morel JB,

Kroj T (2013) The Magnapor the oryzae eﬀector AVR1-CO39 is translo-

cated into rice cells independently of a fungal-derived machinery. Plant

J 74:1–12

Rodriguez PA, Bos JI (2013) Toward understanding the role of aphid eﬀectors

in plant infestation. Mol Plant Microbe Interact 26:25–30

Saitoh H, Fujisawa S, Mitsuoka C, Ito A, Hirabuchi A, Ikeda K, Irieda H, Yoshino

K, Yoshida K, Matsumura H, Tosa Y, Win J, Kamoun S, Takano Y, Terauchi

R (2012) Large-scale gene disruption in Magnaporthe oryzae identiﬁes

MC69, a secreted protein required for infection by monocot and dicot

fungal pathogens. PLoS Pathog 8:e002711

Sakulkoo W, Oses-Ruiz M, Oliveira Garcia E, Soanes DM, Littlejohn GR, Hacker

C, Correia A, Valent B, Talbot NJ (2018) A single fungal MAP kinase

controls plant cell-to-cell invasion by the rice blast fungus. Science

359:1399–1403

Salzberg SL, Sommer DD, Schatz MC, Phillippy AM, Rabinowicz PD, Tsuge S,

Furutani A, Ochiai H, Delcher AL, Kelley D, Madupu R, Puiu D, Radune

D, Shumway M, Trapnell C, Aparna G, Jha G, Pandey A, Patil PB, Ishihara

H, Meyer DF, Szurek B, Verdier V, Koebnik R, Dow JM, Ryan RP, Hirata H,

Tsuyumu S, Won Lee S, Ronald PC, Sonti RV, Van Sluys M-A, Leach JE,

White FF, Bogdanove AJ (2008) Genome sequence and rapid evolution

of the rice pathogen Xanthomonas oryzae pv. oryzae PXO99A. BMC

Genomics 9:204

Shangguan X, Zhang J, Liu B, Zhao Y, Wang H, Wang Z, Guo J, Rao W, Jing S,

Guan W, Ma Y, Wu Y, Hu L, Chen R, Du B, Zhu L, Yu D, He G (2018) A

Mucin-like protein of planthopper is required for feeding and induces

immunity response in plants. Plant Physiol 176:552–565

Content courtesy of Springer Nature, terms of use apply. Rights reserved.

Page 20 of 21

Debetal. Rice (2021) 14:94

Shen Y, Ronald P (2002) Molecular determinants of disease and resistance in

interactions of Xanthomonas oryzae pv. oryzae and rice. Microbes Infect

4:1361–1367

Shi X, Long Y, He F, Zhang C, Wang R, Zhang T, Wu W, Hao Z, Wang Y, Wang GL,

Ning Y (2018) The fungal pathogen Magnaporthe oryzae suppresses

innate immunity by modulating a host potassium channel. PLoS

Pathog 14:e1006878

Shinya T, Hojo Y, Desaki Y, Christeller JT, Okada K, Shibuya N, Galis I (2016)

Modulation of plant defense responses to herbivores by simultaneous

recognition of diﬀerent herbivore-associated elicitors in rice. Sci Rep

6:32537

Shipman EN, Jones K, Jenkinson CB, Kim DW, Zhu J, Khang CH (2017) Nuclear

and structural dynamics during the establishment of a specialized

eﬀector-secreting cell by Magnaporthe oryzae in living rice cells. BMC

Cell Biol 18:11

Singh R, Dangol S, Chen Y, Choi J, Cho YS, Lee JE, Choi MO, Jwa NS (2016)

Magnaporthe oryzae eﬀector AVR-Pii helps to establish compatibility

by inhibition of the rice NADP-Malic enzyme resulting in disruption of

oxidative burst and host innate immunity. Mol Cells 39:426–438

Sinha DK, Bentur JS, Nair S (2011) Compatible interaction with its rice host

leads to enhanced expression of the gamma subunit of oligosaccharyl

transferase in the Asian rice gall midge, Orseolia oryzae. Insect Mol Biol

20:567–575

Sinha DK, Atray I, Bentur JS, Nair S (2012) Expression of Orseolia oryzae nucleo-

side diphosphate kinase (OoNDPK) is enhanced in rice gall midge

feeding on susceptible rice hosts and its over-expression leads to salt

tolerance in Escherichia coli. Insect Mol Biol 21:593–603

Sogawa C (1967) Chemical Nature of the Sheath Materials Secreted by Leaf-

hoppers (Homoptera). Appl Entomol Zool 2:13–21

Sōgawa C (1982) THE RICE BROWN PLANTHOPPER: feeding physiology and

host plant interactions. Annu Rev Entomol 27:49–73

Song C, Yang B (2010) Mutagenesis of 18 type III eﬀectors reveals virulence

function of XopZ(PXO99) in Xanthomonas oryzae pv. oryzae. Mol Plant

Microbe Interact 23:893–902

Song WY, Wang GL, Chen LL, Kim HS, Pi LY, Holsten T, Gardner J, Wang B,

Zhai WX, Zhu LH, Fauquet C, Ronald P (1995) A receptor kinase-like

protein encoded by the rice disease resistance gene, Xa21. Science

270:1804–1806

Streubel J, Pesce C, Hutin M, Koebnik R, Boch J, Szurek B (2013) Five phyloge-

netically close rice SWEET genes confer TAL eﬀector-mediated suscepti-

bility to Xanthomonas oryzae pv. oryzae. New Phytol 200:808–819

Sugio A, Yang B, Zhu T, White FF (2007) Two type III eﬀector genes of Xan-

thomonas oryzae pv. oryzae control the induction of the host genes

OsTFIIAgamma1 and OsTFX1 during bacterial blight of rice. Proc Natl

Acad Sci USA 104:10720–10725

Sun X, Cao Y, Yang Z, Xu C, Li X, Wang S, Zhang Q (2004) Xa26, a gene confer-

ring resistance to Xanthomonas oryzae pv. oryzae in rice, encodes an

LRR receptor kinase-like protein. Plant J 37:517–527

Sun QH, Hu J, Huang GX, Ge C, Fang RX, He CZ (2005) Type-II secretion

pathway structural gene xpsE, xylanase- and cellulase secretion and

virulence in Xanthomonas oryzae pv. oryzae. Plant Pathol 54:15–21

Sweigard JA, Carroll AM, Kang S, Farrall L, Chumley FG, Valent B (1995) Identi-

ﬁcation, cloning, and characterization of PWL2, a gene for host species

speciﬁcity in the rice blast fungus. Plant Cell 7:1221–1233

Tang M, Ning Y, Shu X, Dong B, Zhang H, Wu D, Wang H, Wang GL, Zhou B

(2017) The Nup98 homolog APIP12 targeted by the eﬀector AvrPiz-t

is involved in rice basal resistance against Magnaporthe oryzae. Rice (n

Y) 10:5

Tayi L, Maku R, Patel HK, Sonti RV (2016a) Action of multiple cell wall-degrad-

ing enzymes is required for elicitation of innate immune responses dur-

ing Xanthomonas oryzae pv. oryzae infection in rice. Mol Plant Microbe

Interact 29:599–608

Tayi L, Maku RV, Patel HK, Sonti RV (2016b) Identiﬁcation of pectin degrading

enzymes secreted by Xanthomonas oryzae pv. oryzae and determina-

tion of their role in virulence on rice. PLoS ONE 11:66396

Tayi L, Kumar S, Nathawat R, Haque AS, Maku RV, Patel HK, Sankaranarayanan R,

Sonti RV (2018) A mutation in an exoglucanase of Xanthomonas oryzae

pv. oryzae, which confers an endo mode of activity, aﬀects bacterial

virulence, but not the induction of immune responses, in rice. Mol Plant

Pathol 19:1364–1376

Tian D, Wang J, Zeng X, Gu K, Qiu C, Yang X, Zhou Z, Goh M, Luo Y, Murata-Hori

M, White FF, Yin Z (2014) The rice TAL eﬀector-dependent resistance

protein XA10 triggers cell death and calcium depletion in the endo-

plasmic reticulum. Plant Cell 26:497–515

Toruno TY, Stergiopoulos I, Coaker G (2016) Plant-pathogen eﬀectors: cellular

probes interfering with plant defenses in spatial and temporal manners.

Annu Rev Phytopathol 54:419–441

Tran TT, Perez-Quintero AL, Wonni I, Carpenter SCD, Yu Y, Wang L, Leach JE,

Verdier V, Cunnac S, Bogdanove AJ, Koebnik R, Hutin M, Szurek B (2018)

Functional analysis of African Xanthomonas oryzae pv. oryzae TALomes

reveals a new susceptibility gene in bacterial leaf blight of rice. PLoS

Pathog 14:e1007092

Triplett LR, Cohen SP, Heﬀelﬁnger C, Schmidt CL, Huerta AI, Tekete C, Verdier

V, Bogdanove AJ, Leach JE (2016) A resistance locus in the American

heirloom rice variety Carolina Gold Select is triggered by TAL eﬀectors

with diverse predicted targets and is eﬀective against African strains of

Xanthomonas oryzae pv. oryzicola. Plant J 87:472–483

van Buyten E, Hofte M (2013) Pythium species from rice roots diﬀer in viru-

lence, host colonization and nutritional proﬁle. BMC Plant Biol 13:203

Varden FA, de la Concepcion JC, Maidment JH, Banﬁeld MJ (2017) Taking the

stage: eﬀectors in the spotlight. Curr Opin Plant Biol 38:25–33

Wang Y, Wang Y (2018) Trick or treat: microbial pathogens evolved apoplas-

tic eﬀectors modulating plant susceptibility to infection. Mol Plant

Microbe Interact 31:6–12

Wang YS, Pi LY, Chen X, Chakrabarty PK, Jiang J, de Leon AL, Liu GZ, Li L, Benny

U, Oard J, Ronald PC, Song WY (2006) Rice XA21 binding protein 3 is

a ubiquitin ligase required for full Xa21-mediated disease resistance.

Plant Cell 18:3635–3646

Wang X, Kota U, He K, Blackburn K, Li J, Goshe MB, Huber SC, Clouse SD (2008)

Sequential transphosphorylation of the BRI1/BAK1 receptor kinase

complex impacts early events in brassinosteroid signaling. Dev Cell

15:220–235

Wang CL, Qin TF, Yu HM, Zhang XP, Che JY, Gao Y, Zheng CK, Yang B, Zhao

KJ (2014) The broad bacterial blight resistance of rice line CBB23 is

triggered by a novel transcription activator-like (TAL) eﬀector of Xan-

thomonas oryzae pv. oryzae. Mol Plant Pathol 15:333–341

Wang C, Zhang X, Fan Y, Gao Y, Zhu Q, Zheng C, Qin T, Li Y, Che J, Zhang M,

Yang B, Liu Y, Zhao K (2015) XA23 is an executor R protein and confers

broad-spectrum disease resistance in rice. Mol Plant 8:290–302

Wang R, Ning Y, Shi X, He F, Zhang C, Fan J, Jiang N, Zhang Y, Zhang T, Hu Y, Bel-

lizzi M, Wang GL (2016a) Immunity to rice blast disease by suppression

of eﬀector-triggered necrosis. Curr Biol 26:2399–2411

Wang S, Sun J, Fan F, Tan Z, Zou Y, Lu D (2016b) A Xanthomonas oryzae pv.

oryzae eﬀector, XopR, associates with receptor-like cytoplasmic kinases

and suppresses PAMP-triggered stomatal closure. Sci China Life Sci

59:897–905

Wang Y, Wu J, Kim SG, Tsuda K, Gupta R, Park SY, Kim ST, Kang KY (2016c) Mag-

naporthe oryzae-secreted protein MSP1 induces cell death and elicits

defense responses in rice. Mol Plant Microbe Interact 29:299–312

Wang C, Wang G, Zhang C, Zhu P, Dai H, Yu N, He Z, Xu L, Wang E (2017)

OsCERK1-mediated chitin perception and immune signaling requires

receptor-like cytoplasmic kinase 185 to activate an MAPK cascade in

rice. Mol Plant 10:619–633

Weber E, Ojanen-Reuhs T, Huguet E, Hause G, Romantschuk M, Korhonen TK,

Bonas U, Koebnik R (2005) The type III-dependent Hrp pilus is required

for productive interaction of Xanthomonas campestris pv. vesicatoria

with pepper host plants. J Bacteriol 187:2458–2468

White FF, Yang B (2009) Host and pathogen factors controlling the rice-Xan-

thomonas oryzae interaction. Plant Physiol 150:1677–1686

Wilkins KE, Booher NJ, Wang L, Bogdanove AJ (2015) TAL eﬀectors and activa-

tion of predicted host targets distinguish Asian from African strains

of the rice pathogen Xanthomonas oryzae pv. oryzicola while strict

conservation suggests universal importance of ﬁve TAL eﬀectors. Front

Plant Sci 6:536

Wu J, Kou Y, Bao J, Li Y, Tang M, Zhu X, Ponaya A, Xiao G, Li J, Li C, Song MY,

Cumagun CJ, Deng Q, Lu G, Jeon JS, Naqvi NI, Zhou B (2015) Compara-

tive genomics identiﬁes the Magnaporthe oryzae avirulence eﬀector

AvrPi9 that triggers Pi9-mediated blast resistance in rice. New Phytol

206:1463–1475

Content courtesy of Springer Nature, terms of use apply. Rights reserved.

Page 21 of 21

Debetal. Rice (2021) 14:94

Xiang Y, Cao Y, Xu C, Li X, Wang S (2006) Xa3, conferring resistance for rice bac-

terial blight and encoding a receptor kinase-like protein, is the same as

Xa26. Theor Appl Genet 113:1347–1355

Yamaguchi K, Nakamura Y, Ishikawa K, Yoshimura Y, Tsuge S, Kawasaki T (2013a)

Suppression of rice immunity by Xanthomonas oryzae type III eﬀector

Xoo2875. Biosci Biotechnol Biochem 77:796–801

Yamaguchi K, Yamada K, Ishikawa K, Yoshimura S, Hayashi N, Uchihashi K,

Ishihama N, Kishi-Kaboshi M, Takahashi A, Tsuge S, Ochiai H, Tada Y, Shi-

mamoto K, Yoshioka H, Kawasaki T (2013b) A receptor-like cytoplasmic

kinase targeted by a plant pathogen eﬀector is directly phosphorylated

by the chitin receptor and mediates rice immunity. Cell Host Microbe

13:347–357

Yan X, Talbot NJ (2016) Investigating the cell biology of plant infection by the

rice blast fungus Magnaporthe oryzae. Curr Opin Microbiol 34:147–153

Yang B, White FF (2004) Diverse members of the AvrBs3/PthA family of type III

eﬀectors are major virulence determinants in bacterial blight disease of

rice. Mol Plant Microbe Interact 17:1192–1200

Yang B, Sugio A, White FF (2006) Os8N3 is a host disease-susceptibility gene

for bacterial blight of rice. Proc Natl Acad Sci USA 103:10503–10508

Ye W, Yu H, Jian Y, Zeng J, Ji R, Chen H, Lou Y (2017) A salivary EF-hand calcium-

binding protein of the brown planthopper Nilaparvata lugens func-

tions as an eﬀector for defense responses in rice. Sci Rep 7:40498

Yoshida K, Saitoh H, Fujisawa S, Kanzaki H, Matsumura H, Yoshida K, Tosa Y,

Chuma I, Takano Y, Win J, Kamoun S, Terauchi R (2009) Association

genetics reveals three novel avirulence genes from the rice blast fungal

pathogen Magnaporthe oryzae. Plant Cell 21:1573–1591

Yoshimura S, Yamanouchi U, Katayose Y, Toki S, Wang ZX, Kono I, Kurata N, Yano

M, Iwata N, Sasaki T (1998) Expression of Xa1, a bacterial blight-resist-

ance gene in rice, is induced by bacterial inoculation. Proc Natl Acad Sci

USA 95:1663–1668

Yuan M, Wang S (2013) Rice MtN3/saliva/SWEET family genes and their

homologs in cellular organisms. Mol Plant 6:665–674

Yuan M, Chu Z, Li X, Xu C, Wang S (2009) Pathogen-induced expressional loss

of function is the key factor in race-speciﬁc bacterial resistance con-

ferred by a recessive R gene xa13 in rice. Plant Cell Physiol 50:947–955

Yun CS, Motoyama T, Osada H (2015) Biosynthesis of the mycotoxin tenu-

azonic acid by a fungal NRPS-PKS hybrid enzyme. Nat Commun 6:8758

Zhang S, Wang L, Wu W, He L, Yang X, Pan Q (2015) Function and evolution

of Magnaporthe oryzae avirulence gene AvrPib responding to the rice

blast resistance gene Pib. Sci Rep 5:11642

Zhang C, Fang H, Shi X, He F, Wang R, Fan J, Bai P, Wang J, Park CH, Bellizzi M,

Zhou X, Wang GL, Ning Y (2020) A fungal eﬀector and a rice NLR protein

have antagonistic eﬀects on a Bowman-Birk trypsin inhibitor. Plant

Biotechnol J 18:2354–2363

Zhao S, Mo WL, Wu F, Tang W, Tang JL, Szurek B, Verdier V, Koebnik R, Feng JX

(2013) Identiﬁcation of non-TAL eﬀectors in Xanthomonas oryzae pv.

oryzae Chinese strain 13751 and analysis of their role in the bacterial

virulence. World J Microbiol Biotechnol 29:733–744

Zhou J, Peng Z, Long J, Sosso D, Liu B, Eom JS, Huang S, Liu S, Vera Cruz C,

Frommer WB, White FF, Yang B (2015) Gene targeting by the TAL eﬀec-

tor PthXo2 reveals cryptic resistance gene for bacterial blight of rice.

Plant J 82:632–643

Zou HS, Song X, Zou LF, Yuan L, Li YR, Guo W, Che YZ, Zhao WX, Duan YP, Chen

GY (2012) EcpA, an extracellular protease, is a speciﬁc virulence factor

required by Xanthomonas oryzae pv. oryzicola but not by X. oryzae pv.

oryzae in rice. Microbiology 158:2372–2383

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Phosphate accumulation in rice leaves promotes fungal pathogenicity and represses host immune responses during pathogen infection

Article

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Jan 2024

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Verticillium dahliae isolates causing devastating vascular wilt in cotton plants can be divided into defoliating and nondefoliating pathotypes. The mechanisms underlying how V. dahliae uses secretory proteins to manipulate plant physiological processes and suppress immunity in cotton plants have received renewed research focus over the past several years. Here, we describe the role of a secretory protein named VdSAP (secretory aspartyl protease) from the defoliating V. dahliae strain XJ592 in virulence and defoliation. Deletion of VdSAP in strain XJ592 led to significantly reduced virulence and cotton plant defoliation. VdSAP functioned as a protease that targeted cotton plant GhARP (auxin‐repressed protein), and VdSAP negatively regulated GhARP content in plants. Transient expression of GhARP in Nicotiana benthamiana enhanced the expression of plant defence signals and inhibited plant abscission signals. Furthermore, GhARP negatively regulated the ethylene (ET) signal and positively regulated the salicylic acid (SA) signal. In addition, GhARP interacted with 1‐aminocyclopropane carboxylate oxidases (GhACOs), suggesting that it might function through the ET signal during V. dahliae–cotton plant interactions. These results suggest that GhARP is a molecular link between plant defence and abscission signals, and that VdSAP decreases accumulation of GhARP and enhances the virulence and defoliation caused by V. dahliae.

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Rice is a crucial food crop worldwide, but its yield and quality are significantly affected by Meloidogyne graminicola is a root knot nematode. No rice variety is entirely immune to this nematode disease in agricultural production. Thus, the fundamental strategy to combat this disease is to utilize rice resistance genes. In this study, we conducted transcriptome and metabolome analyses on two rice varieties, ZH11 and IR64. The results indicated that ZH11 showed stronger resistance than IR64. Transcriptome analysis revealed that the change in gene expression in ZH11 was more substantial than that in IR64 after M. graminicola infection. Moreover, GO and KEGG enrichment analysis of the upregulated genes in ZH11 showed that they were primarily associated with rice cell wall construction, carbohydrate metabolism, and secondary metabolism relating to disease resistance, which effectively enhanced the resistance of ZH11. However, in rice IR64, the number of genes enriched in disease resistance pathways was significantly lower than that in ZH11, which further explained susceptibility to IR64. Metabolome analysis revealed that the metabolites detected in ZH11 were enriched in flavonoid metabolism and the pentose phosphate pathway, compared to IR64, after M. graminicola infection. The comprehensive analysis of transcriptome and metabolome data indicated that flavonoid metabolism plays a crucial role in rice resistance to M. graminicola infection. The content of kaempferin, apigenin, and quercetin in ZH11 significantly increased after M. graminicola infection, and the expression of genes involved in the synthetic pathway of flavonoids also significantly increased in ZH11. Our study provides theoretical guidance for the precise analysis of rice resistance and disease resistance breeding in further research.

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Article

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Jessie Fernandez

Magnaporthe oryzae is a hemibiotrophic fungus responsible for the economically devastating and recalcitrant rice blast disease. However, the blast fungus is not only restricted to rice plants as it can also infect wheat, millet, and other crops. Despite previous outstanding discoveries aimed to understand and control the disease, the fungus remains one of the most important pathogens that threatens global food security. To cause disease, M. oryzae initiates morphological changes to attach, penetrate, and colonize rice cells, all while suppressing plant immune defenses that would otherwise hinder its proliferation. As such, M. oryzae actively secretes a battery of small proteins called “effectors” to manipulate host machinery. In this review, we summarize the latest findings in effector identification, expression, regulation, and functionality. We review the most studied effectors and their roles in pathogenesis. Additionally, we discern the current methodologies to structurally catalog effectors, and we highlight the importance of climate change and its impact on the future of rice blast disease.

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Apr 2021
FUNGAL GENET BIOL

Magnaporthe oryzae is the causal agent of rice blast disease, the most widespread and serious disease of cultivated rice. Live cell imaging and quantitative 4D image analysis have provided new insight into the mechanisms by which the fungus infects host cells and spreads rapidly in plant tissue. In this video review article, we apply live cell imaging approaches to understanding the cell and developmental biology of rice blast disease. To gain entry to host plants, M. oryzae develops a specialised infection structure called an appressorium, a unicellular dome-shaped cell which generates enormous turgor, translated into mechanical force to rupture the leaf cuticle. Appressorium development is induced by perception of the hydrophobic leaf surface and nutrient deprivation. Cargo-independent autophagy in the three-celled conidium, controlled by cell cycle regulation, is essential for appressorium morphogenesis. Appressorium maturation involves turgor generation and melanin pigment deposition in the appressorial cell wall. Once a threshold of turgor has been reached, this triggers re-polarisation which requires regulated generation of reactive oxygen species, to facilitate septin GTPase-dependent cytoskeletal re-organisation and re-polarisation of the appressorium to form a narrow, rigid penetration peg. Infection of host tissue requires a further morphogenetic transition to a pseudohyphal-type of growth within colonised rice cells. At the same time the fungus secretes an arsenal of effector proteins to suppress plant immunity. Many effectors are secreted into host cells directly, which involves a specific secretory pathway and a specialised structure called the biotrophic interfacial complex. Cell-to-cell spread of the fungus then requires development of a specialised structure, the transpressorium, that is used to traverse pit field sites, allowing the fungus to maintain host cell membrane integrity as new living plant cells are invaded. Thereafter, the fungus rapidly moves through plant tissue and host cells begin to die, as the fungus switches to necrotrophic growth and disease symptoms develop. These morphogenetic transitions are reviewed in the context of live cell imaging studies.

Xa7, a New Executor R Gene that Confers Durable and Broad-Spectrum Resistance to Bacteria-Blight Disease in Rice

Article

Full-text available

Jan 2021

Bacterial blight (BB) is a globally devastating rice disease caused by Xanthomonas oryzae pv. oryzae (Xoo). The use of disease resistance (R) genes in rice breeding is an effective and economical strategy for the control of this disease. Nevertheless, a majority of R genes lack durable resistance for long-term use under global warming conditions. Here, we report the isolation of a novel executor R gene, Xa7, that confers extremely durable, broad-spectrum, and heat-tolerant resistance to Xoo. The expression of Xa7 was induced by incompatible Xoo strains that secreted the transcription activator-like effector (TALE) AvrXa7 or PthXo3, which recognized effector binding elements (EBEs) in the Xa7 promoter. Furthermore, Xa7 induction was faster and stronger under high temperatures. Overexpression of Xa7 or co-transformation of Xa7 with avrXa7 triggered a hypersensitive response in plants. Constitutive expression of Xa7 activated a defense response in the absence of Xoo but inhibited the growth of transgenic rice plants. In addition, analysis of over 3000 rice varieties showed that the Xa7 locus was found primarily in the indica and aus subgroups. A variation consisting of an 11-bp insertion and a base substitution (G to T) was found in EBE AvrXa7 in the tested varieties, resulting in a loss of Xa7 BB resistance. Through a decade of effort, we have identified an important BB resistance gene and characterized its distinctive interaction with Xoo strains; these findings will greatly facilitate research on the molecular mechanism of Xa7-mediated resistance and promote the use of this valuable gene in breeding.

Erratum to: Magnaporthe oryzae effectors MoHEG13 and MoHEG16 interfere with host infection and MoHEG13 counteracts cell death caused by Magnaporthe-NLPs in tobacco

Article

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May 2016
PLANT CELL REP

A Xanthomonas oryzae type III effector XopL causes cell death through mediating ferredoxin degradation in Nicotiana benthamiana

Article

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Dec 2020

Abstract Plant pathogenic bacteria engage in an ongoing struggle for survival. Gram negative phytopathogenic prokaryotes deploy type III secretion system to deliver effector proteins into plant cells to manipulate the host cellular environment. In many cases, the targets of these effector proteins are unknown. The bacterial blight pathogen, Xanthomonas oryzae pv. oryzae (Xoo), causes a devastating disease in rice and the Xoo-rice interaction is an example of the ongoing evolutionary battle between plants and pathogens. In this study, we show that an effector XopL from Xoo exhibits E3 ubiquitin ligase activity and induces cell death in the nonhost Nicotiana benthamiana (Nb). Through yeast two-hybrid, co-immunoprecipitation, and biomolecular fluorescence complementation assays, it was shown that XopL interacts with ferredoxin (NbFd), an electron transport molecule in plant chloroplasts. XopL induced defense-related response in Nb and specifically targeted NbFd for ubiquitination and ubiquitin-mediated degradation, a process that increased the production of reactive oxygen species (ROS). This study demonstrates the ubiquitination and degradation of NbFd as a result of XopL activity, which further illustrates the tremendous functional diversity in Xanthomonas effector proteins.

Xa1 Allelic R Genes Activate Rice Blight Resistance Suppressed by Interfering TAL Effectors

Article

Full-text available

Jun 2020

Xanthomonas oryzae pathovar oryzae (Xoo) uses transcription activator-like effectors (TALEs) to cause bacterial blight (BB) in rice. In turn, rice has evolved several mechanisms to resist BB by targeting TALEs. One mechanism involves the nucleotide-binding leucine-rich repeat (NLR) resistance gene Xa1 and TALEs. Reciprocally, Xoo has evolved TALE variants, C-terminally truncated versions (interfering TALEs or iTALEs), to overcome Xa1 resistance. However, it remains unknown to what extent the two co-adaptive mechanisms mediate Xoo-rice interactions. In this study, we cloned and characterized five additional Xa1 allelic R genes, Xa2, Xa31(t), Xa14, CGS-Xo1 11 , and Xa45(t) from a collection of rice accessions. Sequence analysis revealed that Xa2 and Xa31(t) from different rice cultivars are identical. These genes and their predicted proteins were found to be highly conserved, forming a group of Xa1 alleles. The XA1 alleles could be distinguished by the number of C-terminal tandem repeats consisting of 93 amino acid residues and ranged from four in XA14 to seven in XA45(t). Xa1 allelic genes were identified in the 3000 rice genomes surveyed. On the other hand, iTALEs could suppress the resistance mediated by Xa1 allelic R genes, and iTALE genes were prevalent (∼95%) in Asian, but not in African Xoo strains. Our findings demonstrate the prominence of a defense mechanism in which rice depends on Xa1 alleles and a counteracting mechanism in which Xoo relies on iTALEs for BB.

A Fungal Effector and a Rice NLR Protein Have Antagonistic Effects on a Bowman‐Birk Trypsin Inhibitor

Article

Full-text available

Jul 2020
PLANT BIOTECHNOL J

Bowman‐Birk trypsin inhibitors (BBIs) play important roles in animal and plant immunity, but how these protease inhibitors are involved in the immune system remains unclear. Here, we show that the rice (Oryza sativa) BBI protein APIP4 is a common target of a fungal effector and an NLR receptor for innate immunity. APIP4 exhibited trypsin inhibitor activity in vitro and in vivo. Knock‐out of APIP4 in rice enhanced susceptibility and overexpression of APIP4 increased resistance to the fungal pathogen Magnaporthe oryzae. The M. oryzae effector AvrPiz‐t interacted with APIP4 and suppressed APIP4 trypsin inhibitor activity. By contrast, the rice NLR protein Piz‐t interacted with APIP4，enhancing APIP4 transcript and protein levels, and protease inhibitor activity. Our findings reveal a novel host defense mechanism in which a host protease inhibitor targeted by a fungal pathogen is protected by an NLR receptor.

Magnaporthe oryzae Auxiliary Activity Protein MoAa91 Functions as Chitin-Binding Protein To Induce Appressorium Formation on Artificial Inductive Surfaces and Suppress Plant Immunity

Article

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Mar 2020

The rice blast fungus Magnaporthe oryzae generates infection structure appressoria in response to surface cues largely due to functions of signaling molecules, including G-proteins, regulators of G-protein signaling (RGS), mitogen-activated protein (MAP) kinase pathways, cAMP signaling, and TOR signaling pathways. M. oryzae encodes eight RGS and RGS-like proteins (MoRgs1 to MoRgs8), and MoRgs1, MoRgs3, MoRgs4, and MoRgs7 were found to be particularly important in appressorium development. To explore the mechanisms by which these proteins regulate appressorium development, we have performed a comparative in planta transcriptomic study and identified an a uxiliary a ctivity family 9 protein (Aa9) homolog that we named MoAa91. We showed that MoAa91 was secreted from appressoria and that the recombinant MoAa91 could compete with a chitin elicitor-binding protein precursor (CEBiP) for chitin binding, thereby suppressing chitin-induced plant immunity. By identifying MoAa91 as a novel signaling molecule functioning in appressorium development and an effector in suppressing host immunity, our studies revealed a novel mechanism by which RGS and RGS-like proteins regulate pathogen-host interactions.

Xanthomonas oryzae pv. oryzae XopQ protein suppresses rice immune responses through interaction with two 14‐3‐3 proteins but its phospho‐null mutant induces rice immune responses and interacts with another 14‐3‐3 protein

Article

Full-text available

May 2019
MOL PLANT PATHOL

Many bacterial phytopathogens employ effectors secreted through the type‐III secretion system to suppress plant innate immune responses. The Xanthomonas type‐III secreted non‐TAL effector protein Xanthomonas outer protein Q (XopQ) exhibits homology to nucleoside hydrolases. Previous work indicated that mutations which affect the biochemical activity of XopQ fail to affect its ability to suppress rice innate immune responses, suggesting that the effector might be acting through some other pathway or mechanism. In this study, we show that XopQ interacts in yeast and in planta with two rice 14‐3‐3 proteins, Gf14f and Gf14g. A serine to alanine mutation (S65A) of a 14‐3‐3 interaction motif in XopQ abolishes the ability of XopQ to interact with the two 14‐3‐3 proteins and to suppress innate immunity. Surprisingly, the S65A mutant gains the ability to interact with a third 14‐3‐3 protein that is a negative regulator of innate immunity. The XopQS65A mutant is an inducer of rice immune responses and this property is dominant over the wild‐type function of XopQ. Taken together, these results suggest that XopQ targets the rice 14‐3‐3 mediated immune response pathway and that its differential phosphorylation might enable interaction with alternative 14‐3‐3 proteins.

A bacterial F‐box effector suppresses SAR immunity through mediating the proteasomal degradation of OsTrxh2 in rice

Article

Sep 2020

Plant bacterial pathogens usually cause diseases by secreting and translocating numerous virulence effectors into host cells and suppressing various host immunity pathways. The widespread ubiquitin systems in host cells have been demonstrated to be interfered or hijacked frequently by numerous pathogenic bacteria with various strategies. Some T3SS effectors of plant pathogens have been demonstrated to impersonate the F‐box protein (FBP) component of SKP1/CUL1/F‐box (SCF) E3 ubiquitin system for their own benefit. And numerous putative eukaryotic‐like F‐box effectors have been screened in different bacterial pathogens by bioinformatics analyses, but the targets of most F‐box effectors in the host immunity remain unknown. Here, we show that XopI, a putative F‐box effector of African Xoo (X. oryzae pv. oryzae) strain BAI3, strongly inhibits host’s OsNPR1‐dependent resistance to Xoo. The xopI knockout mutant displays lower virulence to rice than BAI3. Mechanistically, we identify a trithorax‐like protein, OsTrxh2, as an XopI‐interacting protein in rice. While OsTrxh2 positively regulates the rice immunity by catalyzing the dissociation of OsNPR1 into monomers in rice. The XopI effector serves as a F‐box adapter to form an OSK1‐XopI‐OsTrxh2 interaction complex, and it further disrupts OsNPR1‐mediated resistance through proteasomal degradation of OsTrxh2. Our results indicate that XopI targets OsTrxh2 and further represses OsNPR1‐dependent signaling, thereby subverting rice SAR (systemic acquired resistance) immunity.

Interaction of the Xanthomonas effectors XopQ and XopX results in induction of rice immune responses

Article

Jul 2020

Xanthomonas oryzae pv. oryzae uses several type III secretion system (T3SS) secreted effectors, namely XopN, XopQ, XopX, and XopZ, to suppress rice immune responses that are induced following treatment with cell wall degrading enzymes. Here we show that a T3SS secreted effector XopX interacts with two of the eight rice 14‐3‐3 proteins. Mutants of XopX that are defective in 14‐3‐3 binding are also defective in suppression of immune responses, suggesting that interaction with 14‐3‐3 proteins is required for suppression of host innate immunity. However, Agrobacterium mediated delivery of both XopQ and XopX into rice cells results in induction of rice immune responses. These immune responses are not observed when either protein is individually delivered into rice cells. XopQ‐ XopX induced rice immune responses are not observed with a XopX mutant that is defective in 14‐3‐3 binding. Yeast two‐ hybrid, BiFC and co‐ IP assays indicate that XopQ and XopX interact with each other. A screen for Xanthomonas effectors which can suppress XopQ‐ XopX induced rice immune responses, led to the identification of five effectors, namely XopU, XopV, XopP, XopG and AvrBs2, that could individually suppress these immune responses. These results suggest a complex interplay of Xanthomonas T3SS effectors in suppression of both pathogen triggered immunity and effector triggered immunity to promote virulence on rice.

Arms and ammunitions: effectors at the interface of rice and it’s pathogens and pests

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