Citation: Nataša Čerekovic, Palmiro Poltronieri. Plant signaling pathways activating defence response and interfering mechanisms by pathogen effectors, protein decoys and bodyguards[J]. AIMS Molecular Science, 2017, 4(3): 370-388. doi: 10.3934/molsci.2017.3.370
| [1] | Laura Serna . Crosstalk among hormones and signaling networks during stomatal development in Arabidopsis hypocotyls. AIMS Molecular Science, 2016, 3(4): 550-559. doi: 10.3934/molsci.2016.4.550 |
| [2] | Stephen Schultz, Dario Siniscalco . Endocannabinoid system involvement in autism spectrum disorder: An overview with potential therapeutic applications. AIMS Molecular Science, 2019, 6(1): 27-37. doi: 10.3934/molsci.2019.1.27 |
| [3] | Seidu A. Richard, Wu Min, Zhaoliang Su, Hua-Xi Xu . Epochal neuroinflammatory role of high mobility group box 1 in central nervous system diseases. AIMS Molecular Science, 2017, 4(2): 185-218. doi: 10.3934/molsci.2017.2.185 |
| [4] | Marta Monzón . Approaches to therapy against prion diseases focused on the individual defence system. AIMS Molecular Science, 2017, 4(3): 241-251. doi: 10.3934/molsci.2017.3.241 |
| [5] | Nicola Gaetano Gatta, Rosaria Romano, Elenamaria Fioretti, Vittorio Gentile . Transglutaminase inhibition: possible therapeutic mechanisms to protect cells from death in neurological disorders. AIMS Molecular Science, 2017, 4(4): 399-414. doi: 10.3934/molsci.2017.4.399 |
| [6] | Valentina Contrò, John R. Basile, Patrizia Proia . Sex steroid hormone receptors, their ligands, and nuclear and non-nuclear pathways. AIMS Molecular Science, 2015, 2(3): 294-310. doi: 10.3934/molsci.2015.3.294 |
| [7] | Giulia Ambrosi, Pamela Milani . Endoplasmic reticulum, oxidative stress and their complex crosstalk in neurodegeneration: proteostasis, signaling pathways and molecular chaperones. AIMS Molecular Science, 2017, 4(4): 424-444. doi: 10.3934/molsci.2017.4.424 |
| [8] | Renata Tisi, Marco Rigamonti, Silvia Groppi, Fiorella Belotti . Calcium homeostasis and signaling in fungi and their relevance for pathogenicity of yeasts and filamentous fungi. AIMS Molecular Science, 2016, 3(4): 505-549. doi: 10.3934/molsci.2016.4.505 |
| [9] | Jehad Shaikhali, Gunnar Wingsle . Redox-regulated transcription in plants: Emerging concepts. AIMS Molecular Science, 2017, 4(3): 301-338. doi: 10.3934/molsci.2017.3.301 |
| [10] | William M. Scovell, Sachindra R. Joshi . The changing paradigm: estrogen receptor α recognition on DNA and within the dynamic nature of nucleosomes. AIMS Molecular Science, 2015, 2(2): 48-63. doi: 10.3934/molsci.2015.2.48 |
The first layer of plant defence against pathogens consists in the recognition of microbial fingerprints, called Pathogen or Microbial Associated Molecular Pattern (PAMP/MAMP), by a set of Pattern Recognition Receptors (PRR). PAMP are classified as: (1) structural PAMPs that regroup molecules like polysaccharides (and lipopolysaccharides) involved in the maintenance of the microbial cell integrity and (2) the encoded PAMPs that are made of amino acid sequences [1,2,3,4,5,6]. Both PAMPs are under similar selective pressure from PRRs, but encoded PAMPs are under selection and evolve more rapidly, thanks to genome mutations. In addition to sequence conservation, encoded PAMP are spread in several pathogens, but not present in the plant hosts. For instance, the enigmatic MAMP of Xanthomonas (eMax) protein is present in several Xanthomonads [7], flagellin is present in motile bacteria, eubacterial Elongation Factor thermo-unstable (EF-Tu) is widespread and the necrosis and ethylene inducing peptide 1 (Nep1)-Like Proteins (NLPs) are present in several plant pathogen kingdoms (bacteria, fungi and oomycetes) [9,10,11].
Among proteins recognized as PAMP, the most studied in plant defense are flagellin and EF-Tu. EF-Tu, codified by the tuf gene, is one of the most abundant proteins in bacteria and belongs to the moonlighting protein family, i.e. proteins playing several functions carried by a single polypeptide chain. EF-Tu has also been found associated with bacterial membrane [12], thus allowing its recognition by plant membrane receptors [13].
Studying the minimal eliciting peptide in Brassicaceae, elf18, Zipfel identified the EF-Tu receptor (EFR), belonging to the Leucine Rich Repeat (LRR) receptors family. The conserved N-terminus has been shown to elicit innate immunity in Arabidopsis plants [14,15]. EF-Tu may undergo N-terminal modifications having opposing effects. For instance, N-terminal acetylation enhances EF-Tu elicitor activity, whereas natural mutations within the 18 first amino acids of EF-Tu (elf18) lower the innate immune signaling [16]. Dicotyledonous plants (dicots) show differential responses to the K2R substitution in elf18. Xanthomonas campestris pv. campestris B100 produces an elf18B mutant while elf18G is present in Pseudomonas syringae pv. tomato DC3000, with lower activation of Hypersensitive Response (HR). Solanaceae plants lack a functional EFR, thereby relying on other PAMP sensing receptors.
Although monocotyledonous plants (monocots) lack elf18 recognition system [17], it has also been shown that a second and distinct EF-Tu epitope is able to induce immune responses in rice [18]: an EF-Tu middle region comprising Lys176 to Gly225, termed EFa50, is fully active as a PAMP in rice. In the leaves of rice plants, EF-Tu induced H2O2 generation and callose deposition, and also triggered resistance to co-infection with pathogenic bacteria.
Flagellin is recognized in plants by at least three flagellin receptors [8,19,20], specific to different plant lineages. Flagellin Sensing 2 (FLS2) is the receptor for the 22 amino acid peptide (flg22) derived from flagellin. Other flagellin receptors recognise longer peptides. FLS3 senses a 28 amino acid peptide derived from flagellin in tomato [19], while in rice an LRR receptor is able to recognise a flagellin C-terminal peptide [21,22,23,24]. Flagellin triggers cell death in tobacco thanks to bacterial O-glycosylation of the hypervariable part of flagellin [22,25,26]. The flagellin C-terminal is glycosylated with several glycan repeats in Acidovorax avenae and Pseudomonas syringae pv. tabaci 6605.
An evasion mechanism is exemplified by the evolution of the flagellin-encoding genes in plant pathogens Ralstonia solanacearum or Xanthomonas campestri pv campestris B186 (XccB186) to evade FLS2 recognition [27,28].
A different evasion strategy is exemplified by the Pseudomonads AprA protein, which digests monomeric flagellin, thus hampering plant FLS recognition [29].
In plants, nucleotide-binding domain (NBD)-and leucine-rich repeat (LRR)-based receptors and receptor like proteins (RLPs), lacking the cytoplasmic kinase domain, are sentinels of plant immunity that monitor host proteins for perturbations induced by pathogen released proteins, able to trigger defence signals [5,30]. In LRR receptors, the hydrophobic LLR domains are exposed on external protein surfaces, thus determining protein-protein interaction modules. Plants evolved this protein-protein interaction domain several times during the development of mechanisms to defend themselves from viruses, virulence factors, enzymes and effectors of bacterial and fungal pathogens. RLKs, once activated by their ligands, form a complex with their co-receptors, such as BRI-ASSOCIATED RECEPTOR KINASE 1/SOMATIC EMBRYOGENESIS RECEPTOR KINASE 3 (BAK1/SERK3) [6,7,31,32,33,34,35,36,37], allowing trans-phosphorylation between BAK1 and FLS2 or EFR kinase domains. After flg22 binding, FLS2 releases BOTRYTIS-INDUCED KINASE 1 (BIK1) and associates with BAK1.
A GxxxGxxxG motif in the trans-membrane (TM) domain of LRR receptors and RLPs, is essential for interaction with SUPPRESSOR OF BIR1-1/EVERSHED (SOBIR1/EVR) [31]. LRR-RLPs constitutively interact with SOBIR1, with interplay of kinase activity and reciprocal phosphorylaton. Upon ligand perception by LRR-RLP, the associated SOBIR1 in turn interacts with BAK1/SERK3, suggesting that a similar downstream signalling pathway is activated (Figure 1). Peptide ligand receptor complex formation has been shown to follow a two step phase: flg22 first triggers RLK heterodimerization and later assembly into larger complexes through homomerization [35]. This event initiates downstream signalling for defence activation, followed by internalization of the activated PRR complexes through endocytosis, that poses an end to the signal allowing reconstitution of the receptors onto the membranes (figure 2). The downstream signalling results in the activation of a plant response, including transcription of Pathogenesis-related (PR) proteins.
Figure 1. Formation of the LRR Receptor/co-repceptor kinase complex. EFR-SOBIR1-SERK complex and heterodimerization. After trans-phosphorylation beween the kinase domains, receptor endocytosis switches off the signal.
Figure 2. Activation of SOBIR1 and trans location. Protein folding by Endoplasmic Reticulum Quality Control (ERQC) system is needed for kinase domain co-receptors such as SOBIR1, cooperating with FLS2 and EFR, and with Cf9 protein (Receptor for Cladosporium Avr9) and Cf4 (for Avr4) in tomato. When brefeldin A, an inhibitor of translocation from ER to Golgi compartment and to plasma membrane, is added, the translocation to the membrane compartment does not occur. The formation of the complex with the LRR Receptor requires specific conditions, such as higher temperature and exposure for a minimum time before the creation of high affinity interaction.The signaling pathway that lead to plant defence involves the phosphorylation of LRR-receptors, their translocation from membranes to vacuoles, as a negative feedback, the activation of downstream Mitogen Activated Protein Kinase Kinases (MAPKKs). MAPKKs signaling is involved in plant defense, regulation of vesicle trafficking, activation of Transcription Factors (TFs), and transcription of target genes such as AVR9/CF-9 RAPIDLY ELICITED 132 (ACRE132) and HAIRPIN INDUCED 1 (Hin1) whose expression as defense-related marker genes denotes the efficacy of the treatment experiments.
The plant LRR-Ⅻ family, differentially expanded in rice and Arabidopsis, includes either FLS2 and Xa21 [34]. PTI responses include the production of reactive oxygen species (ROS) [30], callose deposition in the plant cell wall, stomatal closure and the activation of defense-related genes, and interfere with the survival and multiplication of non-adapted microbial invaders [38,39,40,41]. ROS are generated in the apoplast by the respiratory burst oxidase homologs (RBOHs) [39,40,42], and the RLK signaling and ROS production are each influenced by the other (crosstalk).
The growth hormones jasmonic acid (JA); salicylic acid (SA); ethylene (ET), indole acetic acid (IAA); gibberellic acid (GA), activate signaling pathways that drive changes in gene expression, resulting in specific defense responses and induction of pathogenesis-related proteins. Defense comes at the cost of reduced growth, and plants have evolved strategies to minimize costs and optimize the balance between growth and defense [43]. Different cellular pathways, dependent on phytohormones-activated Transcription Factors, bring to the expression of defense proteins.
Jasmonate is known to regulate abiotic and biotic stress response: its active compound, 7-iso-jasmonic acid-isoleucine (JA-Ile), releases the JASMONATE-ZIM-DOMAIN (JAZ) repressor from the transcription factor MYC2, containing the G-box domain; JA also activates transcription factors involved in abiotic stress, that are ethylene and JA regulated, containing the GCC motif [44,45,46].
The induction of defence proteins such as pathogenesis-related protein 1 (PR1) and pathogen-induced defensin (PDF1.2) marker genes has been extensively used as marker of plant defense regulated by SA and JA, respectively. The mon-expressor of pathogenesis-related genes1 (NPR1) is a well known master regulator of gene expression during immune response, a transcription activator sensing the redox state of the plant cell. NPR1 binds directly to SA via two cysteine residues. Upon SA treatment, NPR1 oligomers are monomerised due to a change in the intracellular redox status. NPR1 monomers are translocated to the nucleus where they activate gene expression [47].
The plant hypersensitive response (HR) leading to disease resistance is characterized by the rapid accumulation of nitric oxide (NO). Nitrosylation of cysteines in enzymes of JA synthesis have been found to be important in regulating JA signaling. In plants, NO-mediated nitrosylation activates transcription factors such as MYB (MYeloBlastosis gene), a basic helix-loop-helix (bHLH) TF, involved in JA-dependent signaling. SA binding protein 3 (SABP3), modulating the SA response and integrating the JA signaling, is nitrosylated by NO during the hypersensitive response (HR) [45].
This NO signaling triggers localized hypersensitive cell death, inducing sets of defence genes, and mediates a network that is involved in the establishment of Systemic Acquired Resistance (SAR). In general, local and systemic defense response, including systemic acquired resistance (SAR), against biotrophic pathogens is mediated by SA, whereas JA and ET mediate responses against necrotrophs. The crosstalk between SA and JA pathways can be either mutually antagonistic or synergistic.
There are several mechanisms that pathogens use to switch off plant defense activation Pathogens secrete toxins and/or effector proteins able to hijack PTI signaling and to inactivate PRR-based defences, in order to allow nutrients availability, and to support pathogen spread. Large repertoires of effector activities have been found for pathogens with different lifestyles. There are effectors in extracellular bacteria released in host cells by type Ⅲ secretion system (TTSS) (T3S); other effectors in oomycetes and fungi able to invaginate specialized feeding organelles, called haustoria, into host cells. The effectors are proteins or secondary metabolites that subvert host physiology for the advantage of the pathogens. The effector proteins are delivered into the host plant to manipulate host defence in several ways, by protein post-translational modification, exerting a wide range of enzymatic modifications, or targeting host proteins to degradation, interfering with phytohormone signaling, vesicle transport and the formation of the cytoskeleton, and by nuclear localisation, acting as transcription factors modifying gene expression profiles. These effectors, named Avirulence (Avr) genes, or Xop genes for Xanthomonas oryzae pathogenesis genes, modify and inactivate a series of plant signaling pathways leading to a block in plant immune defences [48,49,50,51,52,53].
Effectors represent adaptation to hosts, evolved from genes and functions from saprotrophic ancestors and plant symbionts, from molecules used to suppress ecological competitors. Effectors from evolutionarily diverse pathogens are highly specialised and specific for a limited number of plant proteins with activity and role linked to plant immunity.
The effectors are recognised by plant receptors sensing their presence of their cognate avirulence genes. For instance, the receptors for Cladosporium fulvum (Cf) Avr effectors are RLPs that lead to the formation of protein complexes. The tomato SOBIR1 acts as a co-receptor for Cf proteins. These effectors have been numbered according to the sequential order of discovery.
The Cf receptors, originated from recombination during evolution, are present only in some specific tomato genotypes, leading to race-specific resistance and a strong Hypersensitive Response (HR). This leads to effector triggered immunity (ETI). It has been shown that PTI and ETI have similar anti-pathogen outputs: the effector-triggered immune response is stronger, but race specific, leading to a localised programmed cell death (PCD) or to necrosis, for the containment of pathogen spread, contributing to HR.
Botrytis and Pythium are necrotrophic pathogens, that destroy plant tissues with limited species specificity [52]. The pathogenicity is based on degrading enzymes or toxic metabolites, with a limited number of effectors produced, and cell killing protein toxins. Other fungi have a highly specialized life cycle and restricted host range. The fungi start a growth within the plant apoplast without any symptom, then pathogens produce metabolites and toxins targeting specifically gene products, i.e., a single gene of the pathogen interacts with a single gene of the plant to induce susceptibility [49]. Biotrophic pathogenic fungi, such as rust, powdery mildew, or white rust and downy mildew oomycetes, show host specificity and dependence on the host plant for metabolites. In this case, evolution toward pathogenicity has led to genome shrinking with loss of genes involved in nutrient acquisition, with expansion of effector genes [49].
To protect the effectors from host proteases, fungi evolved several mechanisms of protease inhibition [54]. Many effector proteins secreted into the apoplast are rich in cysteine residues forming cystine knots and disulfide bridges, that increase protein stability in a protease-rich environment, or have high affinity to plant proteases [54,55,56,57,58,59,60,61,62].
Many pathogen effectors are inhibitors of plant proteases [55,56]. The tomato cysteine proteases Rcr3, Pip1, aleurain, and TDI-65 are necessary during basal host defence against fungal pathogens. Pip1 and Rcr3 are strongly induced by fungal effectors and by hormones such as salicylic acid (SA) [56].
Cystatin-like Ehttps://www.aimspress.com/aimspress-data/aimsmoles/2017/3/PIC proteins, secreted by the oomycete Phytophthora infestans, target the C14 proteases in Solanaceae. P. infestans (Pinf), during tomato infection produces Ehttps://www.aimspress.com/aimspress-data/aimsmoles/2017/3/PIC1 and Ehttps://www.aimspress.com/aimspress-data/aimsmoles/2017/3/PIC2b (effector protease inhibitor, cystatin-like), cysteine protease inhibitors that target two tomato proteases, C14 and Phytophthora-inhibited protease-1 (Pip1) [50,51]. The P. infestans EPI1 and EPI10 protease inhibitors [56], induced during infection, interact and inhibit the P69B cysteine protease in tomato apoplast [55]. Oomycetes can produce up to 12–15 Kazal type serine protease inhibitors [56]. In maize, fungal cysteine protease inhibitor Pit2 binds and inhibits CP2, CP1A and CP1B proteases. AvrP123, in Melampsora lini, is a Kazal-like proteinase inhibitor [57].
In Arabidopsis, pathogen Hyaloperonospora arabidopsidis (Hpa) produces cystatin-like Ehttps://www.aimspress.com/aimspress-data/aimsmoles/2017/3/PIC inhibitors targeting RD21 cysteine protease. The rd21 plant mutants were shown susceptible to Botrytis cinerea infection [59].
Effector proteins from Ustilago maidis can block plant immune responses by inhibiting the expression of cysteine proteinase C69 [60].
On the other side, pathogens relay on proteases for the digestion of plant tissues [62]. Therefore, plants acquired a large spectrum of proteinase inhibitors to fight and block the pathogen proteases. Protease inhibitors belonging to the Kunitz family are present in higher plants, such as Solanaceae. Potato, tomato and other Solanaceae contain various Kunitz-type protease inhibitors (PKPIs), with a size of 24,000 Dalton (Da) [63]. Potato tubers infected by Aspergillus carbonarius accumulated several inhibitors with specificity toward different proteases, such as trypsin/chymotrypsin inhibitors in the early phase of infection, followed by papain, ficin, bromelain and cathepsin B inhibitors in later stage of infection [63]. It may be possible that KPIs are processed, as the PKPI P58514.2 [64], a strong inhibitor of P. infestans infection.
In tomato, the Kunitz-type proteinase inhibitor 4 (KTI4), with size 21 kDa, functions downstream of the vacuolar protease SlVPE3. The suppression of expression of VPE3, by gene silencing, affects fruit susceptibility to pathogen infection and fruit disease resistance. The susceptibility of tomato fruit to necrotrophic pathogens such as Botrytis cinerea increases during fruit ripening: KTI4 requires a processing by SlVPE3 into smaller peptides, since their presence is related to tomato resistance to B. cinerea [65].
During infection, C. fulvum produces several effectors with protease inhibitor function. Both Rcr3 and Pip1 plant proteases are inhibited by Avr2 from C. fulvum. Avr2, being a cystatin, inhibits tomato cysteine proteases, including Rcr3, Pip1, aleurain, and TDI-65, important in basal host defence.
The binding of Avr2 to Rcr3 causes the recognition of the complex by tomato Cf-2 immune receptor [59]. When Avr2 binds to Rcr3, this interaction is sensed by Cf-2 leading to Effector Triggered Immunity (ETI).
Avr2 inhibits also Arabidopsis cysteine proteases. XCP2, RD21A and Responsive to Dehydration 21B (RD21B) were identified using yeast two-hybrid assays as interacting partners of protease inhibitors in Arabidopsis [56], that stabilise XCP2. In a biochemical study, XCP1, XCP2 and CPR1 showed high Avr2 affinity, while Responsive to Dehydration 21A (RD21A), aleurain and aleurain-like thiol proteases had low Avr2 affinity [54,55,56,57,58,59,60,61,62].
Rcr3, targeted by Avr2, is involved in basal defense and satisfies the definition of a pathogenesis-related (PR) protein [60].
The guard model hypothesis proposed by Jones and Dangl requires that some R proteins monitor a pathogen effector target rather than interact directly with their cognate pathogen effector. If a pathogen effector mutates to enable modification of the guard-target without being detected by the guard, then the guard and guard-target complex come under evolutionary pressure to regain recognition capacity or avoid modification by the effector or both [66].
The Cf-2–Rcr3–Avr2 interaction is a well-characterized example of an interaction in the tomato–C. fulvum pathosystem that conforms to the guard hypothesis. Rcr3 has the hallmarks of pathogen-driven positive selection. First, it belongs to a multigene family that resides in a complex locus with five paralogs, including Pip1, which is also targeted by Avr2 [60]. Second, there is evidence for divergent selection in and around the substrate-binding grooves in Rcr3 and Pip1 [60].
AvrECP1, AvrECP2, AvrECP4, AvrECP5 and AvrECP7 are secreted cysteine-rich proteins. This property may confer increased resistance to proteolysis and highly compacted structure. AvrECP6 encodes a larger protein containing three LysM carbohydrate-binding domains that may bind chitin. To date, 11 different ECP and Avr genes have been cloned, and at least additional eight are predicted, based on distinct gene-for-gene interactions [67,68,69,70,71].
Resistance genes conferring recognition of ECP1, ECP2, ECP4, and ECP5 have been identified from L. pimpinellifolium and were found to map to a cluster of Homologs of Cladosporium-resistance gene Cf-9 (Hcr9) genes, located on the short arm of tomato chromosome 1.
Avr9B targets a basal defense protein that is significantly upregulated or only expressed in adult plants. Cf-9B recognizes a necrosis-inducing protein (NIP) present in the apoplast of Nicotiana benthamiana (N. benthamiana). The necrosis-inducing protein in N. benthamiana corresponds to the protein targeted in tomato by Avr9B, the complex being recognised by Cf-9B. The heterologous expression of Cf-9B and the Hcr9 genes Peru1 and Peru2 triggers necrosis in a number of Nicotiana species [67,68,69,70,71].
Avr9 is sensed by Cf-9. Avr9 in C. fulvum is a protease inhibitor with a cysteine-knot structure, resembling a carboxypeptidase inhibitor [60]. Avr9 is recognised by High Affinity Binding Sites (HABS) on plasma membrane, and this interaction is sensed by the LRR receptor Cf-9, triggering receptor activation and signaling.
In Solanaceae, the pattern of responses to Cf-9 alone or in combination with Avr9 is mirroring the response to Cf-4 alone or in combination with Avr4 [61,72]. Assuming that the Cf-4–Avr4 interaction is direct, it is deduced that also Cf-9–Avr9 interaction is direct, probably depending on the binding of Avr9 to HABS present in Solanaceae. A difference between Cf-9 and Cf-4 is found in lettuce, which responds to Cf-4/Avr4 interaction but not to Cf-9–Avr9 interaction. Presumably the failure of the Cf-9–Avr9 combination to do so can be attributed to the absence of the HABS in lettuce.
Pseudomonas syringae employs a type Ⅲ secretion system to inject 20–30 different type Ⅲ effector (T3SE) proteins into plant host cells [73].
The P. syringae YopJ/HopZ superfamily of T3SEs has acetyltransferase activity. Acetylation of an NB-LRR plant immune-effector complex suppresses immunity.
HopAO1, secreted by P. syringae, is a tyrosine phosphatase that reduces EFR phosphorylation and prevents PTI (43, 50). XopE1 and XopE2 belong to the HopX (AvrPphE) family of putative transglutaminases with different enzymatic activities like proteases, peptide N-glycanases, and DNA repair proteins [47,74,75].
Many plant receptors for avirulence genes are LRR proteins acting in concert with co-receptor kinases. The presence of pseudokinases devoid of activity interferes with effector function [72,73,74]. There is a competition between the pseudokinase and the pathogen effector for its natural target, with a sponge effect.
The Arabidopsis Nucleotide-binding domain LRR (NLR) protein AtZAR1 (acronym for HOPZ-ACTIVATED RESISTANCE1) was shown to require the ZED1-RELATED KINASE (ZRK) ZRK3. ZED is the pseudokinase, acting as a complex formation hub. HopZ1a is an acetyltransferase that acetylates the pseudokinase AtZED1 and triggers recognition by AtZAR1[76,77,78,79].
HOPZ-ETI-DEFICIENT1 (AtZED1) is a receptor-like cytoplasmic protein that recognizes the Pseudomonas syringae (PtoDC3000) type Ⅲ effector HopF2a. HopF2a does not directly ADP-ribosylate ZRK3: probably ZRK3 acts as an adaptor between AtZAR1 and an unidentified kinase that is modified by HopF2a. AtZAR1 is thus a recognition hub able to activate three LLR proteins (AtZED1, ZRK3, and RKS1) of the type Ⅻ Receptor family, to sense three T3S effectors that have different enzymatic activities and are from different bacteria [76].
AvrAC (XopACXcc) uridylates BIK1 kinase, with inhibition of BIK1 phosphorylation. PBL2, a paralog of BIK1, is similarly uridylated by AvrAC. However, in contrast to BIK1, PBL2 uridylation is specifically required for host recognition of AvrAC to trigger immunity, but not AvrAC virulence. PBL2 thus acts as a decoy and enables AvrAC detection [75].
Among bacterial effectors that interfere with post-translational modifications, HopM1 interacts and induce degradation of an ADP-ribosylation factor-guanine nucleotide exchange factor (ARF-GEF) involved in vesicle trafficking. Some pathogen effectors such as HopU1, HopF2, and AvrRpmi1 are toxins belonging to cholera-like (C type) ADP Ribosyl Transferases (ART): HopU1 ADP ribosylates and inactivates GRP7 RNA binding protein; while HopF2 is a diphtheria-like (D type) ART that modifies MAPKKs. XopQXoo is present in complex with adenosine diphosphate ribose, thus mimicking a Macrodomain protein, thus possibly interfering with ADP ribose hydrolases or masking these post-translational modifications [43,75].
In general, the mechanisms of defence of plants against pathogens involve numerous signals, starting with detection of pathogen-derived PAMPs and effectors molecules, followed by signal transduction from receptors to transcription factors, to the production of antimicrobial molecules and plant cell death.
There are effectors grouped for their roles as defensive effectors, in symbiotic bacteria, that interfere with some component of the plant immune system to protect the symbiosis, and offensive effectors that subvert some physiological functions of the plant for the benefit of the symbiont, i.e. to increase nutrient availability. Host physiological networks may trigger plant immunity and cause cell death while suppressing defence functions to promote nutrition. In addition, for the symbionts, it is necessary to avoid host cell death, while for a hemibiotroph apoptosis may be beneficial or undesirable, depending on the timing of the infection.
FLS2 in Vitis vinifera, VvFLS2 differentially recognizes flagellin-derived epitopes from the endophytic growth promoting bacterium Burkholderia phytofirmans and plant pathogenic bacteria [80].
PTI can also lead to a reduction in type Ⅲ-dependent effector protein translocation, suggesting that plants actively interfere with the expression of T3S genes and/or T3S-dependent protein delivery. It was postulated that mychorrizal fungi and bacteria promoting plant growth modulate the PTI signaling and are able to suppress chitin recognition in favour of the establishment of symbiosis [81,82,83,84,85].
Plant-fungi interactions, as well as plants with other invaders, have shown an evolutionary adaptation of hosts and invaders to produce enzymes and evolve new enzyme inhibitors. Among these products, are protein decoys and bodyguards, able to bind or mimic the targets of plant enzymes in order to act as a sponge. Microbial decoys are proteins mimicking the interaction domain of a protein partner, thus impeding its accessibility, or enzymes interfering with a plant defence mechanism [86,87,88]. Such decoys have been also named bodyguards, in that they are able to protect virulence factors from the action of resistance genes and plant defence pathways.
Glucanases are enzymes that degrade cell walls. Botrytis cinerea produces the family 11 xylanase that is blocked by the plant with production of endoxylanase inhibitors XIP-1 and TAXI-1 [52]. Phytophtora sojae secretes a xyloglucanase that damages soybean cell walls. Soybean, in turn, secretes a defense protein, Glucanase inhibitor protein-1 (GIP1) that binds endo β-1, 3-glucanases. To counteract this plant defense, the oomycete deploys a secreted apoplastic xyloglucan-specific endoglucanase, PsXEG1, and the PsXEG1-like PsXLP1, that binds to GmGIP1 more tightly than does PsXEG1, an inactive enzyme that sequesters the plant inhibitor as a decoy, allowing the oomycete to invade the soybean cells. The gene pair encoding PsXEG1 and PsXLP1 is conserved in many Phytophthora species, and the P. parasitica orthologs PpXEG1 and PpXLP1 have similar functions [86,87,88]. The apoplastic decoy strategy may be widely used in Phytophthora pathosystems.
Chitin and the oligomers derived from the catabolism are sensed as molecular patterns. Fungi deacetylate the N-acetyl-glucosamine present in chitin in order to prevent its recognition as a PAMP. Furthermore, fungi have evolved protein decoys able to interfere with this recognition. Chitin hiding proteins thus antagonise and interfere with plant Chitin Binding Domain-chitinases.
Finally, recent findings disclosed the role of pathogen bodyguards, proteins interfering with plant defence mechanisms, such as the mimicking Transcription Activator Like Effectors (TALE) [50], found in Ralstonia solanacearum and in Xanthomonads.
TAL effectors are able to activate expression of genes that induce plant defences. TALE proteins have a Nuclear Localisation Domain (NLS) and an acidic activation domain (AD), for the activation of the transcription machinery and expression of genes.
Xanthomonas AvrBs3 or TAL family infect more than 200 different plant families. According to their narrow host range, individual Xanthomonas strains are grouped into different pathovars (pv.). Some pathovars cause localised leaf spots and multiply extracellularly, within the leaf mesophyll or apoplast. In contrast, pathovars such as Xanthomonas campestris pv. campestris (Xcc) and Xanthomonas oryzae pv. oryzae (Xoo) have access to the plant vascular system (xylem), spread systemically throughout the plant, and cause black rot or leaf blight disease [46]. Xanthan, released by Xanthomonas, blocks the xylem system causing wilting.
The pepper (Capsicum annuum) resistant cultivars Early Cal Wonder (ECW) carries the Bs1 and Bs3 dominant resistance (R) genes.
The TAL effectors AvrXa7, PthXo1, PthXo2, PthXo3 from Xoo, and PthA and PthB from X. citri pv. citri are major virulence determinants [50,89].
Os8N3/Xa13 is a rice target gene induced by PthXo1 [46]. The recessive xa13 allele acts as an R gene against Xanthomonas infections. Resistance is based on lack of PthXo1-mediated Os8N3 expression in xa13 homozygous plants.
A prototype of the resistance genes recognizing a TAL effector was Xa27 [46]. Xa27 is expressed only in resistant lines during Xanthomonas infection.
Thereafter, the pepper Bs3/avrBs3 dependent HR was studied [50,89]. Cloning of the Bs3 gene from pepper resistant variety ECW-30R showed that Bs3 expression and the HR depend on binding of AvrBs3 to a specific DNA element (UPA box) in the Bs3 promoter. Bs3 encodes a flavin monooxygenase (FMO). At least two additional R genes from rice (Xa7, Xa10) are under investigation. Bs4 is a TIR-NB-LRR protein that localizes to the plant cell cytoplasm, where it directs recognition of AvrBs4 TAL effector.
Nuclear Localisation Sequence (NLS) and Acidic Activation Domain (AD) in AvrBs3 are features typical of eukaryotic motifs, and are conserved: thus, AvrBs3 should have a functional role in plant cells. R genes detecting TAL effectors require the NLS and the AD in their sequence. For the mechanism of recognition, these molecular traps have been termed decoys.
Only a few effectors were shown to be major virulence factors because their deletion leads to a dramatic loss of virulence. AvrBs2 from the pepper and tomato pathogen X. campestris pv. vesicatoria strongly contributes to the multiplication of the bacteria in planta, while mutations in AvrXccC and XopXccN from X. campestris pv. campestris only weakly affect bacterial growth [50,89]. Several recent studies suggest that effectors of Pseudomonas and XopX from X. campestris pv. vesicatoria promote lesion development and growth in Nicotiana benthamiana through suppression of basal plant defense.
Interfering TALEs (iTALEs) are pathogen effectors able to overcome disease resistance [89]. In comparison with typical TALEs, iTALEs lack a transcription activation domain but retain nuclear localization motifs and are expressed from genes previously considered pseudogenes. The rice gene Xa1, encoding a nucleotide-binding leucine-rich repeat protein, was shown to confer resistance against X. oryzae isolates by recognizing multiple TALEs.
However, the presence of iTALEs in many isolates is able to interfere with the broad-spectrum resistance conferred by Xa1. Xa1 activates resistance, hypersensitive response (HR) and cell death, but this activation is suppressed by iTALEs expressed in Xoo and Xoc.
The growth hormones jasmonic acid (JA); ethylene (ET), salicylic acid (SA); indole acetic acid (IAA); gibberellic acid (GA), activate signaling pathways that drive changes in gene expression, resulting in specific defense responses and induction of pathogenesis-related proteins.
Oxylipins, and in particular the lipoxygenase pathway leading to synthesis of JA, are well known regulators of the signaling pathways in response to biotic stresses, in some case overlapping with SA signaling [90,91,92,93,94,95,96,97]. Azelaic acid (AA) has been suggested to be a phloem-mobile signal that primes SA-induced defenses: its biosynthesis pathway is still unknown, being a derivative of oleic acid or its desaturated derivatives, linoleic and linolenic acids, through the activity of lipoxygenases and oxylipin synthesis genes.
Other plant secondary metabolites, such a nitric oxide (NO), contribute to the regulation of JA synthesis and SA-dependent gene expression, including microRNAs [44,45].
Priming is related to compounds able to switch an activation state: during Induced Resistance (IR) response, plants react more rapidly to a stress because they are in an induced state. It was proposed to divide the priming phenomenon into three different stages: a priming phase, a post-challenge primed phase, and a trans-generational primed phase [95,96,97]. In this first stage, the levels of transcripts, proteins and metabolites are altered, with the plant in a standby state. In the post-challenge primed state, reactions fighting the stressor are induced rapidly. In the third phase, plants generated from seeds of primed plants show a priming memory and react rapidly to pathogens.
Induced resistance (IR) leads to various types of systemic resistance throughout the plant. IR is based on two general mechanisms: direct activation of defense responses in systemic tissue after local stimuli and priming, which implies activation of systemic responses, but only when the pathogen reaches these sites. The best characterized type of IR is systemic-acquired resistance (SAR), which is mostly dependent on SA, unlike the less understood JA-dependent defense.
Cross-talk between different signaling pathways has been reported to generate both synergistic and antagonistic defense responses. In some cases, this cross-talk might contribute to fine-tune defense responses against some pathogens according to its mode of infection.
Acibenzolar-S-methyl, or benzothiadiazole, is a functional analogue of SA hormone, that plays a central role in innate immunity as a co-activator of immunity-induced transcription reprogramming. Among the priming agents often used, are: methyl jasmonate, a volatile precursor of JA; beta amino butyric acid (BABA), that spread to leaves induces accumulation of SA, found important in defense against P. syringae; probenazole, inducing a general state of resistance: potassium phosphate, hexanoic acid, 2, 6-dichloroisonicotinic acid and its methyl ester (both referred to as INA), and benzo (1, 2, 3) thiadiazole-7-carbothioic acid S-methyl ester (BTH), are priming agents which trigger SAR [91,92]. Resistance elicitors such as acibenzolar-S-methyl (ASM), cis-jasmone (CJ), β-amino butyric acid (BABA), which involve SA-and JA-dependent and independent signaling pathways, are widely used in field and in agriculture, especially with Solanaceae crops.
Activators or priming compounds approved in EU are: Acibenzolar-S-methyl (benzothiadiazole) and cerevisane [93,94]. Elicitors are plant activators with plant protection effect. Among those approved in EU, are: chitosans, fructose, heptamaloxylglucan, laminarin, pepino mosaic virus strain CH2 isolate 1906, Zucchini yellow mosaic virus strain 2020 [94,95,96,97,98,99]. A possible mechanism dependent on attenuated virus recognition has been proposed as LRR-receptor dependent [100].
COS-OGA is an elicitor made of an oligosaccharidic complex comprising chitooligosaccharides (COSs) and pectin-derived oligogalacturonides (OGAs) [96]. Therefore, it results from the association of both plant non-self PAMP (chitosan, with a mean polymerization degree of 7) and altered self molecules recognised as DAMP (oligopectates with a mean polymerization degree of 11). In plant immunity, OGAs are race-nonspecific elicitors that mimic degradation of plant cell wall and middle lamella pectin by fungal polygalacturonases [96].
Sclerotinia rot is fought using the biocontrol agents Contans, Bacillus pumilus, Pythium oligandrum, and Trichoderma spp., Verticillum spp. under development. Fusarium sp. in cereals, and late blight in potato, are fought using Polyversum (Pythium oligandrum), while Pseudomonas spp. and Bacillus spp. as antagonists are under development. Soil-borne pests (Macrophomina, sp. Verticillium sp., Rhizoctonia sp., Plasmodiopora sp., Aphanomyces sp., Dickeya sp., Pectobacterium sp., Gaeumanomyces graminis) are fought using Polyversum (Pythium oligandrum), Trichoderma spp., Streptomyces spp., while Pseudomonas spp. and Bacillus spp. as antagonists, under development. Powdery and downy mildew are fought using Green pesticides, induced resistance and plant resistance elicitors and antagonists. Laminarine (brown algae) is used as biocontrol for its effect as a DAMP signal. Cydia pomanella, pathogen of apple, pear and walnut, is fought using Granulosis virus and Steinernema carpocapse.
Although there are still studies under way to establish the potential for field application and crop protection [101], the exploitation of plant immune responses and SAR through improvement of transcription factor dependent gene expression is going to increase crop production. This may combine with the identification of race-specific receptors and their introduction into susceptible varieties, to establish plant varieties with increased resistance to their pathogens.
There are several approaches possible to reinforce the immunity of plants to continuously evolving pathogen strains. The introgression of resistance genes has the main drawback that single R genes recognize only specific pathogen genotypes, whereas microbes can quickly loose effectors and evolve novel ones, thereby avoiding recognition. Previously, an effective and resistance against a broad spectrum of bacterial pathogens, was obtained by combining the Wall-associated kinase (WAK) ectodomain with the intracellular domain of FLS2 in tobacco and by transferring immune receptors among plant species, as reviewed in [102,103,104]. In ongoing research, FLS2 and EFR ectodomains were swapped with Cf9 intracellular domain, leading to enhanced activation of HR and necrotic lesions in tobacco (Unpublished results). It may be possible in the future, by exploiting novel techniques such as cisgenesis, to produce plants able to sense pathogen presence by a general PAMP and able to trigger an ETI response followed by HR. In the meantime, another strategy is to potentiate the plant surveillance system and phytohormone signaling leading to SAR by means of priming and chemicals already used in field. In addition, the activated state should not interfere with the normal plant development and the growth/defence trade off [30]. The main problems that we need to face is the differences existing among monocots and dicots, and especially the peculiar mechanisms present in Solanaceae that are not so easily transferred to other plant species. It is envisaged that in the future we will able to engineer olive trees with resistance to Xylella fastidiosa, tropical fruits with resistance to viruses, and to ensure the availability of food products ensuring food security despite the continuous appearance of novel pathogens and the transfer of new world pathogens to Europe and USA due to global trade of commodities.
The authors apologize for the many colleagues' reports not included in this review.
The authors declare no conflict of interest.
| [1] |
Erbs G, Silipo A, Aslam S, et al. (2008) Peptidoglycan and muropeptides from pathogens Agrobacterium and Xanthomonas elicit plant innate immunity: structure and activity. Chem Biol 15: 438-448. doi: 10.1016/j.chembiol.2008.03.017
|
| [2] |
Ranf S, Gisch N, Schaffer M, et al. (2015) A lectin S-domain receptor kinase mediates lipopolysaccharide sensing in Arabidopsis thaliana. Nature Immunol 16: 426-433. doi: 10.1038/ni.3124
|
| [3] |
Cook DE, Mesarich CH, Thomma BP (2015) Understanding plant immunity as a surveillance system to detect invasion. Annu Rev Phytopathol 53: 541-563. doi: 10.1146/annurev-phyto-080614-120114
|
| [4] |
Klarzynski O, Plesse B, Joubert JM, et al.(2000) Linear beta-1,3 glucans are elicitors of defense responses in tobacco. Plant Physiol 124: 1027-1038. doi: 10.1104/pp.124.3.1027
|
| [5] |
Monaghan J, Zipfel C (2012) Plant pattern recognition receptor complexes at the plasma membrane. Curr Opin Plant Biol 15: 349-357. doi: 10.1016/j.pbi.2012.05.006
|
| [6] |
Zhang L, Kars I, Essenstam B, et al. (2014) Fungal endopolygalacturonases are recognized as microbe-associated molecular patterns by the Arabidopsis receptor-like protein RESPONSIVENESS TO BOTRYTIS POLYGALACTURONASES1. Plant Physiol 164: 352-364. doi: 10.1104/pp.113.230698
|
| [7] |
Jehle AK, Fürst U, Lipschis M, et al. (2013) Perception of the novel MAMP eMax from different Xanthomonas species requires the Arabidopsis receptor-like protein ReMAX and the receptor kinase SOBIR. Plant Signal Behav 8: e27408. doi: 10.4161/psb.27408
|
| [8] |
Zipfel C, Robatzek S, Navarro L, et al. (2004) Bacterial disease resistance in Arabidopsis through flagellin perception. Nature 428: 764-767. doi: 10.1038/nature02485
|
| [9] |
Felix G, Duran JD, Volko S, et al. (1999) Plants have a sensitive perception system for the most conserved domain of bacterial flagellin. Plant J 18: 265-276. doi: 10.1046/j.1365-313X.1999.00265.x
|
| [10] | Smith KD, Andersen-Nissen E, Hayashi F, et al. (2003) Toll-like receptor 5 recognizes a conserved site on flagellin required for protofilament formation and bacterial motility. Nature Immunol 4: 1247-1253. |
| [11] |
Oome S, Raaymakers TM, Cabral A, et al. (2014) Nep1-like proteins from three kingdoms of life act as a microbe-associated molecular pattern in Arabidopsis. Proc Natl Acad Sci USA 111: 16955-16960. doi: 10.1073/pnas.1410031111
|
| [12] |
Granato D, Bergonzelli GE, Pridmore RD, et al. (2004) Cell surface-associated elongation factor Tu mediates the attachment of Lactobacillus johnsonii NCC533 (La1) to human intestinal cells and mucins. Infect Immun 72: 2160-2169. doi: 10.1128/IAI.72.4.2160-2169.2004
|
| [13] |
Jonák J (2007) Bacterial elongation factors EF-Tu, their mutants, chimeric forms, and domains: Isolation and purification. J Chromatogr B 849: 141-153. doi: 10.1016/j.jchromb.2006.11.053
|
| [14] |
Zipfel C, Kunze G, Chinchilla D, et al. (2006) Perception of the bacterial PAMP EF-Tu by the receptor EFR restricts Agrobacterium-mediated transformation. Cell 125: 749-760. doi: 10.1016/j.cell.2006.03.037
|
| [15] |
Kunze G, Zipfel C, Robatzek S, et al. (2004) The N terminus of bacterial elongation factor Tu elicits innate immunity in Arabidopsis plants. Plant Cell 16: 3496-3507. doi: 10.1105/tpc.104.026765
|
| [16] |
Lacombe S, Rougon-Cardoso A, Sherwood E, et al. (2010) Interfamily transfer of a plant pattern-recognition receptor confer broad-spectrum bacterial resistance. Nat Biotechnol 28: 365-369. doi: 10.1038/nbt.1613
|
| [17] |
Schwessinger B, Bahar O, Thomas N, et al. (2015) Transgenic Expression of the Dicotyledonous Pattern Recognition Receptor EFR in Rice Leads to Ligand-Dependent Activation of Defense Responses. PLoS Pathog 11: e1004809. doi: 10.1371/journal.ppat.1004809
|
| [18] | Furukawa T, Inagaki H, Takai R, et al. (2013) Two distinct EF-Tu epitopes induce immune responses in rice and Arabidopsis. Mol Plant-Microbe Interact 27: 113-124. |
| [19] |
Hind SR, Strickler SR, Boyle PC, et al. (2016) Tomato receptor FLAGELLIN-SENSING 3 binds flgII-28 and activates the plant immune system. Nat Plants 2: 16128. doi: 10.1038/nplants.2016.128
|
| [20] |
Katsuragi Y, Takai R, Furukawa T, et al. (2015) C-terminal is recognised by a different flagellin sensing receptor. Mol Plant-Microbe Interact 28: 648-658. doi: 10.1094/MPMI-11-14-0372-R
|
| [21] |
Hirai H, Takai R, Iwano M, et al. (2011) Glycosylation regulates specific induction of rice immune responses by Acidovorax avenae flagellin. J Biol Chem 286: 25519-25530. doi: 10.1074/jbc.M111.254029
|
| [22] |
Hirai H, Takai R, Kondo M, et al. (2014) Glycan moiety of flagellin in Acidovorax avenae K1 prevents the recognition by rice that causes the induction of immune responses. Plant Signal Behav 9: e972782. doi: 10.4161/psb.29933
|
| [23] |
Takeuchi K, Ono H, Yoshida M, et al. (2007) Flagellin glycans from two pathovars of Pseudomonas syringae contain rhamnose in D and L configurations in different ratios and modified 4-amino-4,6-dideoxyglucose. J Bacteriol 189: 6945-56. doi: 10.1128/JB.00500-07
|
| [24] |
Che FS, Nakajima Y, Tanaka N, et al. (2000) Flagellin from an incompatible strain of Pseudomonas avenae induces a resistance response in cultured rice cells. J Biol Chem 275: 32347-32356. doi: 10.1074/jbc.M004796200
|
| [25] |
Taguchi F, Shimizu R, Inagaki Y, et al. (2003) Post-translational modification of flagellin determines the specificity of HR induction. Plant Cell Physiol 44: 342-349. doi: 10.1093/pcp/pcg042
|
| [26] |
Yamamoto M, Ohnishi-Kameyama M, Nguyen CL, et al. (2011) Identification of genes involved in the glycosylation of modified viosamine of flagellins in Pseudomonas syringae by mass spectrometry. Genes 2: 788-803. doi: 10.3390/genes2040788
|
| [27] |
Sun Y, Li L, Macho AP, et al. (2013) Structural basis for flg22-induced activation of the Arabidopsis FLS2-BAK1 immune complex. Science 342: 624-628. doi: 10.1126/science.1243825
|
| [28] |
Sun W, Dunning FM, Pfund C, et al. (2006) Within-Species flagellin polymorphism in Xanthomonas campestris pv campestris and its impact on elicitation of Arabidopsis FLAGELLIN SENSING2–dependent defenses. Plant Cell 18: 764-779. doi: 10.1105/tpc.105.037648
|
| [29] |
Pel MJC, van Dijken AJH, Bardoel BW, et al. (2014) Pseudomonas syringae evades host immunity by degrading flagellin monomers with alkaline protease AprA. Mol Plant-Microbe Interact 27: 603-610. doi: 10.1094/MPMI-02-14-0032-R
|
| [30] |
Eckardt NA (2017) The plant cell reviews plant immunity: Receptor-Like Kinases, ROS-RLK crosstalk, quantitative resistance, and the growth/defense trade-off. Plant Cell 29: 601-602. doi: 10.1105/tpc.17.00289
|
| [31] |
Bi G, Liebrand TW, Bye RR, et al. (2016) SOBIR1 requires the GxxxG dimerization motif in its transmembrane domain to form constitutive complexes with receptor-like proteins. Mol Plant Pathol 17: 96-107. doi: 10.1111/mpp.12266
|
| [32] |
Albert I, Böhm H, Albert M, et al. (2015) An RLP23–SOBIR1–BAK1 complex mediates NLP-triggered immunity. Nature Plants 1: 15140. doi: 10.1038/nplants.2015.140
|
| [33] |
Heese A, Hann DR, Gimenez-Ibanez S, et al. (2007) The receptor-like kinase SERK3/BAK1 is a central regulator of innate immunity in plants. Proc Natl Acad Sci USA 104: 12217-12222. doi: 10.1073/pnas.0705306104
|
| [34] |
Chinchilla D, Zipfel C, Robatzek S, et al. (2007) A flagellin-induced complex of the receptor FLS2 and BAK1 initiates plant defence. Nature 448: 497-500. doi: 10.1038/nature05999
|
| [35] |
Schwessinger B, Roux M, Kadota Y, et al. (2011) Phosphorylation-dependent differential regulation of plant growth, cell death, and innate immunity by the regulatory receptor-like kinase BAK1. PLoS Genet 7: e1002046. doi: 10.1371/journal.pgen.1002046
|
| [36] |
Somssich M, Ma Q, Weidtkamp-Peters S, et al. (2015) Real-time dynamics of peptide ligand-dependent receptor complex formation in planta. Sci Signal 8: ra76. doi: 10.1126/scisignal.aab0598
|
| [37] | Dufayard JF, Bettembourg M, Fischer I, et al. (2017) New insights on Leucine-Rich Repeats Receptor-like kinase orthologous relationships in Angiosperms. Front Plant Sci 8: 381. |
| [38] |
Tang D, Wang G, Zhou JM (2017) Receptor kinases in plant-pathogen interactions: More than pattern recognition. Plant Cell 29: 618-637. doi: 10.1105/tpc.16.00891
|
| [39] |
Bigeard J, Colcombet J, Hirt H (2015) Signaling mechanisms in Pattern-Triggered Immunity (PTI). Mol Plant 8: 521-539. doi: 10.1016/j.molp.2014.12.022
|
| [40] |
Wu S, Shan L, He P (2014) Microbial signature-triggered plant defense responses and early signaling mechanisms. Plant Sci 228: 118-126. doi: 10.1016/j.plantsci.2014.03.001
|
| [41] |
Song WY, Wang GL, Chen LL, et al. (1995) A receptor kinase-like protein encoded by the rice disease resistance gene, Xa21. Science 270: 1804-1806. doi: 10.1126/science.270.5243.1804
|
| [42] |
Kimura S, Waszczak C, Hunter K, et al. (2017) Bound by fate: the role of reactive oxygen species in receptor-like kinase signaling. Plant Cell 29: 638-654. doi: 10.1105/tpc.16.00947
|
| [43] |
Karasov TL, Chae E, Herman JJ, et al. (2017) Mechanisms to mitigate the trade-off between growth and defense. Plant Cell 29: 666-680. doi: 10.1105/tpc.16.00931
|
| [44] |
Santino A, Taurino M, De Domenico S, et al. (2013) Jasmonate signalling in plant defense response to multiple (a)biotic stresses. Plant Cell Rep 32: 1085-1098. doi: 10.1007/s00299-013-1441-2
|
| [45] | Poltronieri P, Taurino M, Bonsegna S, et al. (2014) Nitric Oxide: Detection Methods and Possible Roles During Jasmonate-regulated Stress Response, In: Khan MN, Mobin M, Mohammad F, Corpas FJ, Authors, Nitric Oxide in Plants: Metabolism and Role in Stress Physiology, Switzerland: Springer, 127-138. |
| [46] | Santino A, Bonsegna S, De Domenico S, et al. (2010) Plant oxylipins and their contribution to plant defence. Curr Topics Plant Biol 11: 103-111 |
| [47] | Klessig DF, Tian M, Choi HW (2016) Multiple targets of salicylic acid and its derivatives in plants and animals. Front immunol 7: 206. |
| [48] |
Kay S, Bonas U (2009) How Xanthomonas type III effectors manipulate the host plant. Current Opin. Microbiol 12: 37-43. doi: 10.1016/j.mib.2008.12.006
|
| [49] |
Lee S, Yang DS, Uppalapati SR, et al. (2013) Suppression of plant defense responses by extracellular metabolites from Pseudomonas syringae pv. tabaci in Nicotiana benthamiana. BMC Plant Biol 13: 65. doi: 10.1186/1471-2229-13-65
|
| [50] |
Boch J, Bonas U (2010) Xanthomonas AvrBs3 family-type III effectors: Discovery and function. Annu Rev Physiopathol 48: 419-436. doi: 10.1146/annurev-phyto-080508-081936
|
| [51] |
Macho AP, Schwessinger B, Ntoukakis V, et al. (2014) A bacterial tyrosine phosphatase inhibits plant pattern recognition receptor activation. Science 343: 1509-1512. doi: 10.1126/science.1248849
|
| [52] | Brutus A, Reca IB, Herga S, et al. (2005) A family 11 xylanase from the pathogen Botrytis cinerea is inhibited by plant endoxylanase inhibitors XIP-I and TAXI-I. Biochem Biophys Res Commun 337: 160-166. |
| [53] | Tyler BM, Rouxel T (2012) Effectors of fungi and oomycetes: their virulence and avirulence functions and translocation from pathogen to host cells. Mol Plant Immun 123-167. |
| [54] |
Macho AP, Zipfel C (2015) Targeting of plant pattern recognition receptor triggered immunity by bacterial type-III secretion system effectors. Curr Opin Microbiol 23: 14-22. doi: 10.1016/j.mib.2014.10.009
|
| [55] | Tian M, Win J, Song J, et al. (2007) A Phytophthora infestans cystatin-like protein targets a novel tomato papain-like apoplastic protease. Plant Physiol 143: 364-377. |
| [56] |
Song J, Win J, Tian M, et al. (2009) Apoplastic effectors secreted by two unrelated eukaryotic plant pathogens target the tomato defense protease Rcr3. Proc Natl Acad Sci USA 106: 1654-1659. doi: 10.1073/pnas.0809201106
|
| [57] |
Catanzariti AM, Dodds PN, Lawrence GJ, et al. (2006) Haustorially expressed secreted proteins from flax rust are highly enriched for avirulence elicitors. Plant Cell 18: 243-256. doi: 10.1105/tpc.105.035980
|
| [58] |
Tian M, Benedetti B, Kamoun S (2005) A second Kazal-like protease inhibitor from Phytophthora infestans inhibits and interacts with the apoplastic pathogenesis-related protease P69b of tomato. Plant Physiol 138: 1785-1793. doi: 10.1104/pp.105.061226
|
| [59] |
Shindo T, Misas-Villamil JC, Hörger AC, et al. (2012) A role in immunity for Arabidopsis cysteine protease RD21, the ortholog of the tomato immune protease C14. PLoS One 7: e29317. doi: 10.1371/journal.pone.0029317
|
| [60] | Jashni KM, Mehrabi R, Collemare J, et al. (2015) The battle in the apoplast: further insights in the roles of proteases and their inhibitors in plant-pathogen interactions. Front Plant Sci 6: 584. |
| [61] |
van den Hooven HW, van den Burg HA, Vossen P, et al. (2001) Disulfide bond structure of the AVR9 elicitor of the fungal tomato pathogen Cladosporium fulvum: evidence for a cystine knot. Biochem 40: 3458-3466. doi: 10.1021/bi0023089
|
| [62] |
Pogány M, Dankó T, Kámán-Tóth E (2015) Regulatory proteolysis in Arabidopsis-pathogen interactions. Int J Mol Sci 16: 23177-23194. doi: 10.3390/ijms161023177
|
| [63] |
Poltronieri P, Liu S, Cimaglia F, et al. (2012) Characterization of Kunitz-type inhibitor B1 performance using protein chips and AFM. Sensors Actuators B Chem 168: 231-237. doi: 10.1016/j.snb.2012.04.013
|
| [64] | Valueva TA, Revina TA, Mosolov VV, et al. (2000) Primary structure of potato Kunitz-type serine proteinase inhibitor. Biol Chem 381: 1215-1221. |
| [65] |
Wang W, Cai J, Wang P, et al. (2017) Post-transcriptional regulation of fruit ripening and disease resistance in tomato by the vacuolar protease SlVPE3. Genome Biology 18: 47. doi: 10.1186/s13059-017-1178-2
|
| [66] |
Jones JD, Dangl JL (2006) The plant immune system. Nature 444: 323-329. doi: 10.1038/nature05286
|
| [67] |
Ilyas M, Hörger AC, Bozkurt TO, et al. (2015) Functional divergence of two secreted immune proteases of tomato. Curr Biol 25: 2300-2306. doi: 10.1016/j.cub.2015.07.030
|
| [68] |
Houterman PM, Ma L, van Ooijen G, et al (2009) The effector protein Avr2 of the xylem-colonizing fungus Fusarium oxysporum activates the tomato resistance protein I-2 intracellularly. Plant J 58: 970-978. doi: 10.1111/j.1365-313X.2009.03838.x
|
| [69] |
Ma L, Houterman PM, Gawehns F, et al. (2015) The AVR2-SIX5 gene pair is required to activate I-2-mediated immunity in tomato. New Phytol 208: 507-518. doi: 10.1111/nph.13455
|
| [70] |
Shabab M, Shindo T, Gu C, et al. (2008) Fungal effector protein AVR2 targets diversifying defense-related cys proteases of tomato. Plant Cell 20: 1169-1183. doi: 10.1105/tpc.107.056325
|
| [71] |
López-Solanilla E, Bronstein PA, Schneider AR (2004) HopPtoN is a Pseudomonas syringae Hrp (type III secretion system) cysteine protease effector that suppresses pathogen-induced necrosis associated with both compatible and incompatible plant interactions. Mol Microbiol 54: 353-365 doi: 10.1111/j.1365-2958.2004.04285.x
|
| [72] |
Wulff BBH, Chakrabarti A, Jones DA (2009) Recognitional specificity and evolution in the tomato–Cladosporium fulvum pathosystem. Microbiol Plant Mol Int 22: 1191-1202. doi: 10.1094/MPMI-22-10-1191
|
| [73] | Lee S, Yang DS, Uppalapati SR (2013) Suppression of plant defense responses by extracellular metabolites from Pseudomonas syringae pv. tabaci in Nicotiana benthamiana. BMC Plant Biol 13: 65. |
| [74] |
Buttner D (2016) Behind the lines–actions of bacterial type III effector proteins in plant cells. FEMS Microbiol Rev 40: 894-937. doi: 10.1093/femsre/fuw026
|
| [75] | Thieme F, Szczesny R, Urban A, et al. (2007) New type III effectors from Xanthomonas campestris pv. vesicatoria trigger plant reactions dependent on a conserved N-myristoylation motif. Mol Plant-Microbe Interact 20: 1250-1261. |
| [76] |
Seto D, Koulena N, Lo T, et al. (2017) Expanded type III effector recognition by the ZAR1 NLR protein using ZED1-related kinases. Nature Plants 3: 17027. doi: 10.1038/nplants.2017.27
|
| [77] |
Lewis JD, Lo T, Bastedo P, et al. (2014) The rise of the undead: pseudokinases as mediators of effector-triggered immunity. Plant Signal Behav 9: e27563. doi: 10.4161/psb.27563
|
| [78] |
Wang G, Roux B, Feng F, et al. (2015) The decoy substrate of a pathogen effector and a pseudokinase specify pathogen-induced modified-self recognition and immunity in plants. Cell Host Microbe 18: 285-295. doi: 10.1016/j.chom.2015.08.004
|
| [79] |
Baudin M, Hassan JA, Schreiber KJ, et al. (2017) Analysis of the ZAR1 immune complex reveals determinants for immunity and molecular interactions. Plant Physiol 174: 2038-2053. doi: 10.1104/pp.17.00441
|
| [80] |
Trda L, Fernandez O, Boutrot F, et al. (2014) The grapevine flagellin receptor VvFLS2 differentially recognizes flagellin-derived epitopes from the endophytic growth promoting bacterium Burkholderia phytofirmans and plant pathogenic bacteria. New Phytol 201: 1371-1384. doi: 10.1111/nph.12592
|
| [81] |
Zhang X, Dong W, Sun J, et al. (2015) The receptor kinase CERK1 has dual functions in symbiosis and immunity signalling. Plant J 81: 258-267. doi: 10.1111/tpj.12723
|
| [82] | Zeilinger S, Gupta VK, Dahms TE, et al. (2016) Friends or foes? Emerging insights from fungal interactions with plants. FEMS Microbiol Rev 40: 182-207. |
| [83] | Genre A, Russo G (2016) Does a common pathway transduce symbiotic signals in plant-microbe interactions? Front Plant Sci 7: 96. |
| [84] |
Rasmussen SR, Füchtbauer W, Novero M, et al. (2016) Intraradical colonization by arbuscular mycorrhizal fungi triggers induction of a lipochitooligosaccharide receptor. Sci Rep 6: 29733. doi: 10.1038/srep29733
|
| [85] |
Akamatsu A, Shimamoto K, Kawano Y (2016) Crosstalk of signaling mechanisms involved in host defense and symbiosis against microorganisms in rice. Curr Genomics 17: 297-307. doi: 10.2174/1389202917666160331201602
|
| [86] |
Shinya T, Nakagawa T, Kaku H, et al. (2015) Chitin-mediated plant-fungal interactions: catching, hiding and handshaking. Curr Opin Plant Biol 26: 64-71. doi: 10.1016/j.pbi.2015.05.032
|
| [87] | Ma Z, Zhu L, Song T, et al. (2017) A paralogous decoy protects Phytophthora sojae apoplastic effector PsXEG1 from a host inhibitor. Science 355: 710-714. |
| [88] | Paulus JK, Kourelis J, van der Hoorn RAL (2017) Bodyguards: Pathogen-derived decoys that protect virulence factors. Trends Plant Sci 22: 355-357. |
| [89] |
Ji Z, Ji C, Liu B, et al. (2016) Interfering TAL effectors of Xanthomonas oryzae neutralize R-gene-mediated plant disease resistance. Nature Comm 7: 13435. doi: 10.1038/ncomms13435
|
| [90] |
Alexandersson E, Mulugeta T, Lankinen Å, et al. (2016) Plant resistance inducers against pathogens in Solanaceae species-From molecular mechanisms to field application. Int J Mol Sci 17: 1673. doi: 10.3390/ijms17101673
|
| [91] | Borges AA, Sandalio LM (2015) Induced resistance for plant defense. Front Plant Sci 6: 109. |
| [92] |
Iriti M, Varoni EM (2017) Moving to the field: Plant innate immunity in crop protection. Int J Mol Sci 18: 640. doi: 10.3390/ijms18030640
|
| [93] |
Capanoglu E (2010) The potential of priming in food production. Trends Food Sci Technol 21: 399-407. doi: 10.1016/j.tifs.2010.05.001
|
| [94] | Aranega-Bou P, de la O Leyva M, Finiti I, et al. (2014) Priming of plant resistance by natural compounds. Hexanoic acid as a model. Front Plant Sci 5: 488. |
| [95] | Piquerez SJM, Harvey SE, Beynon JL, et al. (2014) Improving crop disease resistance: lessons from research on Arabidopsis and tomato. Front Plant Sci 5: 671. |
| [96] |
Van Aubel G, Cambier P, Dieu M, et al. (2016) Plant immunity induced by COS-OGA elicitor is a cumulative process that involves salicylic acid. Plant Sci 247: 60-70. doi: 10.1016/j.plantsci.2016.03.005
|
| [97] |
Garner CM, Kim SH, Spears BJ, et al. (2016) Express yourself: Transcriptional regulation of plant innate immunity. Sem Cell Dev Biol 56: 150-162. doi: 10.1016/j.semcdb.2016.05.002
|
| [98] |
Iriti M, Picchi V, Rossoni M (2009) Chitosan antitranspirant activity is due to abscisic acid-dependent stomatal closure. Environ Exp Bot 66: 493-500. doi: 10.1016/j.envexpbot.2009.01.004
|
| [99] |
Iriti M, Castorina G, Vitalini S, et al. (2010) Chitosan-induced ethylene-independent resistance does not reduce crop yield in bean. Biol Control 54: 241-247. doi: 10.1016/j.biocontrol.2010.05.012
|
| [100] |
Lamichhane JR, Bischoff-Schaefer M, Bluemel S, et al. (2017) Identifying obstacles and ranking common biological control research priorities for Europe to manage most economically important pests in arable, vegetable and perennial crops. Pest Manag Sci 73: 14-21. doi: 10.1002/ps.4423
|
| [101] | Gouveia BC, Calil IP, Machado JPB, et al. (2016) Immune receptors and co-receptors in antiviral innate immunity in plants. Front Microbiol 7: 2139. |
| [102] |
Brutus A, Sicilia F, Macone A, et al. (2010) A domain swap approach reveals a role of the plant wall-associated kinase 1 (WAK1) as a receptor of oligogalacturonides. Proc Natl Acad Sci USA 107: 9452-9457. doi: 10.1073/pnas.1000675107
|
| [103] | Cervone F, De Lorenzo G, Brutus A, et al. (2009) Constructs expressing chimeric receptors, and their use for controlled activation of defense responses to pathogens in plants. RM2009A000279 Patent. |
| [104] |
Rodriguez-Moreno L, Song Y, Thomma BPHJ (2017) Transfer and engineering of immune receptors to improve recognition capacities in plants. Curr Opin Plant Biol 38: 42-49. doi: 10.1016/j.pbi.2017.04.010
|
| 1. | Giuseppe Malgioglio, Giulio Flavio Rizzo, Sebastian Nigro, Vincent Lefebvre du Prey, Joelle Herforth-Rahmé, Vittoria Catara, Ferdinando Branca, Plant-Microbe Interaction in Sustainable Agriculture: The Factors That May Influence the Efficacy of PGPM Application, 2022, 14, 2071-1050, 2253, 10.3390/su14042253 | |
| 2. | Srinivasan Kameswaran, Bellamkonda Ramesh, Gopi Krishna Pitchika, Manjunatha Bangeppagari, B. Swapna, M. Ramakrishna, P. Sudhakar Reddy, 2024, Chapter 3, 978-3-031-71843-4, 69, 10.1007/978-3-031-71844-1_3 |
Nataša Čerekovic, Palmiro Poltronieri. Plant signaling pathways activating defence response and interfering mechanisms by pathogen effectors, protein decoys and bodyguards[J]. AIMS Molecular Science, 2017, 4(3): 370-388. doi: 10.3934/molsci.2017.3.370
DownLoad: 
