Next Article in Journal
A Dpagt1 Missense Variant Causes Degenerative Retinopathy without Myasthenic Syndrome in Mice
Next Article in Special Issue
Genome-Wide Identification of Auxin-Responsive GH3 Gene Family in Saccharum and the Expression of ScGH3-1 in Stress Response
Previous Article in Journal
Saposin C, Key Regulator in the Alpha-Synuclein Degradation Mediated by Lysosome
 
 
Search for Articles:
Title / Keyword
Author / Affiliation / Email
Journal
Article Type
 
 
Advanced Search
 
Section
Special Issue
Volume
Issue
Number
Page
 
Journals
IJMS
Volume 23
Issue 19
10.3390/ijms231912003
ijms-logo
Submit to this Journal Review for this Journal Propose a Special Issue
► Article Menu

Article Menu

share Share announcement Help format_quote Cite question_answer Discuss in SciProfiles thumb_up
...
Endorse textsms
...
Comment
first_page
settings
Order Article Reprints
Font Type:
Arial Georgia Verdana
Font Size:
Aa Aa Aa
Line Spacing:
Column Width:
Background:
Review

Advances in Fungal Elicitor-Triggered Plant Immunity

by
Jia Guo
and
Yulin Cheng
*
Key Laboratory of Plant Hormones and Development Regulation of Chongqing, School of Life Sciences, Chongqing University, Chongqing 401331, China
*
Author to whom correspondence should be addressed.
Int. J. Mol. Sci. 2022, 23(19), 12003; https://doi.org/10.3390/ijms231912003
Submission received: 15 September 2022 / Revised: 6 October 2022 / Accepted: 8 October 2022 / Published: 9 October 2022
(This article belongs to the Special Issue Crop Stress Biology and Molecular Breeding 2.0)
Browse Figures
Versions Notes

Abstract

:
There is an array of pathogenic fungi in the natural environment of plants, which produce some molecules including pathogen-associated molecular patterns (PAMPs) and effectors during infection. These molecules, which can be recognized by plant specific receptors to activate plant immunity, including PTI (PAMP-triggered immunity) and ETI (effector-triggered immunity), are called elicitors. Undoubtedly, identification of novel fungal elicitors and their plant receptors and comprehensive understanding about fungal elicitor-triggered plant immunity will be of great significance to effectively control plant diseases. Great progress has occurred in fungal elicitor-triggered plant immunity, especially in the signaling pathways of PTI and ETI, in recent years. Here, recent advances in fungal elicitor-triggered plant immunity are summarized and their important contribution to the enlightenment of plant disease control is also discussed.

1. Introduction

Plant diseases are a major problem affecting the yield and quality of crops, and annual losses amounted to 10.1–28.1% for wheat, 24.6–40.9% for rice, 19.5–41.1% for maize and 8.1–21% for potatoes [1]. Pathogenic fungi are the most frequent cause of plant diseases and over 8000 fungal species are capable of infecting plants [2]. In addition, some pathogenic fungi contain toxins, such as aflatoxins and fumonisins, which are harmful to human health [2]. Pathogenic fungi are a persistent threat to global food security, and the application of fungicides is still the main method to control fungal diseases worldwide [3].
Investigating the molecular mechanisms of plant-microbe interactions, mainly including pathogenicity and plant resistance, is crucial for developing novel or safer strategies for effectively controlling plant diseases [4]. For infecting plants, pathogens can produce some important virulence factors, such as cell wall-degrading enzymes, virulence-associated effector proteins and phytotoxins, to promote infection [5]. To survive from biotic stresses, plants have also evolved an extraordinary immune system over the long term by interacting with pathogens [6]. Unlike animals, plants have innate immune systems that perceive danger signals and trigger defense responses, mainly including reactive oxygen species (ROS) burst, ion flow, accumulation of phytoalexins, upregulation of immune genes, hypersensitive response (HR), and systemic acquired resistance (SAR), which play a central role in plant resistance against pathogen infection [7,8].
Elicitors are a general term for a group of substances that act on plants and improve their resistance, and they can be classified into biotic elicitors and abiotic elicitors depending on their source [9]. During pathogen infection on plants, some molecules from pathogens are perceived by plants as danger signals to activate plant immunity. These molecules belong to biotic elicitors and have great application prospects in plant disease control [10]. Pathogen-derived elicitors mainly consist of pathogen-associated molecular patterns (PAMPs) and effectors, which can be recognized by plant cell surface-localized pattern recognition receptors (PRRs) and intracellular nucleotide-binding leucine-rich repeat (NB-LRR) domain receptors (NLRs) to activate PTI (PAMP-triggered immunity) and ETI (effector-triggered immunity), respectively [6,11]. PAMPs are also called microbe-associated molecular pattern (MAMPs), and a well-known fungal PAMP is chitin, from the fungal cell wall [12]. Effectors are secreted by pathogens to enter host plants, and the effectors activating ETI are also called avirulence (AVR) proteins. In recent years, a number of fungal elicitors and their plant receptors have been identified and great progress has occurred in the signaling pathways of fungal elicitor-triggered plant immunity. Here, these recent advances in fungal elicitor-triggered plant immunity are summarized.

2. Classification of Fungal Elicitors

According to their chemical composition, known fungal elicitors can be classified into two major categories, including saccharide elicitors and protein elicitors (Figure 1; Table 1 and Table 2). Chitin and cell wall-degrading enzymes are well-known fungal elicitors, and they belong to oligosaccharide elicitors and protein elicitors, respectively.

2.1. Saccharide Elicitors

Chitin is one of the key structural components in the fungal cell wall and chitosan is the production of deacetylated chitin [13]. Despite the low content (1~2% in dry yeast cell wall, 10~20% in the cell wall of filamentous fungi), chitin is studied as a model of fungal PAMPs, and it can be recognized by specific receptors, resulting in activating downstream immune signals [14]. As a derivative of chitin, chitosan can also induce immune response-like chitin [15]. Plants do not contain chitin, but contains chitin-degrading enzymes, which can degrade the cell wall of the fungi, and the resulting products, chitin oligosaccharides and chitosan oligosaccharides, can act as elicitors to activate the plant immune system, inducing ion fluxes, increase of chitinase activity, synthesis of phytoalexins, production of ROS and expression of defense genes [16]. Receptors containing the lysin motif (LysM) located on the surface of plant cells can recognize chitin in different plants [17,18].
Glucan is a type of polysaccharide, made up of glucose linked by glycosidic bonds, and glucan fragment obtained from the hydrolysis of glucan has elicitor activity [19]. The recognition to chitin is conserved in plants while the recognition to glucan is dependent on its origin and the species of plants [14]. Glucan, with two forms including α-glucan and β-glucan, is an important structural component and the most abundant polysaccharide in cell walls of fungi [20]. Among all the β-glucan of fungal cell wall, β-1,3-glucan has the highest percentage ranging from 65 to 90 percent, which binds to β-1,6-glucan in the form of a branch [21,22,23]. Ayers et al. found that β-glucan could enhance resistance in plants as a PAMP by promoting the accumulation of phytoalexins and improving their activity against pathogen infection [24]. Researchers showed that a large number of legumes including soybean, alfalfa, bean, lupin, and pea had a specific receptor in their membrane to bind with β-1,3/-1,6-glucan heptaglucoside [25,26]. Rebaque et al. have found that mixed-linked β-1,3/1,4-glucans (the smallest structure is MLG43) induce MLG43-triggered PTI immunity in Arabidopsis, partially dependent on some known plant PRRs, including CERK1, LYK4 and LYK5 [27]. During the interaction between plants and β-glucan, immune responses such as ROS production, MAPKs activation, and defensive gene expression can be observed [27].

2.2. Protein Elicitors

Compared to saccharide elicitors, protein elicitors appear to be relatively diverse and mainly include cell wall-related enzymes (CWDEs), NEP1-like proteins (NLPs), harpins, glycoprotein elicitors, GPI-anchored proteins, secreted proteins of unknown function, and AVR proteins (Figure 1; Table 1 and Table 2).

2.2.1. Cell Wall-Related Enzymes

Pathogens secrete cell wall-related enzymes, most of which are cell wall-degrading enzymes (CWDEs), to degrade important components of plant cell walls in order to draw nutrients from plants or maintain the integrity of fungal pathogens [28,29]. Fungal cell wall-related enzymes may be recognized by plants as elicitors, enhancing plant resistance to pathogenic fungi, and they mainly include the glycoside hydrolase (GH), carbohydrate esterase (CE) and polysaccharide lyase (PL) families. GHs-elicitors were identified in many plant pathogenic fungi, such as Botrytis cinerea, Colletotrichum lindemuthianum, Fusarium graminearum, Rhizoctonia solani, and Verticillium dahlia [30]. EIX (ethylene-inducing xylanase), identified in the nonpathogenic fungus Trichoderma viride originally, with β-1-4-endoglucanase activity, is an important class of elicitor in the GH11 family [31], and EIX-induced PTI immunity is not dependent on its enzymatic activity but the receptors LeEIX1 and LeEIX2 [32]. EIX homologues were isolated from plant pathogenic fungi, including B. cinerea, F. graminearum and V. dahliae, and FGSG_03624 from F. graminearum, BcXyn11A from B. cinerea, and VdEIX3, from V. dahliae also have the ability to trigger PTI immune responses and plant resistance to fungal infection [33,34,35,36]. In addition to GH11, other CWDEs-related GHs, including GH10, GH12, GH28, and GH45, have been proven to be fungal elicitors [37,38]. In addition to these CWDEs-related GHs, other fungal GHs have been proven to be fungal elicitors [39,40,41]. B. cinerea BcCrh1, a GH16 transglycosylase which catalyzes crosslinking of chitin and glucan polymers in fungal cell walls, has been proven to be an atypical fungal elicitor that functions in plant cytoplasm, and Arabidopsis thaliana expressing BcCrh1 significantly increased resistance to B. cinerea [39].
Compared with GHs, CEs and PLs are relatively rarely reported to show elicitor activity [38]. SsCut1 and VdCUT11, two protein elicitors belonging to the CE family, were isolated from Sclerotinia sclerotiorum and V. dahlia, respectively [42,43]. SsCut1-treated plants showed induced expression of defense genes and significantly enhanced plant resistance to S. sclerotiorum and Phytophthora sojae [42]. Purified VdCUT11 induced cell death and triggered immune responses in N. benthamiana, cotton and tomato [43]. In addition, VdPEL1, belonging to the PL family, was identified in V. dahlia and purified VdPEL1 increased plant resistance to B. cinerea and V. dahlia [44].

2.2.2. NEP1-like Proteins (NLPs)

Necrosis- and ethylene-inducing peptide 1 (Nep1)-like proteins (NLPs) with approximately 25k-Da, are firstly separated from culture filtrates of F. oxysporum, and are proven to be widely distributed in pathogenic fungi, such as B. cinerea, B. elliptica, C. higginsianum, V. dahliae and Magnaporthe oryzae [45,46]. Most NLPs contain the conserved peptide nlp20, which is therefore recognized by the PRR RLP23 and triggers the plant PTI immune responses [47,48]. Further research revealed that cytotoxic NLPs are able to bind to glycosyl inositol phosphoryl ceramide (GIPC) sphingolipids in plasma membranes of dicot plants, leading to tissue necrosis, then activating the defense response by promoting the accumulation of 1-aminocy clopropane-1-carboxylic acid synthase (ASC) and 1-aminocy clopropane-1-carboxylic acid oxidase (ACO) in plant cells [49].

2.2.3. Harpin Proteins

Harpin proteins are heat stable, cysteine-free and glycine-rich proteins, and they can enhance plant resistance by eliciting a variety of immune responses such as HR, ROS bursts and ion fluxes [50]. Some harpin protein elicitors, such as Hrip1, MoHrip1 and MoHrip2, have been identified in Alternaria tenuissima and M. oryzae [51,52,53]. It has been demonstrated that Hrip1 from necrotrophic fungus A. tenuissima is able to induce cell death, pathogenesis-related (PR) genes expression, and (SAR) in tobacco [51]. Miao et al. showed that Hrip1 enhanced Arabidopsis resistance mainly by regulating the biosynthesis of defense related-jasmonic acid (JA) [54]. Both MoHrip1 and MoHrip2 from M. oryzae can induce cell death and defense responses, MoHrip1 regulated the levels of SA and GA in plants, and MoHrip2 induced the production of hydrogen peroxide and nitric oxide (NO) [52,53].

2.2.4. Glycoprotein Elicitors

Glycoprotein elicitors including Elicitor1, Elicitor2, and Elicitor3 have been isolated from Colletotrichum lagenarium, and the chitinase activity of watermelon leaves can be increased upon the treatment of these elicitors [55]. Furthermore, glycoprotein elicitors can enhance resistance by inducing HR and lipid peroxidation. The treatment of specific glycoprotein elicitor GP66 from M. oryzae induced antioxidant activity and HR reaction [56]. Yang et al. purified a glycoprotein elicitor from A. tenuissima, and they found that it was able to enhance the resistance against tobacco mosaic virus in tobacco [57]. Glycoprotein elicitors can be divided into two types depending on the functional domain, one of which functions by sugar residue while the other utilizes amino acid residues [58], and the molecular mechanisms of glycoprotein elicitor-triggered immunity remain to be investigated.

2.2.5. GPI-Anchored Proteins

Glycosylphosphatidylinositol (GPI) anchoring is one of the conserved post-translational modifications in eukaryotes, and GPI-anchored proteins are transported to the extracellular leaflet of the plasma membrane and cell wall [59,60]. Some studies have shown that GPI-anchored proteins from fungal plant pathogens, such as Colletotrichum graminicola and M. oryzae, are essential for fungal cell wall integrity and fungal pathogenicity [61,62]. A recent study showed that a Ser-Thr-rich GPI-anchored protein (SGP1) from Ustilaginoidea virens, the causal agent of rice false smut, is required for U. virens pathogenicity and is also a fungal PAMP triggering PTI immunity [63]. SGP1 is widely distributed among fungi and its homologues from many fungi can also trigger PTI immune responses [63]. Moreover, SGP1 treatment in N. benthamiana and rice significantly improved plant resistance to multiple fungal and bacterial pathogens [63], indicating good prospects of SGP1 elicitor in plant disease control.

2.2.6. Secreted Proteins of Unknown Function

Some secreted proteins of unknown function from fungal plant pathogens are also proven to be elicitors triggering PTI immunity [64,65,66]. The fungal elicitor RcCDI1 identified in Rhynchosporium commune, whose homologues are found in a variety of fungi including Zymoseptoria tritici, M. oryzae and Neurospora crassa, can induce cell death in solanaceae [64]. Unlike the usual plant cell death, which is normally inhibited by the effector proteins AVR3a and PexRD2, cell death induced by RcCDI1 is not inhibited by these effector proteins, indicating RcCDI1-triggered immunity may be a novel immune pathway [64]. Furthermore, whether RcCDI1 induces other immune responses such as ROS and ethylene accumulation remains to be investigated. The Valsa mali elicitor VmE02, which has homologues in a lot of fungi, induces cell death, accumulation of ROS, callose deposition, activation of salicylic acid (SA) and JA-induced immune responses, and this process is dependent on some known components of the PTI signaling pathway, such as BAK1, SOBIR1, HSP90, and STG1 [65]. However, not all homologues of VmE02 can induce plant cell death, possibly due to the lack of a PRR recognition region or the diversity of protein sequences [65]. Further research revealed that the protein elicitor VmE02 is recognized by the PRR RE02 in N. benthamiana, and RE02-silenced plants show reduced resistance to fungal infection [67].

2.2.7. Avirulence (AVR) Proteins

Unlike the above elicitors, AVR proteins usually interact with receptor proteins inside the plant cells and induce ETI responses [68]. The fungal AVR gene was first cloned in 1991 [69], and AVR proteins were identified in many plant pathogenic fungi, such as Cladosporium fulvum, Puccinia graminis f. sp. tritici, Leptosphaeria maculans, M. oryzae, Blumeria graminis f. sp. hordei, Melampsora lini, Albugo candida, and Fusarium oxysporum f. sp. lycopersici (Table 2) [70]. AVR proteins are recognized by resistance (R) proteins in plants and induce a series of immune responses such as intracellular ROS production and ion leakage, causing HR and SAR [70]. The identification of novel AVR proteins and their corresponding receptors (R proteins) is of great significance to plant disease control [70]. Two research studies published in Science in 2017 successfully cloned two important AVR genes (AvrSr50 and AvrSr35) from P. graminis f. sp. tritici, the causal agents of wheat stem rust, and found that they activate wheat’s ETI immune responses by binding to wheat receptors (R proteins) Sr50 and Sr35, respectively [71,72], which provides significant insights into the control of wheat stem rust.
Table
Table 1. Summary of important fungal elicitors which trigger plant PTI immunity.
Table 1. Summary of important fungal elicitors which trigger plant PTI immunity.
TypeOriginElicitor NameReceptorReceptor TypeCo-ReceptorRef.
Saccharidefungi cell wallchitin/chitosanOsCEBiP,
LYK5		LysM-RLP, LysM-RLKOsCERK1,
CERK1		[73,74,75,76]
β-Glucan---[27]
GH11Trichoderma virideTvEIXLeEIX2LRR-RLPBAK1[31,32,77]
Botrytis cinereaBcXyn11A---[34]
Fusarium graminearumFGSG_03624---[35]
Verticillium dahliaeVdEIX3NbEIX2LRR-RLP-[36]
GH10Rhizoctonia solaniRSAG8_07159,
FGSG_11487		---[78]
GH12B. cinereaBcXYG1---[79]
F. oysporumFoEG1---[80]
V. dahliaeVdEG1---[81]
VdEG3---
GH16B. cinereaBcCrh1---[39]
GH18Magnaporthe oryzaMoChia1/MoChiOsTPR1Tetratricopeptide repeat protein-[40]
MoChi/MoChia1OsMBL1Jacalin-related mannose-binding lectin-[41]
GH28B. cinereaBcPG1 to BcPG4, BcPG6RLP42/RBPG1LRR-RLP-[82]
GH45R. solaniEG1---[83]
CESclerotinia sclerotiorumSsCut1---[42]
V. dahliaeVdCUT11---[43]
PLV. dahliaeVdPEL1---[44]
NLPB. cinereaBcNEP1, BcNEP2RLP23LRR-RLP-[84,85]
HarpinAlternaria tenuissimaHrip1---[51]
M. oryzaeMoHrip1, MoHrip2---[52,53]
GlycoproteinM. oryzaeGP66---[56]
GPI-anchored proteinUstilaginoidea virensSGP1---[63]
Secreted protein of unknown functionRhynchosporium communeRcCDI1---[64]
Valsa maliVmE02RE02LRR-RLP-[67]
F. graminearumFg02685---[66]
Table
Table 2. Summary of known fungal AVR proteins whose corresponding receptors have been identified.
Table 2. Summary of known fungal AVR proteins whose corresponding receptors have been identified.
AVRReceptorRef.
SpeciesNameSpeciesNameType
Albugo candidaCCG28, CCG30, CCG33, CCG40, CCG67, CCG71, CCG79 and CCG104ArabidopsisWRR4ATNL[86]
CCG45, CCG57, CCG61 and CCG70ArabidopsisWRR4BTNL
Blumeria graminis f. sp. hordeiAVRa1, AVRa6, AVRa7, AVRa9, AVRa10, AVRa13 and AVRa22barleyMLA1, MLA6, MLA7, MLA9, MLA10, MLA13 and MLA22CNL[87,88,89]
B. graminis f. sp. tritici (Bgt), B. graminis f. sp. Secalis, and B. graminis f. sp. TriticaleAvrPm2, BgsE-5845 and BgtriticaleE-5845wheatPm2CNL[90]
BgtAvrPm3A2/F2, AVRPM3B2/C2 and AVRPM3D3wheatPM3A, PM3F, PM3B, PM3C and PM3DCNL[91,92]
AvrPm17ryePm17CNL[93]
Cladosporium fulvumapoplastic effectors, including Avr2, Avr4, Avr4E and Avr9tomatoCf-2, Cf-4, Hcr9-4E and Cf-9PRR[94,95,96,97,98]
Fusarium oxysporum f. sp. lycopersiciFoAvr2tomatoI2CNL[99]
F. oxysporum f. sp. melonisAvrFom2melonFom-2CNL[100]
Leptosphaeria maculansapoplastic AvrLm1oilseed rapeLepR3PRR[101]
Magnaporthe oryzaeAvrPi9, Avr-Pi54, AvrPib, Avr-Pik, Avr-Pita and AvrPiz-tricePi9, Pi54, Pib, Pik, Pi-ta and Piz-tCNL[102,103,104,105,106,107]
Avr-Pia and Avr1-CO39ricePia-2/RGA5CNL[108]
AvrPiiricePi5-1, Pi5-2, Pii-1 and Pii-2CNL[109]
Melampsora liniAvrL2-A, AvrM, AvrP and AvrP123flaxL2, M, P and P2TNL[110,111]
AvrL567 effectorsflaxL5, L6 and L7TNL[112]
Puccinia graminis f. sp. triticiAvrSr27 and AvrSr35wheatSr27 and Sr35CNL[72]
AvrSr50ryeSr50CNL[71]
P. polysoraAvrRppCmaizeRppCCNL[113]
AvrRppKmaizeRppKCNL[114]

3. The Receptors of Fungal Elicitors

3.1. Types of Receptors

The immune response induced by elicitors in plant species is dependent on the corresponding receptors on the cell membrane or within the cell. These receptors mainly contain the cell surface-localized pattern recognition receptors (PRRs) and intracellular nucleotide-binding leucine-rich repeat (NB-LRR) domain receptors (NLRs) [6,115].

3.1.1. PRRs

As the key component of PTI signaling pathways, PRRs participate in the recognition of PAMPs, resulting in triggering PTI immune responses in plants [12]. PRRs are mainly divided into receptor-like protein kinases (RLKs) and receptor-like proteins (RLPs), and RLKs are comprised of a transmembrane helix, an extracellular domain, and a cytosolic kinase domain, while RLPs contain a short cytosolic tail instead of the cytosolic kinase domain [12]. The corresponding PRRs of some fungal elicitors have been identified mainly by virus-induced gene silencing (VIGS), microscale thermophoresis (MST) assay and co-immunoprecipitation (Co-IP), and these identified PRRs mainly belong to RLPs with leucine-rich repeat (LRR) ectodomains (LRR-RLPs) (Table 1). Interestingly, one chitinase elicitor MoChi/MoChia1 has been reported to induce PTI immune responses by interacting with two other membrane proteins, including tetratricopeptide repeat protein (TPR) and jacalin related mannose-binding lectin (MBL), instead of typical PRRs [40,41]. Unlike typical elicitors, MoChi/MoChia1 competed with OsMBL1 or OsTPR1 for chitin binding, thereby re-establishing the chitin-triggered immune response [40,41].
During PTI signaling pathways, PRRs usually require the involvement of co-receptors [116]. The somatic embryogenesis receptor kinase (SERK) family has been proven to act as co-receptors of PRRs, especially RLK-type PRRs [116]. BRI1-associated receptor kinase 1 (BAK1) is a well-known co-receptor of PRRs recognizing bacterial PAMPs, and it is also a co-receptor of LeEIX1 recognizing fungal EIX [77]. VIGS assay in N. benthamiana showed that BAK1 is also involved in PTI immune responses mediated by many other fungal elicitors [67,80,84,85], but whether BAK1 is a co-receptor of PRRs recognizing these fungal elicitors remains to be investigated. Chitin is the most studied fungal PAMP, and the rice chitin elicitor-binding protein (OsCEBiP) has been proven to be a significant chitin receptor in rice [75,76]. As OsCEBiP belongs to be RLPs and does not have intracellular domains, rice chitin elicitor receptor kinase 1 (OsCERK1), which is a lysin motif (LysM)-containing RLK, is proven to be a co-receptor of OsCEBiP for recognizing fungal chitin [18]. In Arabidopsis, the homolog of OsCEBiP, LYM2, was identified, but it did not induce immune responses [117]. Arabidopsis recognizes chitin to induce immune responses mainly lysin motif receptor kinase 5 (LYK5), and CERK1, which was able to phosphorylate LYK5 and triggered LYK5 internalization upon chitin treatment, is a co-receptor for LYK5 in Arabidopsis [73,74]. These results highlight the difference of PTI signaling pathways in different plants.
In addition to being the receptors of pathogen PAMPs, PRRs can be recognized by apoplastic effectors to induce ETI immunity [118]. Tomato cf-9, which belongs to RLP-type PRR, was the first identified plant PRR in 1994 and recognizes the apoplastic effector Avr9 from Cladosporium fulvum [118]. Other plant PRRs, including Cf-4, Hcr9-4E and Cf-9 in tomato and LepR3 in oilseed rape, have been also proven to recognize fungal apoplastic effectors (AVR proteins) (Table 2).

3.1.2. NLRs

NLRs, which evolved from a common ancestral prokaryotic adenosine triphosphatase, belong to the key and conserved components between plant intracellular innate immune systems and animal intracellular innate immune systems and mediate plant ETI immunity [119]. As the prominent intracellular immune receptors and R proteins, NLRs can be divided into three major classes, including the helical coiled-coil NLRs (CNLs), RPW8-L-like coiled-coil domain NLRs (RNLs) and Toll/interlecukin-1 receptor/resistance protein NLRs (TNLs) based on their variable N-terminal domains [119,120]. Based on the role of NLRs in plant ETI immunity, NLRs can also divided into sensor NLRs, which are involved in the recognition of intracellular effectors and helper NLRs, which do not regulate effectors but act as helpers or co-receptors to transduce immune signals from sensor NLRs [119,120]. RPS2 in Arabidopsis, which regulate effectors AvrRpm1 and AvrRpt2 from Pseudomonas syringae, and N in tobacco, which regulates effector p50 from tobacco mosaic virus (TMV), were the first identified NLRs in 1994 [118]. To date, numerous sensor NLRs recognizing fungal effectors have been identified in different plants and most of these NLRs belong to the CNL class (Table 2). Unlike PRRs, which mostly regulate specific PAMPs in a one-to-one way, NLRs recognize AVR proteins in one-to-one, many-to-one, or one-to-many ways [118]. The Arabidopsis WRR4A or WRR4B can regulate multiple effectors from Albugo candida [86], and wheat Pm2 can even regulate multiple effectors from different fungal pathogens [90]. In contrast, the effector AvrPii from M. oryzae can also be regulated by multiple rice NLRs [109]. Despite the great progress in the identification of NLRs that regulate fungal AVR proteins (Table 2), cloning of NLR genes remains challenging in some agricultural, horticultural and forestry crops, mainly due to their complex genomes and long growth cycles.

3.2. The Important Role of Immune Receptors Recognizing Fungal Elicitors in Disease Resistance Breeding

The breeding of disease-resistant cultivars is the most effective and economical method for plant disease control, and plant immune receptors directly or indirectly recognizing pathogen elicitors, mainly including PRRs and NLRs, have been proven to be key gene resources of disease-resistance breeding [121,122]. Traditional breeding or genetic engineering breeding can mediate the transfer of immune receptors from resistant plants to susceptible plants, thus conferring disease resistance in susceptible plants [122]. Transgenic overexpression of wheat NLRs, such as PM3A, PM3F, PM3B and PM3C, significantly increased wheat resistance to powdery mildew in the field [123]. In addition, transgenic expression of the barley MLA1, a NLR recognizing powdery mildew AVRa1, and tomato VE1, a RLP-type PRR recognizing apoplastic effector from V. dahlia, can induce Arabidopsis disease resistance [87,124], suggesting interfamily transfer of immune receptors mediated by genetic engineering breeding is a promising method for disease-resistance breeding.
Plants are faced with the harm of many pathogens during growth and thus exploiting broad-spectrum disease resistance, which confers plant resistance against more than one pathogen species or against most races or strains of the same species, is a major goal of plant breeding [125]. Although most PRRs regulate specific PAMPs in the one-to-one way, a few plant PRRS have been proven to sense different elicitors from fungi, oomycetes or bacteria [118]. Transgenic overexpression of rice LYP4 and LYP6, which are dual functional PRRs sensing both bacterial peptidoglycan and fungal chitin, conferred rice resistance to both bacterial and fungal diseases [126], and the ectopic expression of Arabidopsis RLP23, a PRR recognizing different NLR proteins from fungi and oomycetes, in potato induced resistance to both fungal and oomycete diseases [48]. One NLR usually confers plant resistance to one or some pathogen strains which contain corresponding AVR proteins but pyramiding multiple NLRs can confer broad-spectrum disease resistance [125]. By introducing a transgene cassette of five resistance (NLR) genes into wheat, transgenic wheat showed broad-spectrum resistance to the notorious phytopathogenic fungus P. graminis f. sp. tritici [127]. Recently, transgenic rice carrying a designer rice NLR receptor RGA5HMA2 conferred resistance to M. oryzae carrying noncorresponding AVR proteins, indicating that introducing engineered NLR receptors can also be used in plant breeding for broad-spectrum disease resistance [128]. In addition to these receptors directly recognizing pathogen elicitors and functioning as positive regulatory factors of plant immunity, some receptor kinases, including BIR (BAK1-interacting receptor-like kinase) and FER (FERONIA), were proven to negatively regulate PRR signaling mainly limiting the formation of BAK1-receptor complex [118]. A recent study showed that genome editing mediated the inactivation of wheat receptor-like cytoplasmic kinase, TaPsIPK1, and conferred broad-spectrum resistance to stripe rust fungus P. striiformis f. sp. tritici without impacting important agronomic traits [129]. BAK1 is proven to be the co-receptor of some fungal elicitors or involved in PTI immunity-triggered by many fungal elicitors [67,77,80,84,85], and thus genome editing of these receptor kinases (BIR and FER) functioning as negative regulatory factors of plant PTI immunity may also be an important method for exploiting broad-spectrum disease resistance.

4. Signaling Pathways of Fungal Elicitor-Triggered Plant Immunity

Upon the recognition between pathogen elicitors and plant receptors, these plant receptors, including PRRs and NLRs, will be activated, and then the signal cascades will be transduced in plant cells to trigger a series of PTI or ETI defense responses, which protect the plant from pathogen infection [130,131]. Noticeably, great progress has occurred in the signaling pathways of fungal PAMPs-triggered PTI and fungal effector-triggered ETI (Figure 2).

4.1. Fungal PAMPs-Triggered PTI

As the first line of innate immunity in plants, PTI immunity effectively controls the colonization of many pathogenic fungi [132]. The PRR complex plays a role in recognition with elicitors and signal transduction of PTI immunity [133], but receptors of most identified fungal elicitors remain unknown (Table 1). As one of the key structural components in the fungal cell wall, chitin is the most studied fungal PAMP, and great progress has occurred in the signaling pathways of chitin-triggered PTI (Figure 2). In Arabidopsis, the two LysM receptor-like kinases (LYKs), including LYK5 and CERK1, are thought to be the major chitin receptors, with LYK5 being phosphorylated by CERK1 and thus entering cells to induce downstream immune responses [73,74]. In addition, in vitro experiments have demonstrated that another LYK, LYK4, can interact with LYK5 to enhance the chitin-induced immune responses and improve plant resistance to fungi [134]. In contrast, two other LYKs, LYK2 and LYK3, are not to be involved in and negatively regulate the chitin-induced immune responses, respectively [135]. LIK1, an LRR-RLK, was also proven to be phosphorylated by CERK1 [136]. Unusually, the interaction between LIK1 and CERK1 inhibits CERK1 recognition of chitin and negatively regulates chitin-induced immune responses in Arabidopsis [136].
The receptor-like cytoplasmic kinases (RLCK), with no extracellular domain and no transmembrane helix, but only the cytosolic kinase domain, also has an important role in triggering PTI immune responses [137]. Typically, RLCKs are phosphorylated by PRRs, which in turn activate their immune functions that induce downstream immune signals [133]. In Arabidopsis, recognition of fungal chitin can activate a variety of RLCKs that induce PTI signals, including ROS burst, stomatal closure, callose deposition, MAPK cascades activation and defense genes expression. Ion flow is also one of the important signals of PTI, and GNGC has an important role in chitin-mediated calcium entry, and the study indicated a reduction in Ca2+ spikes in the GNGC mutant [138]. BOTRYTIS-INDUCED KINASE 1 (BIK1), an important RLCK, plays an important role in chitin-induced ROS production. The BIK1 phosphorylated by CERK1 has been reported to directly phosphorylate NADPH oxidase, the respiratory burst ortholog D (RBOHD), leading to ROS production [139]. Several phosphorylation sites have been identified on RBOHD to date, including the S347 site which can be phosphorylated in chitin-induced PTI [139]. RLCK VII-1, RLCK VII-4, RLCK VII-5 and RLCK VII-7 were also suggested to have the ability to induce ROS production [140]. ROS production induced by chitin was significantly higher in the WT than the rlck vii-1, rlck vii-4, rlck vii-5 and rlck vii-7 mutants [140]. RLCK VII-1 and RLCK VII-4 were specifically required for chitin-triggered PTI, whereas RLCK VII-5 and RLCK VII-7 are essential components of the immune pathways induced by a variety of PRRs [140]. ROS production is considered to be the starting signal of multiple immune pathways in plants, with the ability to enhance ion flow, NO production, and lead to the closure of plant stomata, which have an important role in the plant’s immune response [141,142,143]. Meanwhile, the strong scavenging system of plants ensures that ROS content in tissues will not be too high while ROS is produced at a high speed [144,145].
In addition to ROS production, activation of related RLCKs induces callose deposition. PBL1, a homolog of BIK1, was reported to be involved in chitin-induced callose synthesis, and pbl1 mutant showed a significant reduction in callose deposition [146]. Another PBL protein, PBL27, a homolog of the cytoplasmic kinase OsRLCK185, was shown to be directly phosphorylated by CERK1 and had a role in inducing callose deposition [147]. Moreover, PBL27 acts as a MAPKKK kinase to phosphorylate MAPKKK5, which in turn activates MPK3/4/6, and several phosphorylation sites including S-617, S-622, S-658, S-660, T-677, and S-685 have been identified [148]. Phosphorylation of PBL27 by CERK1 enhances the activation of the MAPK cascade [148]. In MAPKKK5 mutants, chitin-induced callose deposition is significantly reduced, and therefore PBL27-induced callose deposition may be achieved through activation of MAPKKK5 [148]. Similar to PBL27, PBL19 activates MPK3/6 by phosphorylating MAPKKK5 [149]. The difference is that its phosphorylation sites are Ser-599, Ser-682, and Ser-692, whereas PBL19 phosphorylates the Ser-599 site [149]. Additionally, MPK6 activated by PBL19 is capable of enhancing immune signals by phosphorylating both the Ser-682 and Ser-692 of MAPKKK5 [149]. This is undoubtedly a positive feedback mechanism that has an important role in achieving strong disease resistance in Arabidopsis. It has also been reported that PBL19 can activate MPK4 by phosphorylating the MAPKKK MEKK1 [149]. Activation of the MAPK cascade normally phosphorylates downstream transcription factors and promotes the expression of defense genes. The transcription factor WRKY33 has been reported to act as a substrate for MPK3/6 and is phosphorylated to positively regulate the expression of ACS2 and ACS6 genes [150]. When infected by B. cinerea, ACS2 and ACS6 in Arabidopsis are involved in ethylene synthesis and plant disease resistance [150].

4.2. Fungal Effector-Triggered ETI

To overcome this first layer of defense (PTI immunity) and infect plants successfully, pathogenic fungi have evolved to secrete effectors into plant cells to inhibit plant PTI immunity, making plants more susceptible to pathogens, which is called effector-triggered susceptibility (ETS) [151]. Plants correspondingly produce resistance (R) proteins encoded by R genes, most of which are NLRs, to recognize some specific pathogen effectors (also called AVR proteins), thus triggering plant ETI immunity [152,153]. HR is a marked feature of plant ETI immunity and the activation of HR in infected sites markedly controls the colonization of pathogenic fungi [152,153]. Some plant R proteins can directly recognize fungal AVR proteins to induce ETI immune responses. For example, AvPi-ta from M. oryzae can be directly recognized by Pi-ta in rice, interacting with the LRR domain of Pi-ta and thus activating ETI immune responses in rice [154]. However, researchers found that most plant R proteins did not actually interact directly with AVR proteins. Thus, the defense hypothesis was put forward, which suggests that R proteins recognize AVR proteins through intermediate proteins and AVR proteins attack target proteins in plants and R proteins act as monitor proteins [155,156]. For example, the effector Avr2 from C. fulvum is not directly recognized by the R protein Cf-2 but is dependent on its target protein Rcr3 [155].
TNL-type NLRs meditated plant ETI immunity is usually dependent on members of the EDS1 family, including EDS1, PAD4 and SAG101, which share similar structural domains, a N-terminal α/β-hydrolase-like domain and a C-terminal EP domain containing the α-helical [157]. EDS1 was reported to function through its EP structural domain, in which a positively charged residue can be wrapped around its homologous protein to form a dimer [157,158]. In angiosperms, the helper NLRs ADR1 and NRG1 are generally thought to interact with EDS1-PAD4 and EDS1-SAG101, respectively, and mediate SA synthesis and cell death, respectively [159,160]. It was found that the Arabidopsis R protein, RPW8, which confers plant resistance to powdery mildew, induced SA- and EDS1-dependent defense responses, resulting in HR and the induced expression of defense genes [161]. This process was also dependent on PAD4, EDS5, and NPR1, but was inhibited by the MAPKK kinase EDR1, which controls plant exposure to spontaneous HR-like lesions (SHL) [161]. AVR proteins from C. fulvum can be recognized by Cf proteins in tomato, inducing ROS accumulation, HR, activation of ion channels and MAPKs, and expression of defense genes [162,163]. Cf-4 is an LRR-RLP that is dependent on the co-receptor BAKI to function. ETI induced by Cf-4 requires EDS1, but it is not clear whether helper NLR, SAG101 or PAD4 is involved in the ETI immunity [164]. The cytosolic heat shock protein 90 (Hsp90) is involved in plant ETI immunity-triggered by C. fulvum Avr2 by stimulating MAPKs, which in turn phosphorylates ACS and transcription factors to promote PR gene expression, ethylene synthesis, and HR production [165].

4.3. Convergent Pathways between Fungal Elicitor-Triggered PTI and ETI

Arabidopsis receptor-like cytoplasmic kinase PBL19 has been proven to activate MPK4 by phosphorylating the MAPKKK MEKK1 during chitin-triggered PTI [149]. A recent study showed that PBL19 can also interact with EDS1, which is an important component of ETI upon treatment of fungal chitin, leading to the phosphorylation of EDS1 and strengthening the immune signal of plants [166]. This study suggests that EDS1 may be one of the key molecules linking PTI and ETI. In addition, Pruitt et al. also found that EDS1 and PAD4 in the ETI pathway were also involved in PTI trigged by fungal elicitor pg13, and reduction in ethylene production was observed in the pad4 and eds1 mutant compared to the wild-type response to pg13 elicitor [167]. Toll/interleukin-1 receptor (TIR) domains of NLRs were proven to be required for plant ETI immunity via their NADase activity [168,169], and a recent study showed that activation of TIR signalling is also involved in PTI immunity triggered by npl20 and other elicitors [170], which also highlights the noticeable PTI-ETI crosstalk.

5. Conclusions and Prospects

This review summarizes recent advances in fungal elicitor-triggered plant immunity, including classification of fungal elicitors, the receptors of fungal elicitors, and signaling pathways of fungal elicitor-triggered plant immunity, which provides significant insights into plant–microbe interactions and plant disease control. Identification of novel elicitors is an important research topic in plant pathology because elicitors can be directly utilized in plant disease control and usually provide long-term plant protection [171]. Although many fungal elicitors have been identified (Table 1), little is known about elicitors in post-harvest fungal diseases mainly on fruit, which causes serious economic losses every year [172,173]. Similarities and differences between uncharted fungal elicitor-triggered plant immunity on fruit and the well-known fungal elicitor-triggered plant immunity on leaves remain to be investigated. In addition, only a few plant receptors that recognize fungal elicitors, especially PAMPs, have been identified so far, which undoubtedly poses a limitation to disease-resistance breeding. Thus, methods for identifying plant receptors need to be optimized, and the recent genome-wide silencing assay in the model plant N. benthamiana [174] may be a promising method of identifying receptors.
Numerous studies have revealed the signaling pathways of PTI immunity triggered by fungal elicitors, especially the well-known fungal PAMP, chitin (Figure 2). PTI can be triggered both in the early and late stages of plant infection, whereas ETI triggering is concentrated in the late stages of infection and lasts for a longer period of time. However, the signaling pathways of fungal effector-triggered ETI have been relatively unexplored. The signaling pathways of ETI immunity triggered by bacterial effectors have been studied in detail [118,120], and whether these important components of the ETI signaling pathways triggered by bacterial effectors are involved in fungal effector-triggered ETI remains to be investigated. In addition, the crosstalk between PTI and ETI has been a hot topic in plant immunity research in recent years [118,175]. Thus, further revealing the molecular mechanisms of fungal PAMPs-triggered PTI and fungal effector-triggered ETI will uncover more convergent pathways between PTI and ETI.

Author Contributions

J.G. and Y.C. collected the literature; Y.C. and J.G. wrote the manuscript. All authors have read and agreed to the published version of the manuscript.

Funding

This study was supported by the National Key Research and Development Program of China (2018YFD1000407), the National Natural Science Foundation of China (31972123), the Fundamental Research Funds for the Central Universities (2022CDJXY-004), and the Chongqing Talents: Exceptional Young Talents Project (CQYC20190525).

Institutional Review Board Statement

Not applicable.

Informed Consent Statement

Not applicable.

Data Availability Statement

Not applicable.

Acknowledgments

We thank Zhengguo Li and Juanni Yao from Chongqing University for their comments on the earlier version of the manuscript.

Conflicts of Interest

The authors declare no conflict of interest.

References

  1. Savary, S.; Willocquet, L.; Pethybridge, S.J.; Esker, P.; McRoberts, N.; Nelson, A. The global burden of pathogens and pests on major food crops. Nat. Ecol. Evol. 2019, 3, 430–439. [Google Scholar] [CrossRef] [PubMed]
  2. Fisher, M.C.; Henk, D.A.; Briggs, C.J.; Brownstein, J.S.; Madoff, L.C.; McCraw, S.L.; Gurr, S.J. Emerging fungal threats to animal, plant and ecosystem health. Nature 2012, 484, 186–194. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  3. Fones, H.N.; Bebber, D.P.; Chaloner, T.M.; Kay, W.T.; Steinberg, G.; Gurr, S.J. Threats to global food security from emerging fungal and oomycete crop pathogens. Nat. Food 2020, 1, 332–342. [Google Scholar] [CrossRef]
  4. Mehta, A.; Brasileiro, A.C.M.; Souza, D.S.L.; Romano, E.; Campos, M.A.; Grossi-De-Sa, M.F.; Silva, M.S.; Franco, O.L.; Fragoso, R.R.; Bevitori, R.; et al. Plant-pathogen interactions: What is proteomics telling us? FEBS J. 2008, 275, 3731–3746. [Google Scholar] [CrossRef] [Green Version]
  5. Bi, K.; Liang, Y.; Mengiste, T.; Sharon, A. Killing softly: A roadmap of Botrytis cinerea pathogenicity. Trends Plant Sci. 2022. [Google Scholar] [CrossRef]
  6. Jones, J.D.G.; Dangl, J.L. The plant immune system. Nature 2006, 444, 323–329. [Google Scholar] [CrossRef] [Green Version]
  7. de Wit, P.J.G.M. How plants recognize pathogens and defend themselves. Cell. Mol. Life. Sci. 2007, 64, 2726–2732. [Google Scholar] [CrossRef]
  8. Fang, Y.; Gu, Y. Regulation of plant immunity by nuclear membrane-associated mechanisms. Front. Immunol. 2021, 12, 771065. [Google Scholar] [CrossRef]
  9. Sák, M.; Dokupilová, I.; Kaňuková, a.; Mrkvová, M.; Kraic, J. Biotic and abiotic elicitors of stilbenes production in Vitis vinifera L. cell culture. Plants 2021, 10, 490. [Google Scholar] [CrossRef]
  10. Patel, Z.M.; Mahapatra, R.; Jampala, S.S.M. Role of fungal elicitors in plant defense mechanism. Mol. Asp. Plant Benef. Microbes Agric. 2020, 143–158. [Google Scholar] [CrossRef]
  11. Sun, L.; Zhang, J. Regulatory role of receptor-like cytoplasmic kinases in early immune signaling events in plants. Fems. Microbiol. Rev. 2020, 44, 845–856. [Google Scholar] [CrossRef] [PubMed]
  12. Lee, D.H.; Lee, H.S.; Belkhadir, Y. Coding of plant immune signals by surface receptors. Curr. Opin. Plant Biol. 2021, 62, 102044. [Google Scholar] [CrossRef] [PubMed]
  13. Geoghegan, I.A.; Gurr, S.J. Investigating chitin deacetylation and chitosan hydrolysis during vegetative growth in Magnaporthe oryzae. Cell. Microbiol. 2017, 19, e12743. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  14. Fesel, P.H.; Zuccaro, A. beta-glucan: Crucial component of the fungal cell wall and elusive MAMP in plants. Fungal Genet. Biol. 2016, 90, 53–60. [Google Scholar] [CrossRef] [Green Version]
  15. Iriti, M.; Faoro, F. Chitosan as a MAMP, searching for a PRR. Plant Signal. Behav. 2009, 4, 66–68. [Google Scholar] [CrossRef] [Green Version]
  16. Pusztahelyi, T. Chitin and chitin-related compounds in plant–fungal interactions. Mycology 2018, 9, 189–201. [Google Scholar] [CrossRef]
  17. Miya, A.; Albert, P.; Shinya, T.; Desaki, Y.; Ichimura, K.; Shirasu, K.; Narusaka, Y.; Kawakami, N.; Kaku, H.; Shibuya, N. CERK1, a LysM receptor kinase, is essential for chitin elicitor signaling in Arabidopsis. Proc. Natl. Acad. Sci. USA 2007, 104, 19613–19618. [Google Scholar] [CrossRef] [Green Version]
  18. Shimizu, T.; Nakano, T.; Takamizawa, D.; Desaki, Y.; Ishii-Minami, N.; Nishizawa, Y.; Minami, E.; Okada, K.; Yamane, H.; Kaku, H.; et al. Two LysM receptor molecules, CEBiP and OsCERK1, cooperatively regulate chitin elicitor signaling in rice. Plant J. 2010, 64, 204–214. [Google Scholar] [CrossRef] [Green Version]
  19. Yamaguchi, T.; Yamada, A.; Hong, N.; Ogawa, T.; Shibuya, I.N. Differences in the recognition of glucan elicitor signals between rice and soybean: Beta-glucan fragments from the rice blast disease fungus Pyricularia oryzae that elicit phytoalexin biosynthesis in suspension-cultured rice cells. Plant Cell 2000, 12, 817–826. [Google Scholar]
  20. Sun, C. Induction Effect of Yeast Cell Wall on Resistance of Postharvest Pathogenic Fungi in Pear and Tomato Fruits and Related Mechanism. Ph.D. Thesis, Zhejiang University, Hangzhou, China, 2019. [Google Scholar]
  21. Bowman, S.M.; Free, S.J. The structure and synthesis of the fungal cell wall. BioEssays 2006, 28, 799–808. [Google Scholar] [CrossRef]
  22. Shahinian, S.; Bussey, H. β-1,6-Glucan synthesis in Saccharomyces cerevisiae. Mol. Microbiol. 2000, 35, 477–489. [Google Scholar] [CrossRef] [PubMed]
  23. Ruiz-Herrera, J.; Ortiz-Castellanos, L. Cell wall glucans of fungi. A review. Cell Surface 2019, 5, 100022. [Google Scholar] [CrossRef]
  24. Ayers, A.R.; Ebel, J.; Valent, B.; Albersheim, P. Host-pathogen interactions: X. fractionation and biological activity of an elicitor isolated from the mycelial walls of Phytophthora megasperma var. sojae. Plant Physiol. 1976, 57, 760–765. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  25. Cosio, E.G.; Feger, M.; Miller, C.J.; Antelo, L.; Ebel, J. High-affinity binding of fungal β-glucan elicitors to cell membranes of species of the plant family Fabaceae. Planta 1996, 200, 92–99. [Google Scholar] [CrossRef]
  26. Côté, F.; Roberts, K.A.; Hahn, M.G. Identification of high-affinity binding sites for the hepta-beta-glucoside elicitor in membranes of the model legumes Medicago truncatula and Lotus japonicus. Planta 2000, 211, 596–605. [Google Scholar]
  27. Rebaque, D.; Hierro, I.D.; López, G.; Bacete, L.; Vilaplana, F.; Dallabernardina, P.; Pfrengle, F.; Jordá, L.; Sánchez-Vallet, A.; Pérez, R. Cell wall-derived mixed-linked β-1,3/1,4-glucans trigger immune responses and disease resistance in plants. Plant J. 2021, 106, 601–615. [Google Scholar] [CrossRef]
  28. Rotblat, B.; Enshell-Seijffers, D.; Gershoni, J.M.; Schuster, S.; Avni, A. Identification of an essential component of the elicitation active site of the EIX protein elicitor. Plant J. 2002, 32, 1049–1055. [Google Scholar] [CrossRef] [Green Version]
  29. Yang, C.; Liu, R.; Pang, J.; Ren, B.; Zhou, H.; Wang, G.; Wang, E.; Liu, J. Poaceae-specific cell wall-derived oligosaccharides activate plant immunity via OsCERK1 during Magnaporthe oryzae infection in rice. Nat. Commun. 2021, 12, 2178. [Google Scholar] [CrossRef]
  30. Bradley, E.L.; Ökmen, B.; Doehlemann, G.; Henrissat, B.; Bradshaw, R.E.; Mesarich, C.H. Secreted glycoside hydrolase proteins as effectors and invasion patterns of plant-associated fungi and oomycetes. Front. Plant Sci. 2022, 13, 853106. [Google Scholar] [CrossRef]
  31. Fuchs, Y.; Saxena, A.; Gamble, H.R.; Anderson, J.D. Ethylene biosynthesis-inducing protein from cellulysin is an endoxylanase. Plant Physiol. 1989, 89, 138–143. [Google Scholar] [CrossRef]
  32. Enkerli, J.; Felix, G.; Boller, T. The enzymatic activity of fungal xylanase is not necessary for its elicitor activity. Plant Physiol. 1999, 121, 391–398. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  33. Sella, L.; Gazzetti, K.; Faoro, F.; Odorizzi, S.; D’Ovidio, R.; Schäfer, W.; Favaron, F. A Fusarium graminearum xylanase expressed during wheat infection is a necrotizing factor but is not essential for virulence. Plant Physiol. Bioch. 2013, 64, 1–10. [Google Scholar] [CrossRef] [PubMed]
  34. Frías, M.; González, M.; González, C.; Brito, N. A 25-residue peptide from Botrytis cinerea xylanase bcxyn11a elicits plant defenses. Front. Plant Sci. 2019, 10, 474. [Google Scholar] [CrossRef] [PubMed]
  35. Tundo, S.; Paccanaro, M.C.; Bigini, V.; Savatin, D.V.; Faoro, F.; Favaron, F.; Sella, L. The Fusarium graminearum FGSG_03624 xylanase enhances plant immunity and increases resistance against bacterial and fungal pathogens. Int. J. Mol. Sci. 2021, 22, 10811. [Google Scholar] [CrossRef]
  36. Yin, Z.; Wang, N.; Pi, L.; Li, L.; Duan, W.; Wang, X.; Dou, D. Nicotiana benthamiana LRR-RLP NbEIX2 mediates the perception of an EIX-like protein from Verticillium dahliae. J. Integr. Plant Biol. 2021, 63, 949–960. [Google Scholar] [CrossRef]
  37. Rafiei, V.; Vélëz, H.; Tzelepis, G. The role of glycoside hydrolases in phytopathogenic fungi and oomycetes virulence. Int. J. Mol. Sci. 2021, 22, 9359. [Google Scholar] [CrossRef]
  38. Li, Y.; Han, Y.-J.; Qu, M.-Y.; Chen, J.; Chen, X.-F.; Geng, X.-Q.; Wang, Z.-H.; Chen, S.-B. Apoplastic cell death-inducing proteins of filamentous plant pathogens: Roles in plant-pathogen interactions. Front. Genet. 2020, 11, 661. [Google Scholar] [CrossRef]
  39. Bi, K.; Scalschi, L.; Jaiswal, N.; Mengiste, T.; Fried, R.; Sanz, A.B.; Arroyo, J.; Zhu, W.; Masrati, G.; Sharon, A. The Botrytis cinerea Crh1 transglycosylase is a cytoplasmic effector triggering plant cell death and defense response. Nat. Commun. 2021, 12, 2166. [Google Scholar] [CrossRef]
  40. Yang, C.; Yu, Y.; Huang, J.; Meng, F.; Pang, J.; Zhao, Q.; Islam, M.A.; Xu, N.; Tian, Y.; Liu, J. Binding of the Magnaporthe oryzae chitinase MoChia1 by a rice tetratricopeptide repeat protein allows free chitin to trigger immune responses. Plant Cell 2019, 31, 172–188. [Google Scholar] [CrossRef] [Green Version]
  41. Han, Y.; Song, L.; Peng, C.; Liu, X.; Liu, L.; Zhang, Y.; Wang, W.; Zhou, J.; Wang, S.; Ebbole, D.; et al. A Magnaporthe chitinase interacts with a rice jacalin-related lectin to promote host colonization. Plant Physiol. 2019, 179, 1416–1430. [Google Scholar] [CrossRef] [Green Version]
  42. Zhang, H.; Wu, Q.; Cao, S.; Zhao, T.; Chen, L.; Zhuang, P.; Zhou, X.; Gao, Z. A novel protein elicitor (SsCut) from Sclerotinia sclerotiorum induces multiple defense responses in plants. Plant Mol. Biol. 2014, 86, 495–511. [Google Scholar] [CrossRef] [PubMed]
  43. Gui, Y.-J.; Zhang, W.-Q.; Zhang, D.-D.; Zhou, L.; Short, D.P.G.; Wang, J.; Ma, X.-F.; Li, T.-G.; Kong, Z.-Q.; Wang, B.-L.; et al. A Verticillium dahliae extracellular cutinase modulates plant immune responses. Mol. Plant Microbe Interact. 2017, 31, 260–273. [Google Scholar] [CrossRef] [PubMed]
  44. Yang, Y.; Zhang, Y.; Li, B.; Yang, X.; Dong, Y.; Qiu, D. A Verticillium dahliae pectate lyase induces plant immune responses and contributes to virulence. Front. Plant Sci. 2018, 9, 1271. [Google Scholar] [CrossRef] [Green Version]
  45. Van den Ackerveken, G. How plants differ in toxin-sensitivity. Science 2017, 358, 1383–1384. [Google Scholar] [CrossRef] [PubMed]
  46. Seidl, M.F.; Ackerveken, G. Activity and phylogenetics of the broadly occurring family of microbial Nep1-Like proteins. Annu. Rev. Phytopathol. 2019, 57, 367–386. [Google Scholar] [CrossRef] [PubMed]
  47. Böhm, H.; Albert, I.; Oome, S.; Raaymakers, T.M.; Van den Ackerveken, G.; Nürnberger, T. A conserved peptide pattern from a widespread microbial virulence factor triggers pattern-induced immunity in Arabidopsis. PloS Pathog. 2014, 10, e1004491. [Google Scholar] [CrossRef] [Green Version]
  48. Albert, I.; Bohm, H.; Albert, M.; Feiler, C.E.; Imkampe, J.; Wallmeroth, N.; Brancato, C.; Raaymakers, T.M.; Oome, S.; Zhang, H.; et al. An RLP23-SOBIR1-BAK1 complex mediates NLP-triggered immunity. Nat. Plants 2015, 1, 15140. [Google Scholar] [CrossRef]
  49. Lenarcic, T.; Pirc, K.; Hodnik, V.; Albert, I.; Borisek, J.; Magistrato, A.; Nurnberger, T.; Podobnik, M.; Anderluh, G. Molecular basis for functional diversity among microbial Nep1-like proteins. PLoS Pathog. 2019, 15, e1007951. [Google Scholar] [CrossRef] [Green Version]
  50. Wei, Z.M.; Laby, R.J.; Zumoff, C.H.; Bauer, D.W.; He, S.Y.; Collmer, A.; Beer, S.V. Harpin, elicitor of the hypersensitive response produced by the plant pathogen Erwinia amylovora. Science 1992, 257, 85–88. [Google Scholar] [CrossRef]
  51. Kulye, M.; Liu, H.; Zhang, Y.; Zeng, H.; Yang, X.; Qiu, D. Hrip1, a novel protein elicitor from necrotrophic fungus, Alternaria tenuissima, elicits cell death, expression of defence-related genes and systemic acquired resistance in tobacco. Plant Cell Environ. 2012, 35, 2104–2120. [Google Scholar] [CrossRef]
  52. Chen, M.; Zeng, H.; Qiu, D.; Guo, L.; Yang, X.; Shi, H.; Zhou, T.; Zhao, J. Purification and characterization of a novel hypersensitive response-inducing elicitor from Magnaporthe oryzae that triggers defense response in rice. PLoS ONE 2012, 7, e37654. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  53. Chen, M.; Zhang, C.; Zi, Q.; Qiu, D.; Liu, W.; Zeng, H. A novel elicitor identified from Magnaporthe oryzae triggers defense responses in tobacco and rice. Plant Cell Rep. 2014, 33, 1865–1879. [Google Scholar] [CrossRef] [PubMed]
  54. Miao, X.-Y.; Qu, H.-P.; Han, Y.-L.; He, C.-F.; Qiu, D.-W.; Cheng, Z.-W. The protein elicitor Hrip1 enhances resistance to insects and early bolting and flowering in Arabidopsis thaliana. PLoS ONE 2019, 14, e0216082. [Google Scholar] [CrossRef] [PubMed]
  55. Roby, D.; Toppan, A.; Esquerré-Tugayé, M.-T. Cell surfaces in plant-microorganism interactions. Plant Physiol. 1985, 77, 700–704. [Google Scholar] [CrossRef] [Green Version]
  56. Li, Y.-F.; Wang, Z.-Z.; Jia, X.-L. Membrane lipid peroxidation and hypersensitive reaction induced by a glycoprotein elicitor from Magnaporthe grisea in rice leaves. J. Plant Physiol. Mol. Biol. 2004, 30, 147–152. [Google Scholar]
  57. Yang, X.; Qiu, D.; Zeng, H.; Yuan, J.; Mao, J. Purification and characterization of a glycoprotein elicitor from Alternaria tenuissima. World J. Microb. Biot. 2009, 25, 2035–2042. [Google Scholar] [CrossRef]
  58. Radhajeyalakshmi, R.; Velazhahan, R.; Samiyappan, R.; Doraiswamy, S. Systemic induction of pathogenesis related proteins (PRs) in Alternaria solani elicitor sensitized tomato cells as resistance response. Sci. Res. Essays 2009, 4, 685–689. [Google Scholar]
  59. Zurzolo, C.; Simons, K. Glycosylphosphatidylinositol-anchored proteins: Membrane organization and transport. Biochim. Biophys. Acta. 2016, 1858, 632–639. [Google Scholar] [CrossRef]
  60. Fujita, M.; Kinoshita, T. GPI-anchor remodeling: Potential functions of GPI-anchors in intracellular trafficking and membrane dynamics. Biochim. Biophys. Acta. 2012, 1821, 1050–1058. [Google Scholar] [CrossRef]
  61. Oliveira-Garcia, E.; Deising, H.B. The glycosylphosphatidylinositol anchor biosynthesis genes GPI12, GAA1, and GPI8 are essential for cell-wall integrity and pathogenicity of the maize anthracnose fungus Colletotrichum graminicola. Mol. Plant-Microbe Interact. 2016, 29, 889–901. [Google Scholar] [CrossRef] [Green Version]
  62. Liu, C.; Xing, J.; Cai, X.; Hendy, A.; He, W.; Yang, J.; Huang, J.; Peng, Y.L.; Ryder, L.; Chen, X.L. GPI7-mediated glycosylphosphatidylinositol anchoring regulates appressorial penetration and immune evasion during infection of Magnaporthe oryzae. Environ. Microbiol. 2020, 22, 2581–2595. [Google Scholar] [CrossRef]
  63. Song, T.; Zhang, Y.; Zhang, Q.; Zhang, X.; Shen, D.; Yu, J.; Yu, M.; Pan, X.; Cao, H.; Yong, M.; et al. The N-terminus of an Ustilaginoidea virens Ser-Thr-rich glycosylphosphatidylinositol-anchored protein elicits plant immunity as a MAMP. Nat. Commun. 2021, 12, 2451. [Google Scholar] [CrossRef]
  64. Franco-Orozco, B.; Berepiki, A.; Ruiz, O.; Gamble, L.; Griffe, L.L.; Wang, S.; Birch, P.R.J.; Kanyuka, K.; Avrova, A. A new proteinaceous pathogen-associated molecular pattern PAMP identified in Ascomycete fungi induces cell death in Solanaceae. New Phytol. 2017, 214, 1657–1672. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  65. Nie, J.; Yin, Z.; Li, Z.; Wu, Y.; Huang, L. A small cysteine-rich protein from two kingdoms of microbes is recognized as a novel pathogen-associated molecular pattern. New Phytol. 2019, 222, 995–1011. [Google Scholar] [CrossRef] [PubMed]
  66. Xu, Q.; Hu, S.; Jin, M.; Xu, Y.; Jiang, Q.; Ma, J.; Zhang, Y.; Qi, P.; Chen, G.; Jiang, Y.; et al. The N-terminus of a Fusarium graminearum-secreted protein enhances broad-spectrum disease resistance in plants. Mol. Plant Pathol. 2022. [Google Scholar] [CrossRef]
  67. Nie, J.; Zhou, W.; Liu, J.; Tan, N.; Zhou, J.M.; Huang, L. A receptor-like protein from Nicotiana benthamiana mediates VmE02 PAMP-triggered immunity. New Phytol. 2021, 229, 2260–2272. [Google Scholar] [CrossRef] [PubMed]
  68. Petit-Houdenot, Y.; Fudal, I. Complex interactions between fungal avirulence genes and their corresponding plant resistance genes and consequences for disease resistance management. Front. Plant Sci. 2017, 8, 1072. [Google Scholar] [CrossRef] [Green Version]
  69. van Kan, J.A.; van den Ackerveken, G.F.; de Wit, P.J. Cloning and characterization of cDNA of avirulence gene avr9 of the fungal pathogen Cladosporium fulvum, causal agent of tomato leaf mold. Mol. Plant-Microbe Interact. 1991, 4, 52–59. [Google Scholar] [CrossRef]
  70. Zhang, S.; Li, C.; Si, J.; Han, Z.; Chen, D. Action mechanisms of effectors in plant-pathogen interaction. Int. J. Mol. Sci. 2022, 23, 6758. [Google Scholar] [CrossRef] [PubMed]
  71. Chen, J.; Upadhyaya, N.M.; Ortiz, D.; Sperschneider, J.; Li, F.; Bouton, C.; Breen, S.; Dong, C.; Xu, B.; Zhang, X. Loss of AvrSr50 by somatic exchange in stem rust leads to virulence for Sr50 resistance in wheat. Science 2017, 358, 1607–1610. [Google Scholar] [CrossRef] [Green Version]
  72. Salcedo, A.; Rutter, W.; Wang, S.; Akhunova, A.; Bolus, S.; Chao, S.; Anderson, N.; Soto, M.D.; Rouse, M.; Szabo, L. Variation in the AvrSr35 gene determines Sr35 resistance against wheat stem rust race Ug99. Science 2017, 358, 1604–1606. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  73. Cao, Y.; Yan, L.; Tanaka, K.; Nguyen, C.T.; Stacey, G. The kinase LYK5 is a major chitin receptor in Arabidopsis and forms a chitin-induced complex with related kinase CERK1. Elife 2014, 3, e03766. [Google Scholar] [CrossRef] [PubMed]
  74. Erwig, J.; Ghareeb, H.; Kopischke, M.; Hacke, R.; Matei, A.; Petutschnig, E.; Lipka, V. Chitin-induced and CHITIN ELICITOR RECEPTOR KINASE1 (CERK1) phosphorylation-dependent endocytosis of Arabidopsis thaliana LYSIN MOTIF-CONTAINING RECEPTOR-LIKE KINASE5 (LYK5). New Phytol. 2017, 215, 382–396. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  75. Kaku, H.; Nishizawa, Y.; Ishii-Minami, N.; Akimoto-Tomiyama, C.; Dohmae, N.; Takio, K.; Minami, E.; Shibuya, N. Plant cells recognize chitin fragments for defense signaling through a plasma membrane receptor. Proc. Natl. Acad. Sci. USA 2006, 103, 11086–11091. [Google Scholar] [CrossRef] [PubMed]
  76. Kouzai, Y.; Nakajima, K.; Hayafune, M.; Ozawa, K.; Kaku, H.; Shibuya, N.; Minami, E.; Nishizawa, Y. CEBiP is the major chitin oligomer-binding protein in rice and plays a main role in the perception of chitin oligomers. Plant Mol. Biol. 2014, 84, 519–528. [Google Scholar] [CrossRef]
  77. Bar, M.; Sharfman, M.; Ron, M.; Avni, A. BAK1 is required for the attenuation of ethylene-inducing xylanase (Eix)-induced defense responses by the decoy receptor LeEix1. Plant J. 2010, 63, 791–800. [Google Scholar] [CrossRef]
  78. Anderson, J.P.; Sperschneider, J.; Win, J.; Kidd, B.; Yoshida, K.; Hane, J.; Saunders, D.G.O.; Singh, K.B. Comparative secretome analysis of Rhizoctonia solani isolates with different host ranges reveals unique secretomes and cell death inducing effectors. Sci. Rep. 2017, 7, 10410. [Google Scholar] [CrossRef] [Green Version]
  79. Zhu, W.J.; Ronen, M.; Gur, Y.; Minz-Dub, A.; Masrati, G.; Ben-Tal, N.; Savidor, A.; Sharon, I.; Eizner, E.; Valerius, O.; et al. BcXYG1, a secreted xyloglucanase from Botrytis cinerea, triggers both cell death and plant immune responses. Plant Physiol. 2017, 175, 438–456. [Google Scholar] [CrossRef] [Green Version]
  80. Zhang, L.; Yan, J.P.; Fu, Z.C.; Shi, W.J.; Ninkuu, V.; Li, G.Y.; Yang, X.F.; Zeng, H.M. FoEG1, a secreted glycoside hydrolase family 12 protein from Fusarium oxysporum, triggers cell death and modulates plant immunity. Mol. Plant Pathol. 2021, 22, 522–538. [Google Scholar] [CrossRef]
  81. Gui, Y.J.; Chen, J.Y.; Zhang, D.D.; Li, N.Y.; Li, T.G.; Zhang, W.Q.; Wang, X.Y.; Short, D.P.G.; Li, L.; Guo, W.; et al. Verticillium dahliae manipulates plant immunity by glycoside hydrolase 12 proteins in conjunction with carbohydrate-binding module 1. Environ. Microbiol. 2017, 19, 1914–1932. [Google Scholar] [CrossRef] [Green Version]
  82. Zhang, L.S.; Kars, I.; Essenstam, B.; Liebrand, T.W.H.; Wagemakers, L.; Elberse, J.; Tagkalaki, P.; Tjoitang, D.; van den Ackerveken, G.; van Kan, J.A.L. Fungal endopolygalacturonases are recognized as microbe-associated molecular patterns by the Arabidopsis receptor-like protein RESPONSIVENESS TO BOTRYTIS POLYGALACTURONASES1. Plant Physiol. 2014, 164, 352–364. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  83. Ma, Y.A.; Han, C.; Chen, J.Y.; Li, H.Y.; He, K.; Liu, A.X.; Li, D.C. Fungal cellulase is an elicitor but its enzymatic activity is not required for its elicitor activity. Mol. Plant Pathol. 2015, 16, 14–26. [Google Scholar] [CrossRef] [PubMed]
  84. Schouten, A.; van Baarlen, P.; van Kan, J.A.L. Phytotoxic Nep1-like proteins from the necrotrophic fungus Botrytis cinerea associate with membranes and the nucleus of plant cells. New Phytol. 2008, 177, 493–505. [Google Scholar] [CrossRef] [PubMed]
  85. Ono, E.; Mise, K.; Takano, Y. RLP23 is required for Arabidopsis immunity against the grey mould pathogen Botrytis cinerea. Sci. Rep. 2020, 10, 13798. [Google Scholar] [CrossRef]
  86. Redkar, A.; Cevik, V.; Bailey, K.; Zhao, H.; Kim, D.S.; Zou, Z.; Furzer, O.J.; Fairhead, S.; Borhan, M.H.; Holub, E.B.; et al. The Arabidopsis WRR4A and WRR4B paralogous NLR proteins both confer recognition of multiple Albugo candida effectors. New Phytol. 2022. [Google Scholar] [CrossRef]
  87. Lu, X.L.; Kracher, B.; Saur, I.M.L.; Bauer, S.; Ellwood, S.R.; Wise, R.; Yaeno, T.; Maekawa, T.; Schulze-Lefert, P. Allelic barley MLA immune receptors recognize sequence-unrelated avirulence effectors of the powdery mildew pathogen. Proc. Natl. Acad. Sci. USA 2016, 113, E6486–E6495. [Google Scholar] [CrossRef] [Green Version]
  88. Saur, I.M.L.; Bauer, S.; Kracher, B.; Lu, X.L.; Franzeskakis, L.; Muller, M.C.; Sabelleck, B.; Kummel, F.; Panstruga, R.; Maekawa, T.; et al. Multiple pairs of allelic MLA immune receptor-powdery mildew AVR(A) effectors argue for a direct recognition mechanism. Elife 2019, 8, e44471. [Google Scholar] [CrossRef]
  89. Bauer, S.; Yu, D.L.; Lawson, A.W.; Saur, I.M.L.; Frantzeskakis, L.; Kracher, B.; Logemann, E.; Chai, J.J.; Maekawa, T.; Schulze-Lefert, P. The leucine-rich repeats in allelic barley MLA immune receptors define specificity towards sequence-unrelated powdery mildew avirulence effectors with a predicted common RNase-like fold. PloS Pathog. 2021, 17, e1009223. [Google Scholar] [CrossRef]
  90. Praz, C.R.; Bourras, S.; Zeng, F.S.; Sanchez-Martin, J.; Menardo, F.; Xue, M.F.; Yang, L.J.; Roffler, S.; Boni, R.; Herren, G.; et al. AvrPm2 encodes an RNase-like avirulence effector which is conserved in the two different specialized forms of wheat and rye powdery mildew fungus. New Phytol. 2017, 213, 1301–1314. [Google Scholar] [CrossRef] [Green Version]
  91. Bourras, S.; McNally, K.E.; Ben-David, R.; Parlange, F.; Roffler, S.; Praz, C.R.; Oberhaensli, S.; Menardo, F.; Stirnweis, D.; Frenkel, Z.; et al. Multiple avirulence loci and allele-specific effector recognition control the Pm3 race-specific resistance of wheat to powdery mildew. Plant Cell 2015, 27, 2991–3012. [Google Scholar]
  92. Bourras, S.; Kunz, L.; Xue, M.F.; Praz, C.R.; Muller, M.C.; Kalin, C.; Schlafli, M.; Ackermann, P.; Fluckiger, S.; Parlange, F.; et al. The AvrPm3-Pm3 effector-NLR interactions control both race-specific resistance and host-specificity of cereal mildews on wheat. Nat. Commun. 2019, 10, 2292. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  93. Muller, M.C.; Kunz, L.; Schudel, S.; Lawson, A.W.; Kammerecker, S.; Isaksson, J.; Wyler, M.; Graf, J.; Sotiropoulos, A.G.; Praz, C.R.; et al. Ancient variation of the AvrPm17 gene in powdery mildew limits the effectiveness of the introgressed rye Pm17 resistance gene in wheat. Proc. Natl. Acad. Sci. USA 2022, 119, e2108808119. [Google Scholar] [CrossRef] [PubMed]
  94. Jones, D.A.; Thomas, C.M.; Hammondkosack, K.E.; Balintkurti, P.J.; Jones, J.D.G. Isolation of the tomato Cf-9 gene for resistance to Cladosporium Fulvum by transposon tagging. Science 1994, 266, 789–793. [Google Scholar] [CrossRef] [PubMed]
  95. Dixon, M.S.; Hatzixanthis, K.; Jones, D.A.; Harrison, K.; Jones, J.D.G. The tomato Cf-5 disease resistance gene and six homologs show pronounced allelic variation in leucine-rich repeat copy number. Plant Cell 1998, 10, 1915–1925. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  96. Thomas, C.M.; Jones, D.A.; Parniske, M.; Harrison, K.; Balint-Kurti, P.J.; Hatzixanthis, K.; Jones, J.D.G. Characterization of the tomato Cf-4 gene for resistance to Cladosporium fulvum identifies sequences that determine recognitional specificity in Cf-4 and Cf-9. Plant Cell 1997, 9, 2209–2224. [Google Scholar]
  97. Dixon, M.S.; Jones, D.A.; Keddie, J.S.; Thomas, C.M.; Harrison, K.; Jones, J.D.G. The tomato Cf-2 disease resistance locus comprises two functional genes encoding leucine-rich repeat proteins. Cell 1996, 84, 451–459. [Google Scholar] [CrossRef]
  98. Takken, F.L.W.; Thomas, C.M.; Joosten, M.H.A.J.; Golstein, C.; Westerink, N.; Hille, J.; Nijkamp, H.J.J.; De Wit, P.J.G.M.; Jones, J.D.G. A second gene at the tomato Cf-4 locus confers resistance to Cladosporium fulvum through recognition of a novel avirulence determinant. Plant J. 1999, 20, 279–288. [Google Scholar] [CrossRef]
  99. Houterman, P.M.; Ma, L.; van Ooijen, G.; de Vroomen, M.J.; Cornelissen, B.J.C.; Takken, F.L.W.; Rep, M. The effector protein Avr2 of the xylem-colonizing fungus Fusarium oxysporum activates the tomato resistance protein I-2 intracellularly. Plant J. 2009, 58, 970–978. [Google Scholar] [CrossRef]
  100. Schmidt, S.M.; Lukasiewicz, J.; Farrer, R.; van Dam, P.; Bertoldo, C.; Rep, M. Comparative genomics of Fusarium oxysporum f. sp melonis reveals the secreted protein recognized by the Fom-2 resistance gene in melon. New Phytol. 2016, 209, 307–318. [Google Scholar] [CrossRef] [Green Version]
  101. Larkan, N.J.; Lydiate, D.J.; Parkin, I.A.P.; Nelson, M.N.; Epp, D.J.; Cowling, W.A.; Rimmer, S.R.; Borhan, M.H. The Brassica napus blackleg resistance gene LepR3 encodes a receptor-like protein triggered by the Leptosphaeria maculans effector AVRLM1. New Phytol. 2013, 197, 595–605. [Google Scholar] [CrossRef]
  102. Devanna, N.B.; Vijayan, J.; Sharma, T.R. The blast resistance gene Pi54of cloned from Oryza officinalis interacts with Avr-Pi54 through its novel non-LRR domains. PLoS ONE 2014, 9, e104840. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  103. Wu, J.; Kou, Y.J.; Bao, J.D.; Li, Y.; Tang, M.Z.; Zhu, X.L.; Ponaya, A.; Xiao, G.; Li, J.B.; Li, C.Y.; et al. Comparative genomics identifies the Magnaporthe oryzae avirulence effector AvrPi9 that triggers Pi9-mediated blast resistance in rice. New Phytol. 2015, 206, 1463–1475. [Google Scholar] [CrossRef] [PubMed]
  104. Zhang, S.L.; Wang, L.; Wu, W.H.; He, L.Y.; Yang, X.F.; Pan, Q.H. Function and evolution of Magnaporthe oryzae avirulence gene AvrPib responding to the rice blast resistance gene Pib. Sci. Rep. 2015, 5, 11642. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  105. Kanzaki, H.; Yoshida, K.; Saitoh, H.; Fujisaki, K.; Hirabuchi, A.; Alaux, L.; Fournier, E.; Tharreau, D.; Terauchi, R. Arms race co-evolution of Magnaporthe oryzae AVR-Pik and rice Pik genes driven by their physical interactions. Plant J. 2012, 72, 894–907. [Google Scholar] [CrossRef]
  106. Li, W.; Wang, B.H.; Wu, J.; Lu, G.D.; Hu, Y.J.; Zhang, X.; Zhang, Z.G.; Zhao, Q.; Feng, Q.Y.; Zhang, H.Y.; et al. The Magnaporthe oryzae 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. 2009, 22, 411–420. [Google Scholar] [CrossRef] [Green Version]
  107. Jia, Y.L.; Zhou, E.; Lee, S.; Bianco, T. Coevolutionary dynamics of rice blast resistance gene Pi-ta and Magnaporthe oryzae avirulence gene AVR-Pita 1. Phytopathology 2016, 106, 676–683. [Google Scholar] [CrossRef]
  108. Cesari, S.; Thilliez, G.; Ribot, C.; Chalvon, V.; Michel, C.; Jauneau, A.; Rivas, S.; Alaux, L.; Kanzaki, H.; Okuyama, Y.; et al. The rice resistance protein pair RGA4/RGA5 recognizes the Magnaporthe oryzae effectors AVR-Pia and AVR1-CO39 by direct binding. Plant Cell 2013, 25, 1463–1481. [Google Scholar] [CrossRef] [Green Version]
  109. Vo, K.T.X.; Lee, S.K.; Halane, M.K.; Song, M.Y.; Hoang, T.V.; Kim, C.Y.; Park, S.Y.; Jeon, J.; Kim, S.T.; Sohn, K.H.; et al. Pi5 and Pii paired NLRs are functionally exchangeable and confer similar disease resistance specificity. Mol. Cells 2019, 42, 637–645. [Google Scholar]
  110. Anderson, C.; Khan, M.A.; Catanzariti, A.M.; Jack, C.A.; Nemri, A.; Lawrence, G.J.; Upadhyaya, N.M.; Hardham, A.R.; Ellis, J.G.; Dodds, P.N.; et al. Genome analysis and avirulence gene cloning using a high-density RADseq linkage map of the flax rust fungus, Melampsora lini. BMC Genom. 2016, 17, 667. [Google Scholar] [CrossRef] [Green Version]
  111. Ve, T.; Williams, S.J.; Catanzariti, A.M.; Rafiqi, M.; Rahman, M.; Ellis, J.G.; Hardham, A.R.; Jones, D.A.; Anderson, P.A.; Dodds, P.N.; et al. Structures of the flax-rust effector AvrM reveal insights into the molecular basis of plant-cell entry and effector-triggered immunity. Proc. Natl. Acad. Sci. USA 2013, 110, 17594–17599. [Google Scholar] [CrossRef] [Green Version]
  112. Dodds, P.N.; Lawrence, G.J.; Catanzariti, A.M.; Ayliffe, M.A.; Ellis, J.G. The Melampsora lini AvrL567 avirulence genes are expressed in haustoria and their products are recognized inside plant cells. Plant Cell 2004, 16, 755–768. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  113. Deng, C.; Leonard, A.; Cahill, J.; Lv, M.; Li, Y.R.; Thatcher, S.; Li, X.Y.; Zhao, X.D.; Du, W.J.; Li, Z.; et al. The RppC-AvrRppC NLR-effector interaction mediates the resistance to southern corn rust in maize. Mol. Plant 2022, 15, 904–912. [Google Scholar] [CrossRef] [PubMed]
  114. Chen, G.; Zhang, B.; Ding, J.; Wang, H.; Deng, C.; Wang, J.; Yang, Q.; Pi, Q.; Zhang, R.; Zhai, H.; et al. Cloning southern corn rust resistant gene RppK and its cognate gene AvrRppK from Puccinia polysora. Nat. Commun. 2022, 13, 4392. [Google Scholar] [CrossRef]
  115. Wang, J.; Chai, J. Structural insights into the plant immune receptors PRRs and NLRs. Plant Physiol. 2020, 182, 1566–1581. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  116. Ma, X.; Xu, G.; He, P.; Shan, L. SERKing coreceptors for receptors. Trends Plant Sci. 2016, 21, 1017–1033. [Google Scholar] [CrossRef] [PubMed]
  117. Liu, T.; Liu, Z.; Song, C.; Hu, Y.; Han, Z.; She, J.; Fan, F.; Wang, J.; Jin, C.; Chang, J. Chitin-Induced dimerization activates a plant immune receptor. Science 2012, 336, 1160–1164. [Google Scholar] [CrossRef] [Green Version]
  118. Ngou, B.P.M.; Jones, J.D.G.; Ding, P.T. Plant immune networks. Trends Plant Sci. 2022, 27, 255–273. [Google Scholar] [CrossRef]
  119. Jones, J.D.G.; Vance, R.E.; Dangl, J.L. Intracellular innate immune surveillance devices in plants and animals. Science 2016, 354, aaf6395. [Google Scholar] [CrossRef] [Green Version]
  120. Liu, X.X.; Wan, L. Molecular insights into the biochemical functions and signalling mechanisms of plant NLRs. Mol. Plant Pathol. 2022, 23, 772–780. [Google Scholar] [CrossRef]
  121. Rodriguez-Moreno, L.; Song, Y.; Thomma, B.P.H.J. Transfer and engineering of immune receptors to improve recognition capacities in crops. Curr. Opin. Plant Biol. 2017, 38, 42–49. [Google Scholar] [CrossRef]
  122. Schultink, A.; Steinbrenner, A.D. A playbook for developing disease-resistant crops through immune receptor identification and transfer. Curr. Opin. Plant Biol. 2021, 62, 102089. [Google Scholar] [CrossRef] [PubMed]
  123. Brunner, S.; Stirnweis, D.; Quijano, C.D.; Buesing, G.; Herren, G.; Parlange, F.; Barret, P.; Tassy, C.; Sautter, C.; Winzeler, M.; et al. Transgenic Pm3 multilines of wheat show increased powdery mildew resistance in the field. Plant Biotechnol. J. 2012, 10, 398–409. [Google Scholar] [CrossRef] [PubMed]
  124. Fradin, E.F.; Abd-El-Haliem, A.; Masini, L.; van den Berg, G.C.M.; Joosten, M.H.A.J.; Thomma, B.P.H.J. Interfamily transfer of tomato Ve1 mediates Verticillium resistance in Arabidopsis. Plant Physiol. 2011, 156, 2255–2265. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  125. Li, W.; Deng, Y.W.; Ning, Y.S.; He, Z.H.; Wang, G.L. Exploiting broad-spectrum disease resistance in crops: From molecular dissection to breeding. Annu. Rev. Plant Biol. 2020, 71, 575–603. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  126. Liu, B.; Li, J.F.; Ao, Y.; Qu, J.W.; Li, Z.Q.; Su, J.B.; Zhang, Y.; Liu, J.; Feng, D.R.; Qi, K.B.; et al. Lysin motif-containing proteins LYP4 and LYP6 play dual roles in peptidoglycan and chitin perception in rice innate immunity. Plant Cell 2012, 24, 3406–3419. [Google Scholar] [CrossRef] [Green Version]
  127. Luo, M.; Xie, L.Q.; Chakraborty, S.; Wang, A.H.; Matny, O.; Jugovich, M.; Kolmer, J.A.; Richardson, T.; Bhatt, D.; Hoque, M.; et al. A five-transgene cassette confers broad-spectrum resistance to a fungal rust pathogen in wheat. Nat. Biotechnol. 2021, 39, 561–566. [Google Scholar] [CrossRef]
  128. Liu, Y.; Zhang, X.; Yuan, G.X.; Wang, D.L.; Zheng, Y.Y.; Ma, M.Q.; Guo, L.W.; Bhadauria, V.; Peng, Y.L.; Liu, J.F. A designer rice NLR immune receptor confers resistance to the rice blast fungus carrying noncorresponding avirulence effectors. Proc. Natl. Acad. Sci. USA 2021, 118, e2110751118. [Google Scholar] [CrossRef]
  129. Wang, N.; Tang, C.; Fan, X.; He, M.; Gan, P.; Zhang, S.; Hu, Z.; Wang, X.; Yan, T.; Shu, W.; et al. Inactivation of a wheat protein kinase gene confers broad-spectrum resistance to rust fungi. Cell 2022, 185, 2961–2974. [Google Scholar] [CrossRef]
  130. Ngou, B.P.M.; Ding, P.T.; Jones, J.D.G. Thirty years of resistance: Zig-zag through the plant immune system. Plant Cell 2022, 34, 1447–1478. [Google Scholar] [CrossRef]
  131. Wang, W.; Feng, B.; Zhou, J.-M.; Tang, D. Plant immune signaling: Advancing on two frontiers. J. Integr. Plant Biol. 2020, 62, 2–24. [Google Scholar] [CrossRef] [Green Version]
  132. Abdul Malik, N.A.; Kumar, I.S.; Nadarajah, K. Elicitor and receptor molecules: Orchestrators of plant defense and immunity. Int. J. Mol. Sci. 2020, 21, 963. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  133. DeFalco, T.A.; Zipfel, C. Molecular mechanisms of early plant pattern-triggered immune signaling. Mol. Cell 2021, 81, 3449–3467. [Google Scholar] [CrossRef]
  134. Xue, D.-X.; Li, C.-L.; Xie, Z.-P.; Staehelin, C. LYK4 is a component of a tripartite chitin receptor complex in Arabidopsis thaliana. J. Exp. Bot. 2019, 70, 5507–5516. [Google Scholar] [CrossRef] [PubMed]
  135. Paparella, C.; Savatin, D.V.; Marti, L.; De Lorenzo, G.; Ferrari, S. The Arabidopsis LYSIN MOTIF-CONTAINING RECEPTOR-LIKE KINASE3 regulates the cross talk between immunity and abscisic acid responses. Plant Physiol. 2014, 165, 262–276. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  136. Le, M.H.; Cao, Y.; Zhang, X.C.; Stacey, G. LIK1, a CERK1-interacting kinase, regulates plant immune responses in Arabidopsis. PLoS ONE 2014, 9, e102245. [Google Scholar] [CrossRef] [Green Version]
  137. Liang, X.; Zhou, J.M. Receptor-like cytoplasmic kinases: Central players in plant receptor kinase–mediated signaling. Annu. Rev. Plant Biol. 2018, 69, 267–299. [Google Scholar] [CrossRef] [Green Version]
  138. Tian, W.; Hou, C.; Ren, Z.; Wang, C.; Zhao, F.; Dahlbeck, D.; Hu, S.; Zhang, L.; Niu, Q.; Li, L.; et al. A calmodulin-gated calcium channel links pathogen patterns to plant immunity. Nature 2019, 572, 131–135. [Google Scholar] [CrossRef]
  139. Kadota, Y.; Sklenar, J.; Derbyshire, P.; Stransfeld, L.; Asai, S.; Ntoukakis, V.; Jonathan, D.G.J.; Shirasu, K.; Menke, F.; Jones, A.; et al. Direct regulation of the NADPH oxidase RBOHD by the PRR-associated kinase BIK1 during plant immunity. Mol. Cell 2014, 54, 43–55. [Google Scholar] [CrossRef] [Green Version]
  140. Rao, S.; Zhou, Z.; Miao, P.; Bi, G.; Hu, M.; Wu, Y.; Feng, F.; Zhang, X.; Zhou, J.-M. Roles of receptor-like cytoplasmic kinase VII members in pattern-triggered immune signaling. Plant Physiol. 2018, 177, 1679–1690. [Google Scholar] [CrossRef] [Green Version]
  141. Lv, S.; Zhang, Y.; Li, C.; Liu, Z.; Yang, N.; Pan, L.; Wu, J.; Wang, J.; Yang, J.; Lv, Y.; et al. Strigolactone-triggered stomatal closure requires hydrogen peroxide synthesis and nitric oxide production in an abscisic acid-independent manner. New Phytol. 2018, 217, 290–304. [Google Scholar] [CrossRef] [Green Version]
  142. Lin, W.; Tsuda, K.; Sato, M.; Cohen, J.D.; Katagiri, F.; Glazebrook, J. Arabidopsis CaM binding protein CBP60g contributes to MAMP-induced SA accumulation and is involved in disease resistance against Pseudomonas syringae. PLoS Pathog. 2009, 5, e1000301. [Google Scholar]
  143. Waszczak, C.; Carmody, M.; Kangasjärvi, J. Reactive oxygen species in plant signaling. Annu. Rev. Plant Biol. 2018, 69, 209–236. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  144. Dvořák, P.; Krasylenko, Y.; Zeiner, A.; Šamaj, J.; Takáč, T. Signaling toward reactive oxygen species-scavenging enzymes in plants. Front. Plant Sci. 2021, 11, 2178. [Google Scholar] [CrossRef] [PubMed]
  145. Kumar, A.; Guleria, S.; Ghosh, D.; Dogra, V.; Kumar, S. Managing reactive oxygen species—Some learnings from high altitude extremophytes. Environ. Exp. Bot. 2021, 189, 104525. [Google Scholar] [CrossRef]
  146. Zhang, J.; Li, W.; Xiang, T.; Liu, Z.; Laluk, K.; Ding, X.; Zou, Y.; Gao, M.; Zhang, X.; Chen, S.; et al. Receptor-like cytoplasmic kinases integrate signaling from multiple plant immune receptors and are targeted by a Pseudomonas syringae effector. Cell Host Microbe 2010, 7, 290–301. [Google Scholar] [CrossRef] [Green Version]
  147. Shinya, T.; Yamaguchi, K.; Desaki, Y.; Yamada, K.; Narisawa, T.; Kobayashi, Y.; Maeda, K.; Suzuki, M.; Tanimoto, T.; Takeda, J.; et al. Selective regulation of the chitin-induced defense response by the Arabidopsis receptor-like cytoplasmic kinase PBL27. Plant J. 2014, 79, 56–66. [Google Scholar] [CrossRef] [PubMed]
  148. Yamada, K.; Yamaguchi, K.; Shirakawa, T.; Nakagami, H.; Mine, A.; Ishikawa, K.; Fujiwara, M.; Narusaka, M.; Narusaka, Y.; Ichimura, K.; et al. The Arabidopsis CERK1-associated kinase PBL27 connects chitin perception to MAPK activation. EMBO J. 2016, 35, 2468–2483. [Google Scholar] [CrossRef]
  149. Bi, G.; Zhou, Z.; Wang, W.; Li, L.; Rao, S.; Wu, Y.; Zhang, X.; Menke, F.L.H.; Chen, S.; Zhou, J.-M. Receptor-like cytoplasmic kinases directly link diverse pattern recognition receptors to the activation of mitogen-activated protein kinase cascades in Arabidopsis. Plant Cell 2018, 30, 1543–1561. [Google Scholar] [CrossRef]
  150. Li, G.; Meng, X.; Wang, R.; Mao, G.; Han, L.; Liu, Y.; Zhang, S. Dual-level regulation of ACC synthase activity by MPK3/MPK6 cascade and its downstream WRKY transcription factor during ethylene induction in Arabidopsis. PLoS Genet. 2012, 8, e1002767. [Google Scholar] [CrossRef]
  151. Martel, A.; Ruiz-Bedoya, T.; Breit-McNally, C.; Laflamme, B.; Desveaux, D.; Guttman, D.S. The ETS-ETI cycle: Evolutionary processes and metapopulation dynamics driving the diversification of pathogen effectors and host immune factors. Curr. Opin. Plant Biol. 2021, 62, 102011. [Google Scholar] [CrossRef]
  152. Fick, A.; Swart, V.; van den Berg, N. The ups and downs of plant NLR expression during pathogen infection. Front. Plant Sci. 2022, 13, 921148. [Google Scholar] [CrossRef] [PubMed]
  153. Dodds, P.N.; Rathjen, J.P. Plant immunity: Towards an integrated view of plant–pathogen interactions. Nat. Rev. Genet. 2010, 11, 539–548. [Google Scholar] [CrossRef] [PubMed]
  154. Jia, Y.; M Ca Dams, S.A.; Bryan, G.T.; Hershey, H.P.; Valent, B. Direct interaction of resistance gene and avirulence gene products confers rice BLAST resistance. EMBO J. 2000, 19, 4004–4014. [Google Scholar] [CrossRef] [PubMed]
  155. Li, W. Molecular mechanisms of Cf-dependent ETI and Xoo-induced nonhost resistance in Nicotiana benthamiana. Ph.D. Thesis, Zhejiang University, Hangzhou, China, 2015. [Google Scholar]
  156. Kang, H.; Nguyen, Q.-M.; Iswanto, A.B.B.; Hong, J.C.; Bhattacharjee, S.; Gassmann, W.; Kim, S.H. Nuclear localization of HopA1Pss61 is required for effector-triggered immunity. Plants 2021, 10, 888. [Google Scholar] [CrossRef] [PubMed]
  157. Lapin, D.; Bhandari, D.D.; Parker, J.E. Origins and immunity networking functions of EDS1 family proteins. Annu. Rev. Phytopathol. 2020, 58, 253–276. [Google Scholar] [CrossRef] [PubMed]
  158. Bhandari, D.D.; Lapin, D.; Kracher, B.; von Born, P.; Bautor, J.; Niefind, K.; Parker, J.E. An EDS1 heterodimer signalling surface enforces timely reprogramming of immunity genes in Arabidopsis. Nat. Commun. 2019, 10, 772. [Google Scholar] [CrossRef]
  159. Lapin, D.; Kovacova, V.; Sun, X.; Dongus, J.A.; Parker, J.E. A coevolved EDS1-SAG101-NRG1 module mediates cell death signaling by TIR-domain immune receptors. Plant Cell 2019, 31, 2430–2455. [Google Scholar] [CrossRef] [Green Version]
  160. Zhou, J.-M.; Zhang, Y. Plant immunity: Danger perception and signaling. Cell 2020, 181, 978–989. [Google Scholar] [CrossRef]
  161. Xiao, S.; Calis, O.; Patrick, E.; Zhang, G.; Charoenwattana, P.; Muskett, P.; Parker, J.E.; Turner, J.G. The atypical resistance gene, RPW8, recruits components of basal defence for powdery mildew resistance in Arabidopsis. Plant J. 2005, 42, 95–110. [Google Scholar] [CrossRef]
  162. De Jong, C.F.; HonÉE, G.U.Y.; Joosten, M.H.A.J.; De Wit, P.J.G.M. Early defence responses induced by AVR9 and mutant analogues in tobacco cell suspensions expressing the Cf-9 resistance gene. Physiol. Mol. Plant P. 2000, 56, 169–177. [Google Scholar] [CrossRef]
  163. Heese, A.; Ludwig, A.A.; Jones, J.D.G. Rapid phosphorylation of a syntaxin during the Avr9/Cf-9-race-specific signaling pathway. Plant Physiol. 2005, 138, 2406–2416. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  164. Dongus, J.A.; Parker, J.E. EDS1 signalling: At the nexus of intracellular and surface receptor immunity. Curr. Opin. Plant Biol. 2021, 62, 102039. [Google Scholar] [CrossRef] [PubMed]
  165. Stergiopoulos, I.; Wit, P.D. Fungal effector proteins. Annu. Rev. Phytopathol. 2009, 47, 233–263. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  166. Li, Y.; Xue, J.; Wang, F.-Z.; Huang, X.; Gong, B.-Q.; Tao, Y.; Shen, W.; Tao, K.; Yao, N.; Xiao, S.; et al. Plasma membrane-nucleo-cytoplasmic coordination of a receptor-like cytoplasmic kinase promotes EDS1-dependent plant immunity. Nat. Plants 2022, 8, 802–816. [Google Scholar] [CrossRef]
  167. Pruitt, R.N.; Locci, F.; Wanke, F.; Zhang, L.; Saile, S.C.; Joe, A.; Karelina, D.; Hua, C.; Fröhlich, K.; Wan, W.-L.; et al. The EDS1–PAD4–ADR1 node mediates Arabidopsis pattern-triggered immunity. Nature 2021, 598, 495–499. [Google Scholar] [CrossRef]
  168. Wan, L.; Essuman, K.; Anderson, R.G.; Sasaki, Y.; Monteiro, F.; Chung, E.H.; Nishimura, E.O.; DiAntonio, A.; Milbrandt, J.; Dangl, J.L.; et al. TIR domains of plant immune receptors are NAD(+)-cleaving enzymes that promote cell death. Science 2019, 365, 799–803. [Google Scholar] [CrossRef]
  169. Horsefield, S.; Burdett, H.; Zhang, X.X.; Manik, M.K.; Shi, Y.; Chen, J.; Qi, T.C.; Gilley, J.; Lai, J.S.; Rank, M.X.; et al. NAD(+) cleavage activity by animal an plant TIR domains in cell death pathways. Science 2019, 365, 793–799. [Google Scholar] [CrossRef] [Green Version]
  170. Tian, H.; Wu, Z.; Chen, S.; Ao, K.; Huang, W.; Yaghmaiean, H.; Sun, T.; Xu, F.; Zhang, Y.; Wang, S.; et al. Activation of TIR signalling boosts pattern-triggered immunity. Nature 2021, 598, 500–503. [Google Scholar] [CrossRef]
  171. Perez-Hernandez, A.; Gonzalez, M.; Gonzalez, C.; Brito, N. The elicitor protein BcIEB1 and the derived peptide ieb35 provide long-term plant protection. Plant Pathol. 2020, 69, 807–817. [Google Scholar] [CrossRef]
  172. Cheng, Y.L.; Lin, Y.L.; Cao, H.H.; Li, Z.G. Citrus postharvest green mold: Recent advances in fungal pathogenicity and fruit resistance. Microorganisms 2020, 8, 449. [Google Scholar] [CrossRef] [Green Version]
  173. Tian, S.; Torres, R.; Ballester, A.R.; Li, B.; Vilanova, L.; Gonzalez-Candelas, L. Molecular aspects in pathogen-fruit interactions: Virulence and resistance. Postharvest Biol. Tec. 2016, 122, 11–21. [Google Scholar] [CrossRef] [Green Version]
  174. Wang, Y.; Xu, Y.P.; Sun, Y.J.; Wang, H.B.; Qi, J.M.; Wan, B.W.; Ye, W.W.; Lin, Y.C.; Shao, Y.Y.; Dong, S.M.; et al. Leucine-rich repeat receptor-like gene screen reveals that Nicotiana RXEG1 regulates glycoside hydrolase 12 MAMP detection. Nat. Commun. 2018, 9, 594. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  175. Yuan, M.H.; Ngou, B.P.M.; Ding, P.T.; Xiu-Fan, X. PTI-ETI crosstalk: An integrative view of plant immunity. Curr. Opin. Plant Biol. 2021, 62, 102030. [Google Scholar] [CrossRef] [PubMed]
Ijms 23 12003 g001 550
Figure 1. Classification of fungal elicitors. Known fungal elicitors can be classified into two major categories, including saccharide elicitors and protein elicitors. The figure is drawn by Figdraw.
Figure 1. Classification of fungal elicitors. Known fungal elicitors can be classified into two major categories, including saccharide elicitors and protein elicitors. The figure is drawn by Figdraw.
Ijms 23 12003 g001
Ijms 23 12003 g002 550
Figure 2. A model of the signaling pathways of fungal PAMPs-triggered PTI and fungal effector-triggered ETI. ROS, reactive oxygen species; HR, hypersensitive response; SA, salicylic acid. The figure is drawn by BioRender.
Figure 2. A model of the signaling pathways of fungal PAMPs-triggered PTI and fungal effector-triggered ETI. ROS, reactive oxygen species; HR, hypersensitive response; SA, salicylic acid. The figure is drawn by BioRender.
Ijms 23 12003 g002
Publisher’s Note: MDPI stays neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Share and Cite

MDPI and ACS Style

Guo, J.; Cheng, Y. Advances in Fungal Elicitor-Triggered Plant Immunity. Int. J. Mol. Sci. 2022, 23, 12003. https://doi.org/10.3390/ijms231912003

AMA Style

Guo J, Cheng Y. Advances in Fungal Elicitor-Triggered Plant Immunity. International Journal of Molecular Sciences. 2022; 23(19):12003. https://doi.org/10.3390/ijms231912003

Chicago/Turabian Style

Guo, Jia, and Yulin Cheng. 2022. "Advances in Fungal Elicitor-Triggered Plant Immunity" International Journal of Molecular Sciences 23, no. 19: 12003. https://doi.org/10.3390/ijms231912003

Note that from the first issue of 2016, this journal uses article numbers instead of page numbers. See further details here.

Article Metrics

Back to TopTop