Apoplastic Cell Death-Inducing Proteins of Filamentous Plant Pathogens: Roles in Plant-Pathogen Interactions

Abstract

Filamentous pathogens, such as phytopathogenic oomycetes and fungi, secrete a remarkable diversity of apoplastic effector proteins to facilitate infection, many of which are able to induce cell death in plants. Over the past decades, over 177 apoplastic cell death-inducing proteins (CDIPs) have been identified in filamentous oomycetes and fungi. An emerging number of studies have demonstrated the role of many apoplastic CDIPs as essential virulence factors. At the same time, apoplastic CDIPs have been documented to be recognized by plant cells as pathogen-associated molecular patterns (PAMPs). The recent findings of extracellular recognition of apoplastic CDIPs by plant leucine-rich repeat-receptor-like proteins (LRR-RLPs) have greatly advanced our understanding of how plants detect them and mount a defense response. This review summarizes the latest advances in identifying apoplastic CDIPs of plant pathogenic oomycetes and fungi, and our current understanding of the dual roles of apoplastic CDIPs in plant-filamentous pathogen interactions.

Introduction

Filamentous pathogens, such as oomycetes and fungi, are the causal agents of many of the world’s most serious plant diseases, causing extensive annual yield losses of crops worldwide (Giraldo and Valent, 2013; Sánchez-Vallet et al., 2018). Pathogenic oomycetes and fungi secrete a complex repertoire of effector proteins to establish successful interactions with host plants. These oomycete- or fungi-secreted effector proteins may function in the apoplast as well as within plant cells to interfere with host defense by a variety of mechanisms (Dou and Zhou, 2012; Lo Presti and Kahmann, 2017).

Studies from diverse filamentous pathogens have shown that many oomycete or fungal effector proteins possess the ability to induce cell death in plants (Gijzen and Nürnberger, 2006), including avirulence (AVR) proteins which trigger hypersensitive response (HR) upon recognition by cognate resistance (R) proteins (Kamoun, 2006; Ellis et al., 2009), nuclear-localized Crinkling and Necrosis proteins (CRNs) and nucleo-cytoplasmic RxLR proteins with capacity to induce plant cell death (Torto et al., 2003; Amaro et al., 2017), and extracellular cell death-inducing proteins (CDIPs) that function in the plant apoplast (Guo et al., 2019). The role of AVR proteins, CRN and RxLR effectors involved in the interactions of plants with filamentous pathogens have been reviewed extensively (Ellis et al., 2009; Giraldo and Valent, 2013; Amaro et al., 2017; Lo Presti and Kahmann, 2017). Here we focus this review on apoplastic CDIPs of filamentous plant pathogens and their roles in plant-pathogen interactions.

Because cell death plays an important role in the interactions of plants with pathogens, there has been a long-standing interest in the characterization of pathogenic molecules which are able to induce plant cell death (Gijzen and Nürnberger, 2006). Since the characterization of elicitins, a family of conserved small secreted proteins from oomycetes that induce necrosis in Nicotiana species, in the 1980s (Billard et al., 1988; Huet and Pernollet, 1989; Ricci et al., 1989), a large number of apoplastic CDIPs have been identified in oomycete and fungal plant pathogens (Tables 1, 2). These apoplastic CDIPs induce plant cell death in a non-race- or non-species-specific manner, and were initially defined or considered as “elicitors” or “toxins” (Gijzen and Nürnberger, 2006; Derevnina et al., 2016). The role of apoplastic CDIPs in the interactions of plants with filamentous pathogens has been controversial for a long time.

Over the past decades, tremendous progress has been made in understanding the biological functions of apoplastic CDIPs in filamentous oomycetes and fungi, such as their contribution to pathogen virulence and being recognized by plant cells. These findings have greatly enriched our knowledge on the roles of apoplastic CDIPs as virulence factors and how plants detect them and mount a defense response. In this review, we summarize the latest advances in identifying apoplastic CDIP effectors in plant pathogenic oomycetes and fungi, and our current understanding of the dual roles of apoplastic CDIPs in plant-filamentous pathogen interactions.

Apoplastic CDIPs Identified in Plant Pathogenic Oomycetes and Fungi

Apoplastic CDIPs Identified in Phytopathogenic Oomycetes

The purification and identification of extracellular proteins from phytopathogenic oomycetes that induce plant cell death began in the 1980s. Pernollet and colleagues purified three extracellular proteins, namely capsicein, cinnamomin and cryptogein, in culture filtrates of Phytophthora capsici, P. cinnamomi and P. cryptogea, respectively (Billard et al., 1988; Huet and Pernollet, 1989; Ricci et al., 1989). Determination of the amino acid sequences of these proteins led to definition of a novel protein family, called elicitins (Derevnina et al., 2016). Over the past decades, building on advances in molecular biology and genome sequencing, significant progress has been made in identifying extracellular proteins from phytopathogenic oomycetes that induce cell death in plants. To date, over 62 apoplastic CDIPs have been identified in 16 oomycete species (Table 1). While a few identified oomycete apoplastic CDIPs belong to PcF toxin, pectate lyase and glycoside hydrolase (GH) families or with no conserved domains, the majority are elicitins or Nep1 (necrosis- and ethylene-inducing peptide 1)-like proteins (NLPs) (Tables 1, 3).

Apoplastic CDIPs Identified in Phytopathogenic Fungi

Similarly, the availability of genome sequences of fungi has led to a rapid identification of apoplastic CIPDs from phytopathogenic fungi. To date, over 115 apoplastic CDIPs have been identified in 27 fungal species, including biotrophic, hemibiotrophic and necrotrophic pathogens (Table 2). The identified fungi apoplastic CDIPs include CFEM (common in fungal extracellular membrane)-containing proteins, cerato-platanin proteins (CPPs), GHs, NLPs, cutinases, and pectate lyases, and some proteins with other domains or with no conserved domains (Tables 2, 3). Among the identified oomycete and fungus apoplastic CDIPs, GHs, NLPs, Pectate lyases, and VmE02 homologues are widely distributed across oomycetes and fungi (Tables 1–3). On the other hand, many CDIPs are oomycete-specific or fungi-specific. For example, elicitins and elicitin-like proteins are unique to oomycetes, whereas CFEM-containing proteins and CPPs are unique to fungi (Table 3).

Major Protein Families of Oomycete and Fungus Apoplastic CDIPs

CFEM Containing CDIPs

The CFEM domain, which contains eight conserved cysteines, is unique to fungi (Kulkarni et al., 2003; Zhang Z. N. et al., 2015). CFEM was first identified in a M. oryzae MAC1-interacting protein, ACI1 (Kulkarni et al., 2003). CFEM containing proteins are widely distributed in fungi (Zhang Z. N. et al., 2015). While some of CFEM containing proteins have been identified to have prominent roles in pathogenicity or virulence, such as MoPth11 and its ortholog FGRRES_16221 in Magnaporthe oryzae and Fusarium graminearum, respectively (Kou et al., 2017; Dilks et al., 2019), and CgCcw14, CgMam3 in Candida glabrata (Srivastava et al., 2014), several CFEM containing proteins have been identified to possess cell death-inducing activity.

The CFEM-containing protein BcCFEM1 from Botrytis cinerea, contains a CFEM domain at the N-terminus, and a glycosylphosphatidylinositol (GPI) anchored site at the C-terminus. BcCFEM1 was induced and expressed at high levels during early stages of infection on bean leaves. Targeted disruption of the BcCFEM1 gene reduced virulence, conidiation and stress tolerance in B. cinerea. Transient expression of BcCFEM1 in Nicotiana benthamiana leaves triggered obvious chlorosis (Zhu et al., 2017b), suggesting the involvement of BcCFEM1 in eliciting plant responses.

The M. oryzae genome harbors 19 proteins with the CFEM domain (Kou et al., 2017). Two CFEM-containing proteins MoCDIP2 and MoCDIP11 have been identified to induce cell in the non-host N. benthamiana and host rice cells (Chen S. et al., 2013; Guo et al., 2019). MoCDIP2 contains a CFEM domain at the N-terminus, and a GPI-anchored site at the C-terminus, whereas MoCDIP11 contains only a CFEM domain at the N-terminus. Transient expression assays in rice protoplasts or N. benthamiana leaves revealed that the signal peptides that led the secretion of proteins, were required for cell death inducing activity of MoCDIP2 and MoCDIP11, indicating that both two effectors function in the apoplast (Chen S. et al., 2013; Guo et al., 2019).

CPP Family CIDPs

CPPs are small secreted cysteine-rich proteins that widely occur in filamentous fungi but not in bacteria, oomycetes, plants, or animals (Chen H. et al., 2013). CPPs have many aspects in common with expansins. Structural analysis revealed that CPPs have a double ψβ-barrel similar to the D1 domain of expansins (de Oliveira et al., 2011). Moreover, similar to expansins, CPPs possess properties to weaken cellulose (de O Barsottini et al., 2013; Baccelli et al., 2014b). Many CPPs have been shown to function as virulence factors in fungi, and on the other hand are able to induce cell death and elicit defense response in plants (Pazzagli et al., 2014).

The first CPP family CIDP, CP, was identified from the culture filtrates of Ceratocystis fimbriata f. sp. platani, the causal agent of the plane canker stain (Pazzagli et al., 1999). CP induced cell death in host and non-host plants, activated phytoalexin synthesis, pathogenesis-related (PR) gene expression, and mitogen-activated protein kinase (MAPK) phosphorylation, and triggered salicylic acid (SA) and ethylene (ET)-signaling pathways (Pazzagli et al., 1999; Scala et al., 2004; Baccelli et al., 2014a; Luti et al., 2016).

Till now, in addition to CP, 11 more CPP family CIDPs have been identified from different fungal pathogens (Table 2), such as BcSpl1 in B. cinerea (Frías et al., 2011, 2013), EPL1 in Colletotrichum falcatum (Ashwin et al., 2017), CgCP1 in Colletotrichum gloeosporioides (Wang W. et al., 2018), Pop1 in Ceratocystis populicola (Comparini et al., 2009), FgCPP2 in F. graminearum (Quarantin et al., 2016, 2019), FocCP1 in Fusarium oxysporum (Li et al., 2019a; Liu et al., 2019), HaCPL2 in Heterobasidion annosum sensu stricto (Chen et al., 2015), MoSM1/MSP1 (Jeong et al., 2007; Yang et al., 2009; Wang et al., 2016; Hong et al., 2017) in M. oryzae, MpCP1 in Moniliophthora perniciosa (Zaparoli et al., 2009), SsCP1 in Sclerotinia sclerotiorum (Yang et al., 2018b), and VdCP1 in Verticillium dahliae (Zhang et al., 2017a). Similar to CP, these 11 CPP family CIDPs induced strong necrosis and elicited defense responses in plants. For example, BcSpl1 induced strong necrosis, electrolyte leakage, cytoplasm shrinkage, and PR gene expression in plants including tomato, tobacco and Arabidopsis. In addition, BcSpl1 elicited systemic acquired resistance (SAR) in tobacco against Pseudomonas syringae and B. cinerea (Frías et al., 2011). The CPP family CIDPs possess similar biological properties as that of CP. For example, Pop1 and VdCP1 possessed chitin-binding properties (Baccelli et al., 2014b; Zhang et al., 2017a), and Pop1 and FgCPP2 exhibited the ability of loosening cellulose substrates and enhancing fungal cellulase activity in an expansin-like manner as well as CP (Baccelli et al., 2014b; Quarantin et al., 2016, 2019).

Elicitin and Elicitin-Like CDIPs

Elicitins are a family of small, highly conserved proteins secreted by Phytophthora and Pythium species (Derevnina et al., 2016). The first three elicitins, cryptogein, cinnamomin and capsicein were identified from the culture filtrates of P. cryptogea, P. cinnamomi and P. capsici, respectively (Billard et al., 1988; Huet and Pernollet, 1989; Ricci et al., 1989). Sequence analysis revealed that these elicitins share a conserved domain of 98 amino acids, which contains six cysteine residues at conserved positions forming three disulphide bridges (Boissy et al., 1996). Further studies revealed that elicitins are encoded by complex gene families (Kamoun et al., 1993; Panabieres et al., 1995; Jiang et al., 2006). In addition, Phytophthora and Pythium genomes contain a number of elicitin-like proteins possessing diverse, shorter or longer elicitin domains (Jiang et al., 2006).

Over 22 elicitin and elicitin-like CDIPs that induce cell death in certain plant species such as Nicotiana species and some Brassicaceae cultivars have been identified from different Phytophthora pathogens (Table 1). Among the elicitin and elicitin-like CDIPs, β-cryptogein and INF1 have been widely studied for their roles in the interactions of Phytophthora pathogens with plants. Cryptogein induced necrosis on tobacco leaves, triggered SAR and enhanced disease resistance in tobacco. Upon the SAR induction, the expression of the plant extracellular S-like RNase NE gene and its RNase activity were highly up-regulated, indicating that NE possibly associated with the cryptogein-induced SAR (Galiana et al., 1997). Cryptogein promoted the movement of plant respiratory burst oxidase homologues (RBOHs) from the Golgi cisternae to the plasma membrane, which may play a fundamental role for ROS production (Noirot et al., 2014). Cryptogein induced production of ROS, which was differentially regulated by the sphingolipid long-chain bases (LCBs) and their phosphorylated derivatives (LCB-Ps) in tobacco cells (Coursol et al., 2015). In addition, cryptogein induced production of NO, partly dependent on the ROS-dependent pathway, indicating that the defense responses induced by cryptogein involving interaction of the NO and ROS signaling pathways (Kulik et al., 2015). INF1 induced cell death on tobacco and potato leaves with the necrotic activity higher than that of other a-elicitins, such as cacto, parasiticein, capsicein and cryptogein, but less than that of β-cryptogein (Huet et al., 1994). INF1 induced the expression of chitinase, β-1,3-glucanase, phenylalanine ammonia-lyase (PAL), and PR1 genes, and rapid accumulation of H₂O₂ in tobacco (Sasabe et al., 2000; Huitema et al., 2005). INF1 induced the expression of NbrbohB in N. benthamiana, and silencing of NbrbohA or NbrbohB led to a reduction and delay of the necrotic reaction triggered by INF1 (Yoshioka et al., 2003), suggesting that INF1-induced cell death was dependent on the ROS burst.

Elicitins are able to bind sterols, phospholipids or fatty acids, and transport them between biological membranes (Mikes et al., 1997). However, the lipid-binding ability did not influence elicitin-induced response in tobacco. Investigations based on the mutant proteins of cryptogein with limited abilities to bind sterols revealed that induction of ROS synthesis, cytosol acidification and cell death in tobacco cells were not correlated with the sterol-binding abilities of the cryptogein proteins (Dokládal et al., 2012; Ptáčková et al., 2015).

Elicitins do not induce cell death in tomato plants. However, elicitins could induce immune responses in tomato, and enhance plant resistance against Phytophthora spp., bacterial wilt disease, and powdery mildew (Picard et al., 2000; Kawamura et al., 2009; Starý et al., 2019). INF1 induced the expression of jasmonic acid (JA)-responsive PR-6, LeATL6 and LOX-E, and ET-responsive PR-2b and ERF2, but not SA-responsive PR-1a and PR-2a in tomato leaves (Kawamura et al., 2009). Consistently, Starý et al. (2019) showed that cryptogein induced defense responses without cell death in tomato through JA- and ET-signaling pathways, but not SA-signaling pathway. These results indicated that elicitins triggered different signaling pathways between tobacco and tomato.

NLP Family CDIPs

NLP family proteins are characterized by the presence of a common NPP1 (necrosis-inducing Phytophthora protein) domain. This family is widely distributed across taxa including oomycetes, fungi, and bacteria (Gijzen and Nürnberger, 2006). The first NLP protein, namely Nep1, was identified from culture filtrates of F. oxysporum (Bailey, 1995), and has been shown to induce necrosis in plants, such as Erythroxylum coca, Theobroma cacao and Arabidopsis, with activating PR gene expression, ROS production and other general defense response (Bailey et al., 2005; Bae et al., 2006). To date, over 39 NLP family CDIPs have been identified in phytopathogenic oomycetes and fungi. Among them, 20 NLP family CDIPs were from phytopathogenic oomycetes (Table 1), and the remaining 19 NLP CDIPs were from phytopathogenic fungi (Table 2).

NLP family CDIPs have been confirmed to induce cell death in dicot but not monocot plants. Among the identified NLP family CDIPs, PpNLP/NLP_Pp, PsojNIP and PaNie₂₁₃/NLP_Pya have been extensively studied in the context of inducing cell death and immune responses in dicot plants. PpNLP/NLP_Pp induced necrosis in Arabidopsis, and activated PR genes expression, ROS production, callose apposition (Fellbrich et al., 2002), as well as the posttranslational expression of mitogen-activated protein kinase and production of nitric oxide and phytoalexin camalexin, suggesting dual roles of PpNLP/NLP_Pp as both toxin-like virulence factors and plant innate immunity triggers (Qutob et al., 2006). Determining and modeling of the structures of PaNie₂₁₃/NLP_Pya, PpNLP/NLP_Pp, and a PccNLP protein from the phytopathogenic bacterium Pectobacterium carotovorum, revealed that NLPs displayed identical toxin folds which contributed to host infection and plant defense gene activation, suggesting that a common fold of the cytolytic toxin is required for both pathogen virulence and plant immunity activation (Ottmann et al., 2009). Böhm et al. (2014) further identified and characterized a pattern of 20 amino acid residues (nlp20) of cytotoxic NLPs that triggered immunity associated plant defenses in certain dicot plants.

Based on the finding that NLPs display a striking similarity to cytolytic sphingomyelin-binding actinoporins (Ottmann et al., 2009), glycosylinositol phosphorylceramide (GIPC) sphingolipids in eudicot plants were further shown to be bound by NLPs. The inositol phosphorylceramide in GIPCs was covalently bound to glucuronic acid and variable terminal hexoses which were different between eudicots and monocots. Eudicot GPICs typically carried two terminal sugars (series A), while monocots GIPCs bore three terminal sugars (series B) (Cacas et al., 2013). The absence of series A GIPCs lead to insensitivity to NLPs of monocot plants. Consistently, Arabidopsis mutants with altered GIPC composition suffered less cell death than the wild type upon NLP infiltration (Lenarčič et al., 2017). These results thus explained host specificity of cell death induced by NLPs in eudicot plants (Van den Ackerveken, 2017).

Cell Wall-Degrading Enzyme Family CDIPs

Phytopathogenic oomycetes and fungi secrete a large amount of effector proteins related to plant cell wall degradation, such as enzymes to degrade cellulose, xylan, pectin, etc. (Kubicek et al., 2014). Certain cell wall-degrading enzymes (CWDEs) have been proved to be associated with pathogen virulence, and some induced cell death and trigged defense responses in plants. CWDE family CDIPs have been identified in carbohydrate esterase (CE5), glycoside hydrolase (GH) and polysaccharide lyase (PL) families (Tables 1–3).

With functions to degrade plant cuticle or suberin polymers, the CE family cutinases has been associated with important roles in filamentous pathogen-plant interactions. Two cutinase family CDIPs, SsCut1 and VdCUT11 have been identified in S. sclerotiorum and V. dahliae (Zhang H. et al., 2014; Gui et al., 2018), respectively. SsCut1 induced cell death in both dicot and monocot species and activated plant resistance against S. sclerotiorum, P. nicotianae and Phytophthora sojae (Zhang H. et al., 2014). Further, SsCut1-induced cell death along with stomatal closure, ROS burst and NO production, was suppressed by silencing of a C₂H₂-type zinc finger gene NbCZF1 in N. benthamiana, showing that SsCut1-triggered defense could be mediated by NbCZF1-ROS-NO pathway (Zhang et al., 2016). VdCUT11 induced cell death and defense responses in N. benthamiana, cotton, and tomato plants, and the enzymatic activity was required for its cell death-inducing activity (Gui et al., 2018).

GHs hydrolyze the glycosidic bond between carbohydrates or between a carbohydrate and a noncarbohydrate moiety through acid catalysis (Zhao et al., 2013). About 18 GH domain-containing CDIPs have been identified (Table 3). The GH family CDIPs induced cell death as well as defense responses in host and nonhost plants. For example, BcXyn11A induced ROS burst, electrolyte leakage, cytoplasm shrinkage and PR gene expression, and these effects were dependent on its short 25-residue peptide (Frías et al., 2019). BcXYG1 triggered pattern-triggered immunity (PTI) response and systemic resistance in bean (Zhu et al., 2017a). PsXEG1 induced disease resistance in N. benthamiana and soybean (Ma et al., 2015). BcGs1 induced systemic resistance in tobacco and tomato against B. cinerea, Phytophthora syringae and tobacco mosaic virus (Zhang Y. et al., 2015). Furthermore, BcGs1 triggered ROS burst, PAL and peroxidase (POD) enzyme activity, and lignin accumulation in tomato (Yang et al., 2018a). Many of the GH family CDIPs have been shown to possess hydrolase activity. While hydrolase activity of BcPG2 was required for its cell death induction (Kars et al., 2005), the enzymatic activity of most identified GH family CDIPs was not necessary for cell death inducing activity. For example, the cell death inducing activity of Xyn11A, PsXEG1, BcXYG1, VdEG1 and VdEG3 was independent of their enzymatic activity (Brito et al., 2006; Ma et al., 2015; Gui et al., 2017; Zhu et al., 2017a).

The PL family pectate lyases play a critical role in pectin degradation. Four pectate lyases PcPL1, PcPL15, PcPL16 and PcPL20 in P. capsici, and one pectate lyase VdPEL1 in V. dahliae have been identified to have cell death inducing activity in plants (Fu et al., 2015; Yang et al., 2018d). PcPL1, PcPL15, PcPL16 and PcPL20 were highly expressed in P. capsici during infection of pepper, and transient expression of the four PcPLs induced severe cell death in pepper leaves (Fu et al., 2015). VdPEL1 induced cell death in N. benthamiana, tomato, soybean and cotton, and triggered defense responses and systemic resistance to B. cinerea and V. dahliae in N. benthamiana and cotton plants. Furthermore, the enzymatic activity was found to be necessary for cell death-inducing activity (Yang et al., 2018d).

Besides, a SGNH hydrolase subfamily protein BcXyl1 was identified to induce cell death in N. benthamiana, tomato, soybean and cotton (Yang et al., 2018c). BcXyl1 exhibited xylanase activity, but its cell death inducing activity was independent of the enzymatic activity. BcXyl1 triggered plant PTI responses with a pattern of 26-amino acid peptide.

CDIP Families With Other Conserved Domains or Without Conserved Domain

Besides the above-mentioned CDIP families, a number of apoplastic CDIPs contain other conserved domains or no conserved domain (Tables 1, 2), indicating the incredible diversity of apoplastic CDIPs secreted by oomycetes and fungi. On the other hand, many of these apoplastic CDIPs are widely distributed across microbial taxa or different pathogen species and the homologs can induce cell death and defense responses in different plant species, indicating that recognition of these proteins is evolutionarily conserved. For example, the Valsa mali small cysteine-rich protein VmE02 induces cell death in N. benthamiana, tomato, pepper, Arabidopsis and apple and enhances resistance in N. benthamiana against S. sclerotiorum and P. capsic (Nie J. et al., 2019). VmE02 is widely conserved across oomycete and fungal species, and the homologs can induce cell death in N. benthamiana. Similarly, the Colletotrichum orbiculare NIS1 and its homologs from Colletotrichum higginsianum and Fusarium virguliforme (Yoshino et al., 2012; Chang et al., 2016), and the Rhynchosporium commune RcCDI1 and its homologues from M. oryzae, Neurospora crassa and Zymoseptoria tritici (Franco-Orozco et al., 2017), induced cell death in N. benthamiana. These results clearly supported that, although the physiological properties remain unknown, these apoplastic CDIPs are recognized as conserved patterns that induce defense responses in plants.

Apoplastic CDIPs Contribute to Pathogen Virulence

Phytopathogenic oomycetes and fungi initially colonize in the plant apoplast or extracellular space, and subsequently penetrate host cells. Therefore, the apoplastic effectors secreted by oomycetes and fungi are likely the primary weapons of filamentous plant pathogens. Despite the diversity of lifestyles as biotrophic, hemibiotrophic or necrotrophic, filamentous oomycetes and fungi secrete a high number of apoplastic CDIPs. Biotrophic pathogens feed on living plant cells (Giraldo and Valent, 2013). Whether apoplastic CDIPs of biotrophic pathogens actually cause plant cell death or function as important virulence factors during a natural infection remain to be determined (Tables 1, 2). In contrast, necrotrophic pathogens thrive on dead host tissues and take advantage of CDIP-triggered plant cell death. For example, NLP-triggered necrosis could aid infection by necrotrophic pathogens (Van den Ackerveken, 2017). Hemibiotrophic pathogens combine a biotrophic phase in early stages with a necrotrophic phage during later infection stages. Many apoplastic CDIPs of hemibiotrophic pathogens have been found to be highly expressed at late infection stages, suggesting that they contribute to the necrotrophic growth of hemibiotrophic pathogens (Qutob et al., 2002; Kelley et al., 2010).

Functional analysis based on overexpression, deletion or silencing of genes encoding apoplastic CDIPs have functionally proved many of them as important virulence factors in hemibiotrophic and necrotrophic pathogens (Tables 1, 2). Among the 62 identified oomycete apoplastic CDIPs, 12 have been proven to function as virulence factors that are required for pathogenicity or contribute to virulence. The P. cactorum SCR96 belongs to the PcF toxin family. Silencing of the scr96 gene in Phytophthora cactorum caused loss of pathogenicity on host plants, indicating that SCR96 is required for pathogenicity (Chen et al., 2016). In P. capsici, silencing of the genes encoding NLP-like proteins PcNLP2, PcNLP6 or PcNLP14, and the genes encoding pectate lyases PcPL1, PcPL15, PcPL16 or PcPL20 caused significantly reduced virulence on pepper (Feng et al., 2014; Fu et al., 2015), demonstrating the important roles of these apoplastic CDIPs in pathogen virulence. In Phytophthora palmivora, three fractions isolated from culture filtrates including high-molecular-weight glycoprotein, broad-molecular-weight glycoprotein and 42-kDa glycoprotein were observed to promote P. palmivora infection of rubber tree leaves (Pettongkhao and Churngchow, 2019). However, the virulence role of these three glycoproteins remains to be genetically confirmed. The P. sojae XEG1, a GH12 family CDIP, functions as a major virulence factor during infection. Both silencing and overexpression of the PsXEG1 gene in P. sojae severely impaired virulence (Ma et al., 2015). Interestingly, P. sojae also secretes a PsXLP1 (PsXEG1-like) apoplastic effector with a truncated GH12 domain functioning as a decoy to shield XEG1-mediated virulence (Ma et al., 2017).

Among the 115 identified fungi apoplastic CDIPs, 16 have been proven to be required for pathogenicity or contribute to virulence of both hemibiotrophic and necrotrophic pathogens. In B. cinerea, targeted deletion of the genes encoding BcCFEM1 (Zhu et al., 2017b), BcSpl1 (Frías et al., 2011), BcXyl1 (Yang et al., 2018c), or BcXyn11A (Brito et al., 2006) caused severely compromised virulence, suggesting that these CDIPs were important virulence factors of B. cinerea. Overexpression and deletion of BcXYG1 did not significantly affect B. cinerea infection on bean leaves. However, the BcXYG1 overexpression strains produced significantly earlier and more intense local necrosis, suggesting that BcXYG1 contributes to the establishment of infection in early stages (Zhu et al., 2017a). The C. gloeosporioides CgCP1 belongs to the CPP family. Knock-out of CgCP1 in C. gloeosporioides significantly reduced infection on rubber tree leaves (Wang W. et al., 2018). Similar to BcSpl1 and CgCP1, the CPP family CIDPs FocCP1, SsCP1 and VdCP1 function as important virulence factors. Deletion of FocCP1 in F. oxysporum (Liu et al., 2019), SsCP1 in S. sclerotiorum (Yang et al., 2018b), or VdCP1 in V. dahliae (Zhang et al., 2017a) caused significantly reduced virulence of pathogens on hosts banana, Arabidopsis or cotton, respectively. In M. oryzae, deletion of mohrip1, or mohrip2 remarkably compromised fungal virulence on rice (Nie H. et al., 2019; Nie H. Z. et al., 2019). MoHrip1 belongs to the Alt a 1 (AA1) family (Zhang et al., 2017b). Similarly, the V. dahliae PevD1, an AA1 family CDIP, is required for full virulence of V. dahliae on hosts (Zhang et al., 2019). In addition to VdCP1 and PevD1, VdCUT11, VdEG1, VdEG3, VdNLP1, VdNLP2, and VdPEL1 have been shown to play important roles in virulence of V. dahliae. Targeted deletion of VdCUT11 (Gui et al., 2018), VdEG1, VdEG3 (Gui et al., 2017), or VdPEL1 (Yang et al., 2018d) significantly compromised virulence of V. dahliae on cotton plants. Interestingly, while both VdNLP1 and VdNLP2 appear to be dispensable for V. dahliae infection in cotton plants (Zhou et al., 2012), VdNLP1 as well as VdNLP2 deletion strains were found to be significantly less pathogenic on tomato and Arabidopsis (Santhanam et al., 2013), demonstrating the functional diversification of the two NLP family CDIPs in virulence of V. dahliae.

Pathogenicity assays also revealed that many apoplastic CDIPs were not required for fungal pathogenicity or virulence. Targeted deletion of the genes encoding these proteins did not impair the virulence of pathogens (Table 2). One possibility why these apoplastic CDIPs were dispensable for virulence could be due to the functional redundancy with other apoplastic effectors (Yoshino et al., 2012; Guo et al., 2019).

Recognition of Apoplastic CDIPs in Plants: Cell Surface Receptors and Downstream Components

In recent years, there have been breakthroughs in the identification of cell surface receptors recognizing apoplastic CDIPs. By screening T-DNA insertion mutants and natural accessions of Arabidopsis, Albert et al. (2015) identified T-DNA insertion alleles of RLP23 and Arabidopsis accessions carrying a frameshift mutation of RLP23 that were insensitive to the conserved nlp20 pattern found in most NLPs. RLP23 encodes a leucine-rich repeat-receptor-like protein (LRR-RLP), which binds extracellularly to nlp20, thereby mediating NLP-elicited immune response in Arabidopsis (Albert et al., 2015). Transgenic potato plants expressing RLP23 displayed enhanced resistance to oomycete and fungal pathogens, such as P. infestans and S. sclerotiorum (Albert et al., 2015), further supporting that RLP23 confers protection to oomycete and fungal pathogens. More recently, RXEG1 (Response to XEG1), an LRR-RLP that specifically recognizes the GH12 family CDIP XEG1, has been identified from N. benthamiana through a high-throughput virus-induced gene silencing (VIGS) screen (Wang Y. et al., 2018). RXEG1 interacts with XEG1 by the extracellular LRR domain in the apoplast, and regulates XEG1-induced plant cell death and immune responses.

Using a genetic mapping approach, an ELR (elicitin response) gene has been identified from a population derived from the cross of Solanum microdontum genotype mcd360-1 (responds to INF1 with a cell death response) with S. microdontum ssp. gigantophyllum gig714-1 (does not respond to INF1) (Du et al., 2015). ELR encodes an LRR-RLP, and ELR mediates extracellular recognition of a broad range of elicitins exhibiting relatively low sequence similarity, suggesting that ELR recognizes elicitins most likely based on domain similarity but not a small conserved peptide. Moreover, cultivated potato transformed with the ELR gene exhibited enhanced resistance to Phytophthora infestans. Overall, the results suggested ELR as a potential cell surface receptor to mediate response to elicitins. However, the physical association of ELR with INF proteins remains unclear (Du et al., 2015). Interestingly, two intracellular proteins, a lectin-like receptor kinase (NbLRK) and a pepper calcium-binding protein (SRC2-1), have been shown to interact with P. infestans INF1 (Kanzaki et al., 2008) and P. capsici PcINF1 (Liu et al., 2015), and mediate P. infestans INF1 or PcINF1-induced cell death, respectively. These results correspond with the speculation that elicitins could be possibly transported into plant cells through clathrin-mediated endocytosis (Leborgne-Castel et al., 2008). Hence, it would appear that plants possess multiple mechanisms to recognize elicitins.

The three cell surface receptors RLP23, ELR and RXEG1 have extracellular LRRs but lack a cytoplasmic signaling domain. Two LRR receptor-like kinases (LRR-RLKs) SUPPRESSOR OF BIR1-1 (SOBIR1) and/or BRI1-ASSOCIATED KINASE-1/SOMATIC EMBRYOGENESIS RECEPTOR KINASE-3 (BAK1/SERK3) were shown to be essential for RLP23, ELR or RXEG1-induced cell death and immune responses that act as co-receptors to transduce signals to downstream elements. RLP23 forms a complex with SOBIR1 and recruits BAK1/SERK3 into a tripartite complex upon ligand binding (Albert et al., 2015); ELR associates with BAK1/SERK3 and mediates recognition of diverse elicitins from Phytophthora species (Du et al., 2015); RXEG1 associates with BAK1/SERK3 and SOBIR1 to transmit the XEG1-induced defense signal (Wang Y. et al., 2018).

BAK1/SERK3 and SOBIR1 appear to be general and central regulators of plant cell death and defense response induced by diverse apoplastic CDIPs besides nlp20, INF1 and XEG1. In Arabidopsis, bak1 mutants showed a significantly reduced sensitivity to the CPP family CIDP BcSpl1, indicating that BAK1 plays an important role in the perception of BcSpl1 (Frías et al., 2011). In N. benthamiana, VIGS-mediated silencing of BAK1 or SOBIR1, resulted in significant reductions of cell death induced by a number of apoplastic CDIPs, including BcXYG1 (Zhu et al., 2017a), BcXyl1 (Yang et al., 2018c), RcCD1 (Franco-Orozco et al., 2017), VdCUT11 (Gui et al., 2018), VdEG1, VdEG3 (Gui et al., 2017), VmE02 (Nie J. et al., 2019), MgNLP, Zt9, Zt11 or Zt12 (Kettles et al., 2017). These results indicate that BAK1/SERK3 and SOBIR1 are required for apoplastic CDIP-induced cell death.

Several cytosolic, or nucleo-cytoplasmic regulators have been shown to be important components in apoplastic CDIP-induced cell death and defense signal transduction pathways downstream of the cell surface receptor complexes. The ubiquitin ligase–associated protein SGT1 functions as a conserved component in both PTI and effector-triggered immunity (ETI) pathways. Silencing of SGT1 in N. benthamiana suppressed cell death induced by P. capsici PcINF1 (Liu Z. Q. et al., 2016), INF1, INF2A (Huitema et al., 2005), PiNPP1.1, PsojNIP (Kanneganti et al., 2006), BcSpl1 (Frías et al., 2011), NIS1 (Yoshino et al., 2012), NcCDI1 (Franco-Orozco et al., 2017), or VmE02 (Nie J. et al., 2019). In addition, VIGS-mediated silencing analysis revealed that HSP70, HSP90 (Kanzaki et al., 2003; Kanneganti et al., 2006; Yoshino et al., 2012; Nie J. et al., 2019), COI1, MEK2, NPR1, TGA2.2 (Kanneganti et al., 2006), and Avr9/Cf-9-INDUCED F-BOX1 (ACIF1) (Li et al., 2019c) were required for cell death induced by certain apoplastic CDIPs.

Concluding Remarks and Perspectives

An emerging number of studies have shown that many apoplastic CDIPs are required for pathogenicity, or contribute to the virulence of hemibiotrophic and necrotrophic pathogens, demonstrating the important role of these apoplastic CDIPs as essential virulence factors. On the contrary, apoplastic CDIPs were shown to elicit plant defense responses. Over the past decades, studies have documented that many apoplastic CDIPs are recognized by plants as PAMPs, being able to trigger PR gene expression, phytoalexin synthesis, MAPK phosphorylation, SA-, JA/ET-signaling pathways, as well as resistance against pathogens. The recent findings of extracellular recognition of NLPs, elicitins and XEG1 by plant RLPs, RLP23, ELR and RXEG1 (Albert et al., 2015; Du et al., 2015; Wang Y. et al., 2018), respectively, have greatly advanced our understanding of the roles of apoplastic CDIPs in plant-pathogen interactions. More importantly, the identification of receptors for apoplastic CDIPs provides valuable gene resources for engineering crops with broad and durable disease resistance (Albert et al., 2015; Du et al., 2015).

Currently, the majority of apoplastic CDIPs have been characterized based on demonstrations in dicot plants, especially based on transient expression in N. benthamiana, even many apoplastic CDIPs were identified from monocot pathogens. Particularly, recognition receptors and downstream components that have been identified remain restricted to dicot plants. Given the paramount importance of monocot cereal plants, such as rice, wheat and maize, as staple crops, it would be important to determine recognition of apoplastic CDIPs in monocot hosts, which could help engineer monocot cereal crops with broad-spectrum resistance against filamentous pathogens.

References

• 1

  AlbertI.BöhmH.AlbertM.FeilerC. E.ImkampeJ.WallmerothN.et al (2015). An RLP23-SOBIR1-BAK1 complex mediates NLP-triggered immunity.Nat. Plants1:15140. 10.1038/nplants.2015.140

  • Pubmed Abstract
  • CrossRef
  • Google Scholar

• 2

  AmaroT. M. M. M.ThilliezG. J. A.MotionG. B.HuitemaE. (2017). A perspective on CRN proteins in the genomics age: evolution, classification, delivery and function revisited.Front. Plant Sci.8:99. 10.3389/fpls.2017.00099

  • Pubmed Abstract
  • CrossRef
  • Google Scholar

• 3

  AndersonJ. P.SperschneiderJ.WinJ.KiddB.YoshidaK.HaneJ.et al (2017). Comparative secretome analysis of Rhizoctonia solani isolates with different host ranges reveals unique secretomes and cell death inducing effectors.Sci. Rep.7:10410. 10.1038/s41598-017-10405-y

  • Pubmed Abstract
  • CrossRef
  • Google Scholar

• 4

  ArenasY. C.KalkmanE. R.SchoutenA.DiehoM.VredenbregtP.UwumukizaB.et al (2010). Functional analysis and mode of action of phytotoxic Nep1-like proteins of Botrytis cinerea.Physiol. Mol. Plant Pathol.74376–386. 10.1016/j.pmpp.2010.06.003

  • CrossRef
  • Google Scholar

• 5

  AshwinN. M. R.BarnabasL.Ramesh SundarA.MalathiP.ViswanathanR.MasiA.et al (2017). Comparative secretome analysis of Colletotrichum falcatum identifies a cerato-platanin protein (EPL1) as a potential pathogen-associated molecular pattern (PAMP) inducing systemic resistance in sugarcane.J. Proteomics1692–20. 10.1016/j.jprot.2017.05.020

  • Pubmed Abstract
  • CrossRef
  • Google Scholar

• 6

  AshwinN. M. R.BarnabasL.Ramesh SundarA.MalathiP.ViswanathanR.MasiA.et al (2018). CfPDIP1, a novel secreted protein of Colletotrichum falcatum, elicits defense responses in sugarcane and triggers hypersensitive response in tobacco.Appl. Microbiol. Biotechnol.1026001–6021. 10.1007/s00253-018-9009-2

  • Pubmed Abstract
  • CrossRef
  • Google Scholar

• 7

  BaccelliI.LombardiL.LutiS.BernardiR.PicciarelliP.ScalaA.et al (2014a). Cerato-platanin induces resistance in Arabidopsis leaves through stomatal perception, overexpression of salicylic acid- and ethylene-signalling genes and camalexin biosynthesis.PLoS One9:e100959. 10.1371/journal.pone.0100959

  • Pubmed Abstract
  • CrossRef
  • Google Scholar

• 8

  BaccelliI.LutiS.BernardiR.ScalaA.PazzagliL. (2014b). Cerato-platanin shows expansin-like activity on cellulosic materials.Appl. Microbiol. Biotechnol.98175–184. 10.1007/s00253-013-4822-0

  • Pubmed Abstract
  • CrossRef
  • Google Scholar

• 9

  BaeH.KimM. S.SicherR. C.BaeH. J.BaileyB. A. (2006). Necrosis-and ethylene-inducing peptide from Fusarium oxysporum induces a complex cascade of transcripts associated with signal transduction and cell death in Arabidopsis.Plant Physiol.1411056–1067. 10.1104/pp.106.076869

  • Pubmed Abstract
  • CrossRef
  • Google Scholar

• 10

  BaileyB. A. (1995). Purification of a protein from culture filtrates of Fusarium oxysporum that induces ethylene and necrosis in leaves of Erythroxylum coca.Phytopathology851250–1255. 10.1094/Phyto-85-1250

  • CrossRef
  • Google Scholar

• 11

  BaileyB. A.Apel-BirkholdP. C.AkingbeO. O.RyanJ. L.O’NeillN. R.AndersonJ. D. (2000). Nep1 Protein from Fusarium oxysporum Enhances Biological Control of Opium Poppy by Pleospora papaveracea.Phytopathology90812–818. 10.1094/PHYTO.2000.90.8.812

  • Pubmed Abstract
  • CrossRef
  • Google Scholar

• 12

  BaileyB.Apel-BirkholdP. C.LusterD. G. (2002). Expression of NEP1 by Fusarium oxysporum f. sp. erythroxyli after gene replacement and overexpression using polyethylene glycol-mediated transformation.Phytopathology92833–841. 10.1094/PHYTO.2002.92.8.833

  • Pubmed Abstract
  • CrossRef
  • Google Scholar

• 13

  BaileyB. A.BaeH.StremM. D.De MayoloG. A.GuiltinanM. J.VericaJ. A.et al (2005). Developmental expression of stress response genes in Theobroma cacao leaves and their response to Nep1 treatment and a compatible infection by Phytophthora megakarya.Plant Physiol. Biochem.43611–622. 10.1016/j.plaphy.2005.04.006

  • Pubmed Abstract
  • CrossRef
  • Google Scholar

• 14

  BaillieulF.de RuffrayP.KauffmannS. (2003). Molecular cloning and biological activity of α-, β-, and γ-megaspermin, three elicitins secreted by Phytophthora megasperma H20.Plant Physiol.131155–166. 10.1104/pp.012658

  • Pubmed Abstract
  • CrossRef
  • Google Scholar

• 15

  BaillieulF.GenetetI.KoppM.SaindrenanP.FritigB.KauffmannS. (1995). A new elicitor of the hypersensitive response in tobacco: a fungal glycoprotein elicits cell death, expression of defence genes, production of salicylic acid, and induction of systemic acquired resistance.Plant J.8551–560. 10.1046/j.1365-313X.1995.8040551.x

  • Pubmed Abstract
  • CrossRef
  • Google Scholar

• 16

  BarM.SharfmanM.RonM.AvniA. (2010). BAK1 is required for the attenuation of ethylene-inducing xylanase (Eix)-induced defense responses by the decoy receptor LeEix1.Plant J.63791–800. 10.1111/j.1365-313X.2010.04282.x

  • Pubmed Abstract
  • CrossRef
  • Google Scholar

• 17

  BillardV.BruneteauM.BonnetP.RicciP.PernolletJ.HuetJ.et al (1988). Chromatographic purification and characterization of elicitors of necrosis on tobacco produced by incompatible Phytophthora species.J. Chromatogr. A44087–94. 10.1016/s0021-9673(00)94513-8

  • CrossRef
  • Google Scholar

• 18

  BöhmH.AlbertI.OomeS.RaaymakersT. M.Van den AckervekenG.NürnbergerT. (2014). A conserved peptide pattern from a widespread microbial virulence factor triggers pattern-induced immunity in Arabidopsis.PLoS Pathog.10:e1004491. 10.1371/journal.ppat.1004491

  • Pubmed Abstract
  • CrossRef
  • Google Scholar

• 19

  BoissyG.de La FortelleE.KahnR.HuetJ. C.BricogneG.PernolletJ. C.et al (1996). Crystal structure of a fungal elicitor secreted by Phytophthora cryptogea, a member of a novel class of plant necrotic proteins.Structure41429–1439. 10.1016/s0969-2126(96)00150-5

  • CrossRef
  • Google Scholar

• 20

  BoudartG.CharpentierM.LafitteC.MartinezY.JauneauA.GaulinE.et al (2003). Elicitor activity of a fungal endopolygalacturonase in tobacco requires a functional catalytic site and cell wall localization.Plant Physiol.13193–101. 10.1104/pp.011585

  • Pubmed Abstract
  • CrossRef
  • Google Scholar

• 21

  BritoN.EspinoJ. J.GonzálezC. (2006). The endo-β-1, 4-xylanase Xyn11A is required for virulence in Botrytis cinerea.Mol. Plant Microbe Interact.1925–32. 10.1094/MPMI-19-0025

  • Pubmed Abstract
  • CrossRef
  • Google Scholar

• 22

  BuB.QiuD.ZengH.GuoL.YuanJ.YangX. (2014). A fungal protein elicitor PevD1 induces Verticillium wilt resistance in cotton.Plant Cell Rep.33461–470. 10.1007/s00299-013-1546-7

  • Pubmed Abstract
  • CrossRef
  • Google Scholar

• 23

  CacasJ. L.BureC.FurtF.MaaloufJ. P.BadocA.CluzetS.et al (2013). Biochemical survey of the polar head of plant glycosylinositolphosphoceramides unravels broad diversity.Phytochemistry96191–200. 10.1016/j.phytochem.2013.08.002

  • Pubmed Abstract
  • CrossRef
  • Google Scholar

• 24

  CapassoR.CristinzioG.Di MaroA.FerrantiP.ParenteA. (2001). Syringicin, a new α-elicitin from an isolate of Phytophthora syringae, pathogenic to citrus fruit.Phytochemistry58257–262. 10.1016/s0031-9422(01)00201-1

  • CrossRef
  • Google Scholar

• 25

  CapassoR.CristinzioG.EvidenteA.ViscaC.FerrantiP.BlancoF. D. V.et al (1999). Elicitin 172 from an isolate of Phytophthora nicotianae pathogenic to tomato.Phytochemistry50703–709. 10.1016/s0031-9422(98)00539-1

  • CrossRef
  • Google Scholar

• 26

  CapassoR.Di MaroA.CristinzioG.De MartinoA.ChamberyA.DanieleA.et al (2008). Isolation, characterization and structure-elicitor activity relationships of hibernalin and its two oxidized forms from Phytophthora hibernalis Carne 1925.J. Biochem.143131–141. 10.1093/jb/mvm201

  • Pubmed Abstract
  • CrossRef
  • Google Scholar

• 27

  ChangH. X.DomierL. L.RadwanO.YendrekC. R.HudsonM. E.HartmanG. L. (2016). Identification of multiple phytotoxins produced by Fusarium virguliforme Including a phytotoxic effector (FvNIS1) associated with sudden death syndrome foliar symptoms.Mol. Plant Microbe Interact.2996–108. 10.1094/MPMI-09-15-0219-R

  • Pubmed Abstract
  • CrossRef
  • Google Scholar

• 28

  ChangY. H.YanH. Z.LiouR. F. (2015). A novel elicitor protein from Phytophthora parasitica induces plant basal immunity and systemic acquired resistance.Mol. Plant Pathol.16123–136. 10.1111/mpp.12166

  • Pubmed Abstract
  • CrossRef
  • Google Scholar

• 29

  ChenH.KovalchukA.KeriöS.AsiegbuF. O. (2013). Distribution and bioinformatic analysis of the cerato-platanin protein family in Dikarya.Mycologia1051479–1488.

  • Google Scholar

• 30

  ChenH.QuintanaJ.KovalchukA.UbhayasekeraW.AsiegbuF. O. (2015). A cerato-platanin-like protein HaCPL2 from Heterobasidion annosum sensu stricto induces cell death in Nicotiana tabacum and Pinus sylvestris.Fungal Genet. Biol.8441–51. 10.1016/j.fgb.2015.09.007

  • Pubmed Abstract
  • CrossRef
  • Google Scholar

• 31

  ChenM.ZengH.QiuD.GuoL.YangX.ShiH.et al (2012). Purification and characterization of a novel hypersensitive response-inducing elicitor from Magnaporthe oryzae that triggers defense response in rice.PLoS One7:e37654. 10.1371/journal.pone.0037654

  • Pubmed Abstract
  • CrossRef
  • Google Scholar

• 32

  ChenM.ZhangC.ZiQ.QiuD.LiuW.ZengH. (2014). A novel elicitor identified from Magnaporthe oryzae triggers defense responses in tobacco and rice.Plant Cell Rep.331865–1879. 10.1007/s00299-014-1663-y

  • Pubmed Abstract
  • CrossRef
  • Google Scholar

• 33

  ChenQ.ChenZ.LuL.JinH.SunL.YuQ.et al (2013). Interaction between abscisic acid and nitric oxide in PB90-induced catharanthine biosynthesis of catharanthus roseus cell suspension cultures.Biotechnol. Prog.29994–1001. 10.1002/btpr.1738

  • Pubmed Abstract
  • CrossRef
  • Google Scholar

• 34

  ChenS.SongkumarnP.VenuR.GowdaM.BellizziM.HuJ.et al (2013). Identification and characterization of in planta–expressed secreted effector proteins from Magnaporthe oryzae that induce cell death in rice.Mol. Plant Microbe Interact26191–202.

  • Google Scholar

• 35

  ChenX. R.HuangS. X.ZhangY.ShengG. L.LiY. P.ZhuF. (2018). Identification and functional analysis of the NLP-encoding genes from the phytopathogenic oomycete Phytophthora capsici.Mol. Genet. Genomics293931–943. 10.1007/s00438-018-1432-7

  • Pubmed Abstract
  • CrossRef
  • Google Scholar

• 36

  ChenX. R.HuangS. X.ZhangY.ShengG. L.ZhangB. Y.LiQ. Y.et al (2017). Transcription profiling and identification of infection-related genes in Phytophthora cactorum.Mol. Genet. Genomics293541–555. 10.1007/s00438-017-1400-7

  • Pubmed Abstract
  • CrossRef
  • Google Scholar

• 37

  ChenX. R.LiY. P.LiQ. Y.XingY. P.LiuB. B.TongY. H.et al (2016). SCR96, a small cysteine-rich secretory protein of Phytophthora cactorum, can trigger cell death in the Solanaceae and is important for pathogenicity and oxidative stress tolerance.Mol. Plant Pathol.17577–587. 10.1111/mpp.12303

  • Pubmed Abstract
  • CrossRef
  • Google Scholar

• 38

  ChenX. R.ZhangB. Y.XingY. P.LiQ. Y.LiY. P.TongY. H.et al (2014). Transcriptomic analysis of the phytopathogenic oomycete Phytophthora cactorum provides insights into infection-related effectors.BMC Genomics15:980. 10.1186/1471-2164-15-980

  • Pubmed Abstract
  • CrossRef
  • Google Scholar

• 39

  ChurngchowN.RattarasarnM. (2000). The elicitin secreted by Phytophthora palmivora, a rubber tree pathogen.Phytochemistry5433–38. 10.1016/S0031-9422(99)00530-0

  • CrossRef
  • Google Scholar

• 40

  CobosR.Calvo-PenaC.Alvarez-PerezJ. M.IbanezA.Diez-GalanA.Gonzalez-GarciaS.et al (2019). Necrotic and cytolytic activity on grapevine leaves produced by Nep1-like proteins of Diplodia seriata.Front. Plant Sci.10:1282. 10.3389/fpls.2019.01282

  • Pubmed Abstract
  • CrossRef
  • Google Scholar

• 41

  CompariniC.CarresiL.PagniE.SbranaF.SebastianiF.LuchiN.et al (2009). New proteins orthologous to cerato-platanin in various Ceratocystis species and the purification and characterization of cerato-populin from Ceratocystis populicola.Appl. Microbiol. Biotechnol.84309–322. 10.1007/s00253-009-1998-4

  • Pubmed Abstract
  • CrossRef
  • Google Scholar

• 42

  CoursolS.FromentinJ.NoirotE.BričreC.RobertF.MorelJ.et al (2015). Long-chain bases and their phosphorylated derivatives differentially regulate cryptogein-induced production of reactive oxygen species in tobacco (Nicotiana tabacum) BY-2 cells.New Phytol.2051239–1249. 10.1111/nph.13094

  • Pubmed Abstract
  • CrossRef
  • Google Scholar

• 43

  DagvadorjB.OzketenA. C.AndacA.DugganC.BozkurtT. O.AkkayaM. S. (2017). A Puccinia striiformis f. sp. tritici secreted protein activates plant immunity at the cell surface.Sci. Rep.7:1141. 10.1038/s41598-017-01100-z

  • Pubmed Abstract
  • CrossRef
  • Google Scholar

• 44

  de O BarsottiniM. R.de OliveiraJ. F.AdamoskiD.TeixeiraP. J. P. L.do PradoP. F. V.TiezziH. O.et al (2013). Functional diversification of cerato-platanins in Moniliophthora perniciosa as seen by differential expression and protein function specialization.Mol. Plant Microbe Interact.261281–1293. 10.1094/MPMI-05-13-0148-R

  • Pubmed Abstract
  • CrossRef
  • Google Scholar

• 45

  de OliveiraA. L.GalloM.PazzagliL.BenedettiC. E.CappugiG.ScalaA.et al (2011). The structure of the elicitor cerato-platanin (CP), the first member of the CP fungal protein family, reveals a double ψβ-barrel fold and carbohydrate binding.J. Biol. Chem.28617560–17568. 10.1074/jbc.M111.223644

  • Pubmed Abstract
  • CrossRef
  • Google Scholar

• 46

  DerevninaL.DagdasY. F.De la ConcepcionJ. C.BialasA.KellnerR.PetreB.et al (2016). Nine things to know about elicitins.New Phytol.212888–895. 10.1111/nph.14137

  • Pubmed Abstract
  • CrossRef
  • Google Scholar

• 47

  DilksT.HalseyK.De VosR. P.Hammond-KosackK. E.BrownN. A. (2019). Non-canonical fungal G-protein coupled receptors promote Fusarium head blight on wheat.PLoS Pathog.15:e1007666. 10.1371/journal.ppat.1007666

  • Pubmed Abstract
  • CrossRef
  • Google Scholar

• 48

  DokládalL.OborilM.StejskalK.ZdráhalZ.PtáckováN.ChaloupkováR.et al (2012). Physiological and proteomic approaches to evaluate the role of sterol binding in elicitin-induced resistance.J. Exp. Bot.632203–2215. 10.1093/jxb/err427

  • Pubmed Abstract
  • CrossRef
  • Google Scholar

• 49

  DouD.ZhouJ. M. (2012). Phytopathogen effectors subverting host immunity: different foes, similar battleground.Cell Host Microbe12484–495. 10.1016/j.chom.2012.09.003

  • Pubmed Abstract
  • CrossRef
  • Google Scholar

• 50

  DuJ.VerzauxE.Chaparro-GarciaA.BijsterboschG.KeizerL. C.ZhouJ.et al (2015). Elicitin recognition confers enhanced resistance to Phytophthora infestans in potato.Nat. Plants1:15034. 10.1038/nplants.2015.34

  • Pubmed Abstract
  • CrossRef
  • Google Scholar

• 51

  EllisJ. G.RafiqiM.GanP.ChakrabartiA.DoddsP. N. (2009). Recent progress in discovery and functional analysis of effector proteins of fungal and oomycete plant pathogens.Curr. Opin. Plant. Biol.12399–405. 10.1016/j.pbi.2009.05.004

  • Pubmed Abstract
  • CrossRef
  • Google Scholar

• 52

  FangA.HanY.ZhangN.ZhangM.LiuL.LiS.et al (2016). Identification and characterization of plant cell death-inducing secreted proteins from Ustilaginoidea virens.Mol. Plant Microbe Interact.29405–416. 10.1094/MPMI-09-15-0200-R

  • Pubmed Abstract
  • CrossRef
  • Google Scholar

• 53

  FangY. L.PengY. L.FanJ. (2017). The Nep1-like protein family of Magnaporthe oryzae is dispensable for the infection of rice plants.Sci. Rep.7:4372. 10.1038/s41598-017-04430-0

  • Pubmed Abstract
  • CrossRef
  • Google Scholar

• 54

  FellbrichG.RomanskiA.VaretA.BlumeB.BrunnerF.EngelhardtS.et al (2002). NPP1, a Phytophthora-associated trigger of plant defense in parsley and Arabidopsis.Plant J.32375–390. 10.1046/j.1365-313x.2002.01454.x

  • Pubmed Abstract
  • CrossRef
  • Google Scholar

• 55

  FengB. Z.ZhuX. P.FuL.LvR. F.StoreyD.TooleyP.et al (2014). Characterization of necrosis-inducing NLP proteins in Phytophthora capsici.BMC Plant Biol.14:126. 10.1186/1471-2229-14-126

  • Pubmed Abstract
  • CrossRef
  • Google Scholar

• 56

  Franco-OrozcoB.BerepikiA.RuizO.GambleL.GriffeL. L.WangS.et al (2017). A new proteinaceous pathogen-associated molecular pattern (PAMP) identified in Ascomycete fungi induces cell death in Solanaceae.New Phytol.2141657–1672. 10.1111/nph.14542

  • Pubmed Abstract
  • CrossRef
  • Google Scholar

• 57

  FríasM.BritoN.GonzalezC. (2013). The Botrytis cinereal cerato-platanin BcSpl1 is a potent inducer of systemic acquired resistance (SAR) in tobacco and generates a wave of salicylic acid expanding from the site of application.Mol. Plant Pathol.14191–196. 10.1111/j.1364-3703.2012.00842.x

  • Pubmed Abstract
  • CrossRef
  • Google Scholar

• 58

  FríasM.GonzalezC.BritoN. (2011). BcSpl1, a cerato-platanin family protein, contributes to Botrytis cinerea virulence and elicits the hypersensitive response in the host.New Phytol.192483–495. 10.1111/j.1469-8137.2011.03802.x

  • Pubmed Abstract
  • CrossRef
  • Google Scholar

• 59

  FríasM.GonzalezM.GonzalezC.BritoN. (2016). BcIEB1, a Botrytis cinerea secreted protein, elicits a defense response in plants.Plant Sci.250115–124. 10.1016/j.plantsci.2016.06.009

  • Pubmed Abstract
  • CrossRef
  • Google Scholar

• 60

  FríasM.GonzálezM.GonzálezC.BritoN. (2019). A 25-residue peptide from Botrytis cinerea xylanase BcXyn11A elicits plant defenses.Front. Plant Sci.10:474. 10.3389/fpls.2019.00474

  • Pubmed Abstract
  • CrossRef
  • Google Scholar

• 61

  FuL.ZhuC.DingX.YangX.MorrisP. F.TylerB. M.et al (2015). Characterization of cell-death-inducing members of the pectate lyase gene family in Phytophthora capsici and their contributions to infection of pepper.Mol. Plant Microbe Interact.28766–775. 10.1094/MPMI-11-14-0352-R

  • Pubmed Abstract
  • CrossRef
  • Google Scholar

• 62

  FuchsY.SaxenaA.GambleH. R.AndersonJ. D. (1989). Ethylene biosynthesis-inducing protein from cellulysin is an endoxylanase.Plant Physiol.89138–143. 10.1104/pp.89.1.138

  • Pubmed Abstract
  • CrossRef
  • Google Scholar

• 63

  GalianaE.BonnetP.ConrodS.KellerH.PanabičresF.PonchetM.et al (1997). RNase activity prevents the growth of a fungal pathogen in tobacco leaves and increases upon induction of systemic acquired resistance with elicitin.Plant Physiol.1151557–1567. 10.1104/pp.115.4.1557

  • Pubmed Abstract
  • CrossRef
  • Google Scholar

• 64

  GarciaO.MacedoJ. A.TiburcioR.ZaparoliG.RinconesJ.BittencourtL. M.et al (2007). Characterization of necrosis and ethylene-inducing proteins (NEP) in the basidiomycete Moniliophthora perniciosa, the causal agent of witches’ broom in Theobroma cacao.Mycol. Res.111443–455. 10.1016/j.mycres.2007.01.017

  • Pubmed Abstract
  • CrossRef
  • Google Scholar

• 65

  GijzenM.NürnbergerT. (2006). Nep1-like proteins from plant pathogens: recruitment and diversification of the NPP1 domain across taxa.Phytochemistry671800–1807.

  • Google Scholar

• 66

  GiraldoM. C.ValentB. (2013). Filamentous plant pathogen effectors in action.Nat. Rev. Microbiol.11800–814. 10.1038/nrmicro3119

  • Pubmed Abstract
  • CrossRef
  • Google Scholar

• 67

  GonzálezM.BritoN.GonzalezC. (2017). The Botrytis cinerea elicitor protein BcIEB1 interacts with the tobacco PR5-family protein osmotin and protects the fungus against its antifungal activity.New Phytol.215397–410. 10.1111/nph.14588

  • Pubmed Abstract
  • CrossRef
  • Google Scholar

• 68

  GuiY. J.ChenJ. Y.ZhangD. D.LiN. Y.LiT. G.ZhangW. Q.et al (2017). Verticillium dahliae manipulates plant immunity by glycoside hydrolase 12 proteins in conjunction with carbohydrate-binding module 1.Environ. Microbiol.191914–1932. 10.1111/1462-2920.13695

  • Pubmed Abstract
  • CrossRef
  • Google Scholar

• 69

  GuiY. J.ZhangW. Q.ZhangD. D.ZhouL.ShortD. P. G.WangJ.et al (2018). A Verticillium dahliae extracellular cutinase modulates plant immune responses.Mol. Plant Microbe Interact.31260–273. 10.1094/MPMI-06-17-0136-R

  • Pubmed Abstract
  • CrossRef
  • Google Scholar

• 70

  GuoX.ZhongD.XieW.HeY.ZhengY.LinY.et al (2019). Functional identification of novel cell death-inducing effector proteins from Magnaporthe oryzae.Rice12:59. 10.1186/s12284-019-0312-z

  • Pubmed Abstract
  • CrossRef
  • Google Scholar

• 71

  HongY.YangY.ZhangH.HuangL.LiD.SongF. (2017). Overexpression of MoSM1, encoding for an immunity-inducing protein from Magnaporthe oryzae, in rice confers broad-spectrum resistance against fungal and bacterial diseases.Sci. Rep.7:41037. 10.1038/srep41037

  • Pubmed Abstract
  • CrossRef
  • Google Scholar

• 72

  HuetJ.Sallé-TourneM.PernolletJ. (1994). Amino acid sequence and toxicity of the alpha elicitin secreted with ubiquitin by Phytophthora infestans.Mol. Plant Microbe Interact.7302–304. 10.1094/mpmi-7-0302

  • Pubmed Abstract
  • CrossRef
  • Google Scholar

• 73

  HuetJ. C.MansionM.PernolletJ. C. (1993). Amino acid sequence of the α-elicitin secreted by Phytophthora cactorum.Phytochemistry341261–1264. 10.1016/0031-9422(91)80012-p

  • CrossRef
  • Google Scholar

• 74

  HuetJ. C.NespoulousC.PernolletJ. C. (1992). Structures of elicitin isoforms secreted by Phytophthora drechsleri.Phytochemistry311471–1476. 10.1016/0031-9422(92)83089-h

  • CrossRef
  • Google Scholar

• 75

  HuetJ. C.PernolletJ. C. (1989). Amino acid sequence of cinnamomin, a new member of the elicitin family, and its comparison to cryptogein and capsicein.FEBS Lett.257302–306. 10.1016/0014-5793(89)81557-1

  • CrossRef
  • Google Scholar

• 76

  HuetJ. C.PernolletJ. C. (1993). Sequences of acidic and basic elicitin isoforms secreted by Phytophthora megasperma.Phytochemistry33797–805. 10.1016/0031-9422(93)85277-x

  • CrossRef
  • Google Scholar

• 77

  HuitemaE.VleeshouwersV. G.CakirC.KamounS.GoversF. (2005). Differences in intensity and specificity of hypersensitive response induction in Nicotiana spp. by INF1, INF2A, and INF2B of Phytophthora infestans.Mol. Plant Microbe Interact.18183–193. 10.1094/MPMI-18-0183

  • Pubmed Abstract
  • CrossRef
  • Google Scholar

• 78

  JeongJ. S.MitchellT. K.DeanR. A. (2007). The Magnaporthe grisea snodprot1 homolog, MSP1, is required for virulence.FEMS Microbiol. Lett.273157–165. 10.1111/j.1574-6968.2007.00796.x

  • Pubmed Abstract
  • CrossRef
  • Google Scholar

• 79

  JiangR. H.TylerB. M.WhissonS. C.HardhamA. R.GoversF. (2006). Ancient origin of elicitin gene clusters in Phytophthora genomes.Mol. Biol. Evol.23338–351. 10.1093/molbev/msj039

  • Pubmed Abstract
  • CrossRef
  • Google Scholar

• 80

  JinH.HartmanG. L.NickellC. D.WidholmJ. M. (1996). Characterization and purification of a phytotoxin produced by Fusarium solani, the causal agent of soybean sudden death syndrome.Phytopathology86277–282. 10.1094/Phyto-86-277

  • CrossRef
  • Google Scholar

• 81

  KamounS. (2006). A catalogue of the effector secretome of plant pathogenic oomycetes.Annu. Rev. Phytopathol.4441–60. 10.1146/annurev.phyto.44.070505.143436

  • Pubmed Abstract
  • CrossRef
  • Google Scholar

• 82

  KamounS.KlucherK. M.CoffeyM. D.TylerB. M. (1993). A gene encoding a host-specific elicitor protein of Phytophthora parasitica.Mol. Plant Microbe Interact.6573–573. 10.1094/MPMI-6-573

  • Pubmed Abstract
  • CrossRef
  • Google Scholar

• 83

  KamounS.van WestP.de JongA. J.de GrootK. E.VleeshouwersV. G.GoversF. (1997). A gene encoding a protein elicitor of Phytophthora infestans is down-regulated during infection of potato.Mol. Plant Microbe Interact.1013–20. 10.1094/MPMI.1997.10.1.13

  • Pubmed Abstract
  • CrossRef
  • Google Scholar

• 84

  KamounS.Van WestP.VleeshouwersV. G.De GrootK. E.GoversF. (1998). Resistance of Nicotiana benthamiana to Phytophthora infestans is mediated by the recognition of the elicitor protein INF1.Plant Cell101413–1425. 10.2307/3870607

  • CrossRef
  • Google Scholar

• 85

  KannegantiT. D.HuitemaE.CakirC.KamounS. (2006). Synergistic interactions of the plant cell death pathways induced by Phytophthora infestans Nep1-like protein PiNPP1. 1 and INF1 elicitin.Mol. Plant Microbe interact.19854–863. 10.1094/mpmi-19-0854

  • Pubmed Abstract
  • CrossRef
  • Google Scholar

• 86

  KanzakiH.SaitohH.ItoA.FujisawaS.KamounS.KatouS.et al (2003). Cytosolic HSP90 and HSP70 are essential components of INF1-mediated hypersensitive response and non-host resistance to Pseudomonas cichorii in Nicotiana benthamiana.Mol. Plant Pathol.4383–391. 10.1046/j.1364-3703.2003.00186.x

  • Pubmed Abstract
  • CrossRef
  • Google Scholar

• 87

  KanzakiH.SaitohH.TakahashiY.BerberichT.ItoA.KamounS.et al (2008). NbLRK1, a lectin-like receptor kinase protein of Nicotiana benthamiana, interacts with Phytophthora infestans INF1 elicitin and mediates INF1-induced cell death.Planta228977–987. 10.1007/s00425-008-0797-y

  • Pubmed Abstract
  • CrossRef
  • Google Scholar

• 88

  KarsI.KrooshofG. H.WagemakersL.JoostenR.BenenJ. A.van KanJ. A. (2005). Necrotizing activity of five Botrytis cinerea endopolygalacturonases produced in Pichia pastoris.Plant J.43213–225. 10.1111/j.1365-313X.2005.02436.x

  • Pubmed Abstract
  • CrossRef
  • Google Scholar

• 89

  KawamuraY.TakenakaS.HaseS.KubotaM.IchinoseY.KanayamaY.et al (2009). Enhanced defense responses in Arabidopsis induced by the cell wall protein fractions from Pythium oligandrum require SGT1, RAR1, NPR1 and JAR1.Plant Cell Physiol.50924–934. 10.1093/pcp/pcp044

  • Pubmed Abstract
  • CrossRef
  • Google Scholar

• 90

  KelleyB. S.LeeS. J.DamascenoC. M.ChakravarthyS.KimB. D.MartinG. B.et al (2010). A secreted effector protein (Sne1) from Phytophthora infestans is a broadly acting suppressor of programmed cell death.Plant J.62357–366. 10.1111/j.1365-313X.2010.04160.x

  • Pubmed Abstract
  • CrossRef
  • Google Scholar

• 91

  KettlesG. J.BayonC.CanningG.RuddJ. J.KanyukaK. (2017). Apoplastic recognition of multiple candidate effectors from the wheat pathogen Zymoseptoria tritici in the nonhost plant Nicotiana benthamiana.New Phytol.213338–350. 10.1111/nph.14215

  • Pubmed Abstract
  • CrossRef
  • Google Scholar

• 92

  KhatibM.LafitteC.Esquerré-TugayéM. T.BottinA.RickauerM. (2004). The CBEL elicitor of Phytophthora parasitica var. nicotianae activates defence in Arabidopsis thaliana via three different signalling pathways.New Phytol.162501–510. 10.1111/j.1469-8137.2004.01043.x

  • CrossRef
  • Google Scholar

• 93

  KleemannJ.Rincon-RiveraL. J.TakaharaH.NeumannU.van ThemaatE. V. L.van der DoesH. C.et al (2012). Sequential delivery of host-induced virulence effectors by appressoria and intracellular hyphae of the phytopathogen Colletotrichum higginsianum.PLoS Pathog.8:e1002643. 10.1371/journal/ppat.1002643

  • Pubmed Abstract
  • CrossRef
  • Google Scholar

• 94

  KouY. J.TanY. H.RamanujamR.NaqviN. I. (2017). Structure-function analyses of the Pth11 receptor reveal an important role for CFEM motif and redox regulation in rice blast.New Phytol.214330–342. 10.1111/nph.14347

  • Pubmed Abstract
  • CrossRef
  • Google Scholar

• 95

  KubicekC. P.StarrT. L.GlassN. L. (2014). Plant cell wall-degrading enzymes and their secretion in plant-pathogenic fungi.Annu. Rev. Phytopathol.52427–451. 10.1146/annurev-phyto-102313-045831

  • Pubmed Abstract
  • CrossRef
  • Google Scholar

• 96

  KulikA.NoirotE.GrandperretV.BourqueS.FromentinJ.SalloignonP.et al (2015). Interplays between nitric oxide and reactive oxygen species in cryptogein signalling.Plant Cell Environ.38331–348. 10.1111/pce.12295

  • Pubmed Abstract
  • CrossRef
  • Google Scholar

• 97

  KulkarniR. D.KelkarH. S.DeanR. A. (2003). An eight-cysteine-containing CFEM domain unique to a group of fungal membrane proteins.Trends Biochem. Sci.28118–121. 10.1016/S0968-0004(03)00034-3

  • CrossRef
  • Google Scholar

• 98

  KulyeM.LiuH.ZhangY. L.ZengH. M.YangX. F.QiuD. W. (2012). 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.352104–2120. 10.1111/j.1365-3040.2012.02539.x

  • Pubmed Abstract
  • CrossRef
  • Google Scholar

• 99

  Leborgne-CastelN.LherminierJ.DerC.FromentinJ.HouotV.Simon-PlasF. (2008). The plant defense elicitor cryptogein stimulates clathrin-mediated endocytosis correlated with reactive oxygen species production in bright yellow-2 tobacco cells.Plant Physiol.1461255–1266. 10.1104/pp.107.111716

  • Pubmed Abstract
  • CrossRef
  • Google Scholar

• 100

  LenarčičT.AlbertI.BöhmH.HodnikV.PircK.ZavecA. B.et al (2017). Eudicot plant-specific sphingolipids determine host selectivity of microbial NLP cytolysins.Science3581431–1434. 10.1126/science.aan6874

  • Pubmed Abstract
  • CrossRef
  • Google Scholar

• 101

  LiS.DongY.LiL.ZhangY.YangX.ZengH.et al (2019a). The novel cerato-platanin-like protein FocCP1 from Fusarium oxysporum triggers an immune response in plants.Int. J. Mol. Sci.20:2849. 10.3390/ijms20112849

  • Pubmed Abstract
  • CrossRef
  • Google Scholar

• 102

  LiS.NieH.QiuD.ShiM.YuanQ. (2019b). A novel protein elicitor PeFOC1 from Fusarium oxysporum triggers defense response and systemic resistance in tobacco.Biochem. Biophys Res. Commun.5141074–1080. 10.1016/j.bbrc.2019.05.018

  • Pubmed Abstract
  • CrossRef
  • Google Scholar

• 103

  LiX. C.SunY.LiuN. N.WangP.PeiY. K.LiuD.et al (2019c). Enhanced resistance to Verticillium dahliae mediated by an F-box protein GhACIF1 from Gossypium hirsutum.Plant Sci.284127–134. 10.1016/j.plantsci.2019.04.013

  • Pubmed Abstract
  • CrossRef
  • Google Scholar

• 104

  LiuM.KhanN. U.WangN.YangX.QiuD. (2016). The protein elicitor PevD1 enhances resistance to pathogens and promotes growth in Arabidopsis.Int. J. Biol. Sci.12931–943. 10.7150/ijbs.15447

  • Pubmed Abstract
  • CrossRef
  • Google Scholar

• 105

  LiuS.WuB.YangJ.BiF.DongT.YangQ.et al (2019). A cerato-platanin family protein FocCP1 is essential for the penetration and virulence of Fusarium oxysporum f. sp. cubense tropical race 4.Int. J. Mol. Sci.20:3785. 10.3390/ijms20153785

  • Pubmed Abstract
  • CrossRef
  • Google Scholar

• 106

  LiuZ. Q.LiuY. Y.ShiL. P.YangS.ShenL.YuH. X.et al (2016). SGT1 is required in PcINF1/SRC2-1 induced pepper defense response by interacting with SRC2-1.Sci. Rep.6:21651. 10.1038/srep21651

  • Pubmed Abstract
  • CrossRef
  • Google Scholar

• 107

  LiuZ. Q.QiuA. L.ShiL. P.CaiJ. S.HuangX. Y.YangS.et al (2015). SRC2-1 is required in PcINF1-induced pepper immunity by acting as an interacting partner of PcINF1.J. Exp. Bot.663683–3698. 10.1093/jxb/erv161

  • Pubmed Abstract
  • CrossRef
  • Google Scholar

• 108

  Lo PrestiL.KahmannR. (2017). How filamentous plant pathogen effectors are translocated to host cells.Curr. Opin. Plant Biol.3819–24. 10.1016/j.pbi.2017.04.005

  • Pubmed Abstract
  • CrossRef
  • Google Scholar

• 109

  LutiS.CaselliA.TaitiC.BazihizinaN.GonnelliC.MancusoS.et al (2016). PAMP activity of cerato-platanin during plant interaction: an-omic approach.Int. J. Mol. Sci.17:866. 10.3390/ijms17060866

  • Pubmed Abstract
  • CrossRef
  • Google Scholar

• 110

  MaZ.SongT.ZhuL.YeW.WangY.ShaoY.et al (2015). A Phytophthora sojae glycoside hydrolase 12 protein is a major virulence factor during soybean infection and is recognized as a PAMP.Plant Cell272057–2072. 10.1105/tpc.15.00390

  • Pubmed Abstract
  • CrossRef
  • Google Scholar

• 111

  MaZ. H.ZhuL.SongT. Q.WangY.ZhangQ.XiaY. Q.et al (2017). A paralogous decoy protects Phytophthora sojae apoplastic effector PsXEG1 from a host inhibitor.Science355710–714. 10.1126/science.aai7919

  • Pubmed Abstract
  • CrossRef
  • Google Scholar

• 112

  MateosF. V.RickauerM.Esquerré-TugayéM. T. (1997). Cloning and characterization of a cDNA encoding an elicitor of Phytophthora parasitica var. nicotianae that shows cellulose-binding and lectin-like activities.Mol. Plant Microbe Interact.101045–1053. 10.1094/MPMI.1997.10.9.1045

  • Pubmed Abstract
  • CrossRef
  • Google Scholar

• 113

  M’BarekS. B.CordewenerJ. H.GhaffaryS. M. T.van der LeeT. A.LiuZ.GohariA. M.et al (2015). FPLC and liquid-chromatography mass spectrometry identify candidate necrosis-inducing proteins from culture filtrates of the fungal wheat pathogen Zymoseptoria tritici.Fungal Genet. Biol.7954–62. 10.1016/j.fgb.2015.03.015

  • Pubmed Abstract
  • CrossRef
  • Google Scholar

• 114

  MikesV.MilatM. L.PonchetM.RicciP.BleinJ. P. (1997). The fungal elicitor cryptogein is a sterol carrier protein.FEBS Lett.416190–192. 10.1016/S0014-5793(97)01193-9

  • CrossRef
  • Google Scholar

• 115

  MishraA. K.SharmaK.MisraR. S. (2009). Purification and characterization of elicitor protein from Phytophthora colocasiae and basic resistance in Colocasia esculenta.Microbiol. Res.164688–693. 10.1016/j.micres.2008.09.001

  • Pubmed Abstract
  • CrossRef
  • Google Scholar

• 116

  MotteramJ.KüfnerI.DellerS.BrunnerF.Hammond-KosackK. E.NürnbergerT.et al (2009). Molecular characterization and functional analysis of MgNLP, the sole NPP1 domain–containing protein, from the fungal wheat leaf pathogen Mycosphaerella graminicola.Mol. Plant Microbe Interact.22790–799. 10.1094/MPMI-22-7-0790

  • Pubmed Abstract
  • CrossRef
  • Google Scholar

• 117

  Mouton-PerronnetF.BruneteauM.DenoroyL.BouliteauP.RicciP.BonnetP.et al (1995). Elicitin produced by an isolate of Phytophthora parasitica pathogenic to tobacco.Phytochemistry3841–44. 10.1016/0031-9422(94)0058X-A

  • CrossRef
  • Google Scholar

• 118

  NespoulousC.HuetJ. C.PernolletJ. C. (1992). Structure-function relationships of alpha and beta elicitins, signal proteins involved in the plant-Phytophthora interaction.Planta186551–557. 10.1007/bf00198035

  • Pubmed Abstract
  • CrossRef
  • Google Scholar

• 119

  NieH.ZhangL.ZhuangH.YangX.QiuD.ZengH. (2019). Secreted protein MoHrip2 is required for full virulence of Magnaporthe oryzae and modulation of rice immunity.Appl. Microbiol. Biotechnol.1036153–6167. 10.1007/s00253-019-09937-2

  • Pubmed Abstract
  • CrossRef
  • Google Scholar

• 120

  NieH. Z.ZhangL.ZhuangH. Q.ShiW. J.YangX. F.QiuD. W.et al (2019). The secreted protein MoHrip1 is necessary for the virulence of Magnaporthe oryzae.Int. J. Mol. Sci.20:1643. 10.3390/ijms20071643

  • Pubmed Abstract
  • CrossRef
  • Google Scholar

• 121

  NieJ.YinZ.LiZ.WuY.HuangL. (2019). A small cysteine-rich protein from two kingdoms of microbes is recognized as a novel pathogen-associated molecular pattern.New Phytol.222995–1011. 10.1111/nph.15631

  • Pubmed Abstract
  • CrossRef
  • Google Scholar

• 122

  NodaJ.BritoN.GonzálezC. (2010). The Botrytis cinerea xylanase Xyn11A contributes to virulence with its necrotizing activity, not with its catalytic activity.BMC Plant Biol.10:38. 10.1186/1471-2229-10-38

  • Pubmed Abstract
  • CrossRef
  • Google Scholar

• 123

  NoirotE.DerC.LherminierJ.RobertF.MoricovaP.KiêuK.et al (2014). Dynamic changes in the subcellular distribution of the tobacco ROS-producing enzyme RBOHD in response to the oomycete elicitor cryptogein.J. Exp. Bot.655011–5022. 10.1093/jxb/eru265

  • Pubmed Abstract
  • CrossRef
  • Google Scholar

• 124

  OrsomandoG.LorenziM.RaffaelliN.Dalla RizzaM.MezzettiB.RuggieriS. (2001). Phytotoxic protein PcF, purification, characterization, and cDNA sequencing of a novel hydroxyproline-containing factor secreted by the strawberry pathogen Phytophthora cactorum.J. Biol. Chem.27621578–21584. 10.1074/jbc.M101377200

  • Pubmed Abstract
  • CrossRef
  • Google Scholar

• 125

  OttmannC.LuberackiB.KüfnerI.KochW.BrunnerF.WeyandM.et al (2009). A common toxin fold mediates microbial attack and plant defense.Proc. Natl. Acad. Sci. U.S.A10610359–10364.

  • Google Scholar

• 126

  PalmerC. S.SaleebaJ. A.LyonB. R. (2005). Phytotoxicity on cotton ex-plants of an 18.5 kDa protein from culture filtrates of Verticillium dahliae.Physiol. Mol. Plant Pathol.67308–318. 10.1016/j.pmpp.2006.05.003

  • CrossRef
  • Google Scholar

• 127

  PanabieresF.MaraisA.BerreJ. Y.PenotI.FournierD.RicciP.et al (1995). Characterization of a gene cluster of Phytophthora cryptogea which codes for elicitins, proteins inducing a hypersensitive-like response in tobacco.Mol. Plant Microbe Interact.8996–1003. 10.1094/MPMI-8-0996

  • Pubmed Abstract
  • CrossRef
  • Google Scholar

• 128

  PazzagliL.CappugiG.ManaoG.CamiciG.SantiniA.ScalaA. (1999). Purification, characterization, and amino acid sequence of cerato-platanin, a new phytotoxic protein from Ceratocystis fimbriata f. sp. platani.J. Biol. Chem.27424959–24964. 10.1074/jbc.274.35.24959

  • Pubmed Abstract
  • CrossRef
  • Google Scholar

• 129

  PazzagliL.Seidl-SeibothV.BarsottiniM.VargasW. A.ScalaA.MukherjeeP. K. (2014). Cerato-platanins: elicitors and effectors.Plant Sci.22879–87. 10.1016/j.plantsci.2014.02.009

  • Pubmed Abstract
  • CrossRef
  • Google Scholar

• 130

  PettongkhaoS.ChurngchowN. (2019). Novel cell death-inducing elicitors from Phytophthora palmivora promote infection on Hevea brasiliensis.Phytopathology1091769–1778. 10.1094/PHYTO-01-19-0002-R

  • Pubmed Abstract
  • CrossRef
  • Google Scholar

• 131

  PicardK.PonchetM.BleinJ. P.ReyP.TirillyY.BenhamouN. (2000). Oligandrin. A proteinaceous molecule produced by the mycoparasite Pythium oligandrum induces resistance to Phytophthora parasitica infection in tomato plants.Plant Physiol.124379–395. 10.1104/pp.124.1.379

  • Pubmed Abstract
  • CrossRef
  • Google Scholar

• 132

  PtáčkováN.KlempováJ.ObořilM.NedělováS.LochmanJ.KašparovskýT. (2015). The effect of cryptogein with changed abilities to transfer sterols and altered charge distribution on extracellular alkalinization, ROS and NO generation, lipid peroxidation and LOX gene transcription in Nicotiana tabacum.Plant Physiol. Biochem.9782–95. 10.1016/j.plaphy.2015.09.009

  • Pubmed Abstract
  • CrossRef
  • Google Scholar

• 133

  QuarantinA.CastiglioniC.SchäferW.FavaronF.SellaL. (2019). The Fusarium graminearum cerato-platanins loosen cellulose substrates enhancing fungal cellulase activity as expansin-like proteins.Plant Physiol. Biochem.139229–238. 10.1016/j.plaphy.2019.03.025

  • Pubmed Abstract
  • CrossRef
  • Google Scholar

• 134

  QuarantinA.GlasenappA.SchaferW.FavaronF.SellaL. (2016). Involvement of the Fusarium graminearum cerato-platanin proteins in fungal growth and plant infection.Plant Physiol. Biochem.109220–229. 10.1016/j.plaphy.2016.10.001

  • Pubmed Abstract
  • CrossRef
  • Google Scholar

• 135

  QutobD.KamounS.GijzenM. (2002). Expression of a Phytophthora sojae necrosis-inducing protein occurs during transition from biotrophy to necrotrophy.Plant J.32361–373. 10.1046/j.1365-313x.2002.01439.x

  • Pubmed Abstract
  • CrossRef
  • Google Scholar

• 136

  QutobD.KemmerlingB.BrunnerF.KufnerI.EngelhardtS.GustA. A.et al (2006). Phytotoxicity and innate immune responses induced by Nep1-like proteins.Plant Cell183721–3744. 10.1105/tpc.106.044180

  • Pubmed Abstract
  • CrossRef
  • Google Scholar

• 137

  RicciP.BonnetP.HuetJ. C.SallantinM.Beauvais-CanteF.BruneteauM.et al (1989). Structure and activity of proteins from pathogenic fungi Phytophthora eliciting necrosis and acquired resistance in tobacco.Eur. J. Biochem.183555–563. 10.1111/j.1432-1033.1989.tb21084.x

  • Pubmed Abstract
  • CrossRef
  • Google Scholar

• 138

  RonM.AvniA. (2004). The receptor for the fungal elicitor ethylene-inducing xylanase is a member of a resistance-like gene family in tomato.Plant Cell161604–1615. 10.1105/tpc.022475

  • Pubmed Abstract
  • CrossRef
  • Google Scholar

• 139

  Sánchez-ValletA.FouchéS.FudaI.HartmannF. E.SoyerJ. L.TellierA.et al (2018). The genome biology of effector gene evolution in filamentous plant pathogens.Annu. Rev. Phytopathol.5621–40.

  • Google Scholar

• 140

  SanthanamP.van EsseH. P.AlbertI.FainoL.NürnbergerT.ThommaB. P. (2013). Evidence for functional diversification within a fungal NEP1-like protein family.Mol. Plant Microbe Interact.26278–286. 10.1094/MPMI-09-12-0222-R

  • Pubmed Abstract
  • CrossRef
  • Google Scholar

• 141

  SasabeM.TakeuchiK.KamounS.IchinoseY.GoversF.ToyodaK.et al (2000). Independent pathways leading to apoptotic cell death, oxidative burst and defense gene expression in response to elicitin in tobacco cell suspension culture.Eur. J. Biochem.2675005–5013. 10.1046/j.1432-1327.2000.01553.x

  • Pubmed Abstract
  • CrossRef
  • Google Scholar

• 142

  ScalaA.PazzagliL.CompariniC.SantiniA.TegliS.CappugiG. (2004). Cerato-platanin, an early-produced protein by Ceratocystis fimbriata f. sp. platani, elicits phytoalexin synthesis in host and non-host plants.J. Plant Pathol.8627–33. 10.1111/j.1439-0329.2010.00668.x

  • CrossRef
  • Google Scholar

• 143

  SchoutenA.Van BaarlenP.Van KanJ. A. (2008). Phytotoxic Nep1-like proteins from the necrotrophic fungus Botrytis cinerea associate with membranes and the nucleus of plant cells.New Phytol.177493–505. 10.1111/j.1469-8137.2007.02274.x

  • Pubmed Abstract
  • CrossRef
  • Google Scholar

• 144

  SellaL.GazzettiK.FaoroF.OdorizziS.D’OvidioR.SchäferW.et al (2013). A Fusarium graminearum xylanase expressed during wheat infection is a necrotizing factor but is not essential for virulence.Plant Physiol. Biochem.641–10. 10.1016/j.plaphy.2012.12.008

  • Pubmed Abstract
  • CrossRef
  • Google Scholar

• 145

  SharathchandraR. G.GeethaN. P.AmrutheshK. N.KiniK. R.SaroshB. R.ShettyN. P.et al (2006). Isolation and characterisation of a protein elicitor from Sclerospora graminicola and elicitor-mediated induction of defence responses in cultured cells of Pennisetum glaucum.Funct. Plant Biol.33267–278. 10.1071/fp05197

  • CrossRef
  • Google Scholar

• 146

  SrivastavaV. K.SuneethaK. J.KaurR. (2014). A systematic analysis reveals an essential role for high-affinity iron uptake system, haemolysin and CFEM domain-containing protein in iron homoeostasis and virulence in Candida glabrata.Biochem. J.463103–114. 10.1042/BJ20140598

  • Pubmed Abstract
  • CrossRef
  • Google Scholar

• 147

  StaatsM.van BaarlenP.SchoutenA.van KanJ. A. (2007). Functional analysis of NLP genes from Botrytis elliptica.Mol. Plant Pathol.8209–214. 10.1111/j.1364-3703.2007.00382.x

  • Pubmed Abstract
  • CrossRef
  • Google Scholar

• 148

  StarýT.SatkováP.PiterkováJ.MieslerováB.LuhováL.MikulíkJ.et al (2019). The elicitin β-cryptogein’s activity in tomato is mediated by jasmonic acid and ethylene signalling pathways independently of elicitin-sterol interactions.Planta249739–749. 10.1007/s00425-018-3036-1

  • Pubmed Abstract
  • CrossRef
  • Google Scholar

• 149

  TehC. Y.PangC. L.TorX. Y.HoP. Y.LimY. Y.NamasivayamP.et al (2018). Molecular cloning and functional analysis of a necrosis and ethylene inducing protein (NEP) from Ganoderma boninense.Physiol. Mol. Plant Pathol.10642–48. 10.1016/j.pmpp.2018.12.003

  • CrossRef
  • Google Scholar

• 150

  ten HaveA.MulderW.VisserJ.van KanJ. A. L. (1998). The endopolygalacturonase gene Bcpg1 is required for full virulence of Botrytis cinerea.Mol. Plant Microbe Interact.111009–1016. 10.1094/MPMI.1998.11.10.1009

  • Pubmed Abstract
  • CrossRef
  • Google Scholar

• 151

  TengW.ZhangH.WangW.LiD.WangM.LiuJ.et al (2014). ALY proteins participate in multifaceted Nep1Mo-triggered responses in Nicotiana benthamiana and Arabidopsis thaliana.J. Exp. Bot.652483–2494. 10.1093/jxb/eru136

  • Pubmed Abstract
  • CrossRef
  • Google Scholar

• 152

  TortoT. A.LiS.StyerA.HuitemaE.TestaA.GowN. A.et al (2003). EST mining and functional expression assays identify extracellular effector proteins from the plant pathogen Phytophthora.Genome Res.131675–1685. 10.1101/gr.910003

  • Pubmed Abstract
  • CrossRef
  • Google Scholar

• 153

  TundoS.MoscettiI.FaoroF.LafondM.GiardinaT.FavaronF.et al (2015). Fusarium graminearum produces different xylanases causing host cell death that is prevented by the xylanase inhibitors XIP-I and TAXI-III in wheat.Plant Sci.240161–169. 10.1016/j.plantsci.2015.09.002

  • Pubmed Abstract
  • CrossRef
  • Google Scholar

• 154

  Van den AckervekenG. (2017). How plants differ in toxin-sensitivity.Science3581383–1384.

  • Google Scholar

• 155

  VeitS.WörleJ. M.NürnbergerT.KochW.SeitzH. U. (2001). A novel protein elicitor (PaNie) from Pythium aphanidermatum induces multiple defense responses in carrot, Arabidopsis, and tobacco.Plant Physiol.127832–841. 10.1104/pp.010350

  • CrossRef
  • Google Scholar

• 156

  WangB.YangX.ZengH.LiuH.ZhouT.TanB.et al (2012). The purification and characterization of a novel hypersensitive-like response-inducing elicitor from Verticillium dahliae that induces resistance responses in tobacco.Appl. Microbiol. Biotechnol.93191–201. 10.1007/s00253-011-3405-1

  • Pubmed Abstract
  • CrossRef
  • Google Scholar

• 157

  WangJ. Y.CaiY.GouJ. Y.MaoY. B.XuY. H.JiangW. H.et al (2004). VdNEP, an elicitor from Verticillium dahliae, induces cotton plant wilting.Appl. Environ. Microbiol.704989–4995. 10.1128/AEM.70.8.4989-4995.200

  • CrossRef
  • Google Scholar

• 158

  WangW.AnB.FengL.HeC.LuoH. (2018). A Colletotrichum gloeosporioides cerato-platanin protein, CgCP1, contributes to conidiation and plays roles in the interaction with rubber tree.Can. J. Microbiol.64826–834. 10.1139/cjm-2018-0087

  • Pubmed Abstract
  • CrossRef
  • Google Scholar

• 159

  WangY.XuY.SunY.WangH.QiJ.WanB.et al (2018). Leucine-rich repeat receptor-like gene screen reveals that Nicotiana RXEG1 regulates glycoside hydrolase 12 MAMP detection.Nat. Commun.9:594. 10.1038/s41467-018-03010-8

  • Pubmed Abstract
  • CrossRef
  • Google Scholar

• 160

  WangY.HuD.ZhangZ.MaZ.ZhengX.LiD. (2003). Purification and immunocytolocalization of a novel Phytophthora boehmeriae protein inducing the hypersensitive response and systemic acquired resistance in tobacco and Chinese cabbage.Physiol. Mol. Plant Pathol.63223–232. 10.1016/j.pmpp.2003.12.004

  • CrossRef
  • Google Scholar

• 161

  WangY.WuJ.KimS. G.TsudaK.GuptaR.ParkS. Y.et al (2016). Magnaporthe oryzae-secreted protein MSP1 induces cell death and elicits defense responses in rice.Mol. Plant Microbe Interact.29299–312. 10.1094/MPMI-12-15-0266-R

  • Pubmed Abstract
  • CrossRef
  • Google Scholar

• 162

  YangC.LiangY.QiuD.ZengH.YuanJ.YangX. (2018a). Lignin metabolism involves Botrytis cinerea BcGs1-induced defense response in tomato.BMC Plant Biol.18:103. 10.1186/s12870-018-1319-0

  • Pubmed Abstract
  • CrossRef
  • Google Scholar

• 163

  YangG.TangL.GongY.XieJ.FuY.JiangD.et al (2018b). A cerato-platanin protein SsCP1 targets plant PR1 and contributes to virulence of Sclerotinia sclerotiorum.New Phytol.217739–755. 10.1111/nph.14842

  • Pubmed Abstract
  • CrossRef
  • Google Scholar

• 164

  YangY.YangX.DongY.QiuD. (2018c). The Botrytis cinerea xylanase BcXyl1 modulates plant immunity.Front. Microbiol.9:2535. 10.3389/fmicb.2018.02535

  • Pubmed Abstract
  • CrossRef
  • Google Scholar

• 165

  YangY.ZhangY.LiB.YangX.DongY.QiuD. (2018d). A Verticillium dahliae pectate lyase induces plant immune responses and contributes to virulence.Front. Plant Sci.9:1271. 10.3389/fpls.2018.01271

  • Pubmed Abstract
  • CrossRef
  • Google Scholar

• 166

  YangY.ZhangH.LiG.LiW.WangX.SongF. (2009). Ectopic expression of MgSM1, a cerato-platanin family protein from Magnaporthe grisea, confers broad-spectrum disease resistance in Arabidopsis.Plant Biotechnol. J.7763–777. 10.1111/j.1467-7652.2009.00442.x

  • Pubmed Abstract
  • CrossRef
  • Google Scholar

• 167

  YaoZ.RashidK. Y.AdamL. R.DaayfF. (2011). Verticillium dahliae’s VdNEP acts both as a plant defence elicitor and a pathogenicity factor in the interaction with Helianthus annuus.Can. J. Plant Pathol.33375–388. 10.1080/07060661.2011.579173

  • CrossRef
  • Google Scholar

• 168

  YoshinoK.IriedaH.SugimotoF.YoshiokaH.OkunoT.TakanoY. (2012). Cell death of Nicotiana benthamiana is induced by secreted protein NIS1 of Colletotrichum orbiculare and is suppressed by a homologue of CgDN3.Mol. Plant Microbe Interact.25625–636. 10.1094/MPMI-12-11-0316

  • Pubmed Abstract
  • CrossRef
  • Google Scholar

• 169

  YoshiokaH.NumataN.NakajimaK.KatouS.KawakitaK.RowlandO.et al (2003). Nicotiana benthamiana gp91^phox homologs NbrbohA and NbrbohB participate in H₂O₂ accumulation and resistance to Phytophthora infestans.Plant Cell15706–718. 10.1105/tpc.008680

  • Pubmed Abstract
  • CrossRef
  • Google Scholar

• 170

  ZaparoliG.CabreraO. G.MedranoF. J.TiburcioR.LacerdaG.PereiraG. G. (2009). Identification of a second family of genes in Moniliophthora perniciosa, the causal agent of witches’ broom disease in cacao, encoding necrosis-inducing proteins similar to cerato-platanins.Mycol. Res.11361–72. 10.1016/j.mycres.2008.08.004

  • Pubmed Abstract
  • CrossRef
  • Google Scholar

• 171

  ZhangH.DongS.WangM.WangW.SongW.DouX.et al (2010). The role of vacuolar processing enzyme (VPE) from Nicotiana benthamiana in the elicitor-triggered hypersensitive response and stomatal closure.J. Exp. Bot.613799–3812. 10.1093/jxb/erq189

  • Pubmed Abstract
  • CrossRef
  • Google Scholar

• 172

  ZhangH.LiD.WangM.LiuJ.TengW.ChengB.et al (2012). The Nicotiana benthamiana mitogen-activated protein kinase cascade and WRKY transcription factor participate in Nep1(Mo)-triggered plant responses.Mol. Plant Microbe Interact.251639–1653. 10.1094/MPMI-11-11-0293

  • Pubmed Abstract
  • CrossRef
  • Google Scholar

• 173

  ZhangH.WuQ.CaoS.ZhaoT.ChenL.ZhuangP.et al (2014). A novel protein elicitor (SsCut) from Sclerotinia sclerotiorum induces multiple defense responses in plants.Plant Mol. Biol.86495–511. 10.1007/s11103-014-0244-3

  • Pubmed Abstract
  • CrossRef
  • Google Scholar

• 174

  ZhangL.KarsI.EssenstamB.LiebrandT. W.WagemakersL.ElberseJ.et al (2014). Fungal endopolygalacturonases are recognized as microbe-associated molecular patterns by the Arabidopsis receptor-like protein RESPONSIVENESS TO BOTRYTIS POLYGALACTURONASES1.Plant Physiol.164352–364. 10.1104/pp.113.230698

  • Pubmed Abstract
  • CrossRef
  • Google Scholar

• 175

  ZhangH.ZhaoT.ZhuangP.SongZ.DuH.TangZ.et al (2016). NbCZF1, a novel C2H2-Type zinc finger protein, as a new regulator of SsCut-induced plant immunity in Nicotiana benthamiana.Plant Cell Physiol.572472–2484. 10.1093/pcp/pcw160

  • Pubmed Abstract
  • CrossRef
  • Google Scholar

• 176

  ZhangY.GaoY.LiangY.DongY.YangX.QiuD. (2019). Verticillium dahliae PevD1, an Alt a 1-like protein, targets cotton PR5-like protein and promotes fungal infection.J. Exp Bot.70613–626. 10.1093/jxb/ery351

  • Pubmed Abstract
  • CrossRef
  • Google Scholar

• 177

  ZhangY.GaoY.LiangY.DongY.YangX.YuanJ.et al (2017a). The Verticillium dahliae snodprot1-like protein VdCP1 contributes to virulence and triggers the plant immune system.Front. Plant Sci.8:1880. 10.3389/fpls.2017.01880

  • Pubmed Abstract
  • CrossRef
  • Google Scholar

• 178

  ZhangY.LiangY.DongY.GaoY.YangX.YuanJ.et al (2017b). The Magnaporthe oryzae Alt A 1-like protein MoHrip1 binds to the plant plasma membrane.Biochem. Biophys. Res. Commun.49255–60. 10.1016/j.bbrc.2017.08.039

  • Pubmed Abstract
  • CrossRef
  • Google Scholar

• 179

  ZhangY.ZhangY.QiuD.ZengH.GuoL.YangX. (2015). BcGs1, a glycoprotein from Botrytis cinerea, elicits defence response and improves disease resistance in host plants.Biochem. Biophys. Res. Commun.457627–634. 10.1016/j.bbrc.2015.01.038

  • Pubmed Abstract
  • CrossRef
  • Google Scholar

• 180

  ZhangZ. G.WangY. C.LiJ.JiR.ShenG.WangS. C.et al (2004). The role of SA in the hypersensitive response and systemic acquired resistance induced by elicitor PB90 from Phytophthora boehmeriae.Physiol. Mol. Plant Pathol.6531–38. 10.1016/j.pmpp.2004.11.001

  • CrossRef
  • Google Scholar

• 181

  ZhangZ. N.WuQ. Y.ZhangG. Z.ZhuY. Y.MurphyR. W.LiuZ.et al (2015). Systematic analyses reveal uniqueness and origin of the CFEM domain in fungi.Sci. Rep.5:13032. 10.1038/srep13032

  • Pubmed Abstract
  • CrossRef
  • Google Scholar

• 182

  ZhaoZ.LiuH.WangC.XuJ. R. (2013). Comparative analysis of fungal genomes reveals different plant cell wall degrading capacity in fungi.BMC Genomics14:274. 10.1186/1471-2164-14-274

  • Pubmed Abstract
  • CrossRef
  • Google Scholar

• 183

  ZhengA.LinR.ZhangD.QinP.XuL.AiP.et al (2013). The evolution and pathogenic mechanisms of the rice sheath blight pathogen.Nat. Commun.4:1424. 10.1038/ncomms2427

  • Pubmed Abstract
  • CrossRef
  • Google Scholar

• 184

  ZhouB. J.JiaP. S.GaoF.GuoH. S. (2012). Molecular characterization and functional analysis of a necrosis-and ethylene-inducing, protein-encoding gene family from Verticillium dahliae.Mol. Plant Microbe Interact.25964–975. 10.1094/MPMI-12-11-0319

  • Pubmed Abstract
  • CrossRef
  • Google Scholar

• 185

  ZhuW.RonenM.GurY.Minz-DubA.MasratiG.Ben-TalN.et al (2017a). BcXYG1, a secreted Xyloglucanase from Botrytis cinerea, triggers both cell death and plant immune responses.Plant Physiol.175438–456. 10.1104/pp.17.00375

  • Pubmed Abstract
  • CrossRef
  • Google Scholar

• 186

  ZhuW.WeiW.WuY.ZhouY.PengF.ZhangS.et al (2017b). BcCFEM1, a CFEM domain-containing protein with putative GPI-anchored site, is involved in pathogenicity, conidial production, and stress tolerance in Botrytis cinerea.Front. Microbiol.8:1807. 10.3389/fmicb.2017.01807

  • Pubmed Abstract
  • CrossRef
  • Google Scholar