Impact Factor 4.298

The 1st most cited journal in Plant Sciences

This article is part of the Research Topic

Plant Immunity: From model systems to crops species

Review ARTICLE

Front. Plant Sci., 21 November 2014 | https://doi.org/10.3389/fpls.2014.00655

Molecular effects of resistance elicitors from biological origin and their potential for crop protection

  • 1Cell and Molecular Sciences, The James Hutton Institute, Dundee, UK
  • 2OMEX Agriculture Ltd., Lincoln, UK
  • 3The Division of Plant Sciences, College of Life Science, University of Dundee at the James Hutton Institute, Dundee, UK

Plants contain a sophisticated innate immune network to prevent pathogenic microbes from gaining access to nutrients and from colonizing internal structures. The first layer of inducible response is governed by the plant following the perception of microbe- or modified plant-derived molecules. As the perception of these molecules results in a plant response that can provide efficient resistance toward non-adapted pathogens they can also be described as “defense elicitors.” In compatible plant/microbe interactions, adapted microorganisms have means to avoid or disable this resistance response and promote virulence. However, this requires a detailed spatial and temporal response from the invading pathogens. In agricultural practice, treating plants with isolated defense elicitors in the absence of pathogens can promote plant resistance by uncoupling defense activation from the effects of pathogen virulence determinants. The plant responses to plant, bacterial, oomycete, or fungal-derived elicitors are not, in all cases, universal and need elucidating prior to the application in agriculture. This review provides an overview of currently known elicitors of biological rather than synthetic origin and places their activity into a molecular context.

The Role of Defense Elicitors in Plant Immunity

Plants are under constant threat of microbial pathogen attack. Plant cell walls, cuticles and phytoanticipins are preformed, physical and chemical barriers that limit access of microbes to plant cells (Underwood, 2012; Newman et al., 2013). In addition to these non-inducible defenses, plants recognize and respond to defense elicitors which are signal-inducing compounds perceived by the innate immune system that prime and/or induce defense responses (Henry et al., 2012; Maffei et al., 2012; Newman et al., 2013). Elicitor compounds can be biological in origin, derived from either the plant or the microbe, or can be synthetically generated (Walters et al., 2013). We will focus on elicitors from biological origin (Table 1) rather than synthetic analogs of known signaling or defense molecules such as Bion, acibenzolar-S-methyl (ASM), beta-amino-butyric acid (BABA), and cis-jasmone. Elicitor activity has, for example, been shown for plant-derived cell wall components such as oligogalacturonides (Ferrari et al., 2013), proteinaceous pathogen molecules such as bacterial flagellin (Gomez-Gomez and Boller, 2002), oomycete-derived elicitin INF1 (reviewed in Hein et al., 2009) and non-proteinaceous molecules such as lipopolysaccharides (Erbs and Newman, 2012). However, intact plant- or microbe-derived structures as well as highly-polymerized molecules often tend to result in few recognition responses. In contrast, leakage of metabolites or even minor or partial breakdown of complex host or pathogen molecules leads to the production of eliciting components that are biologically active.

TABLE 1
www.frontiersin.org

Table 1. List of plant-, bacterial-, oomycete-, and fungal-derived elicitor compounds, their activity against pathogens and effectiveness in plants.

The co-evolution between plants and potential microbial pathogens has been described as a zigzag model by Jones and Dangl (2006) and can also be applied to deducing the biological activity of elicitors (Figure 1). According to the zigzag model, the first inducible responses are a consequence of the perception of chemical elicitors, microbe-associated molecular patterns (MAMPs), pathogen-associated molecular patterns (PAMPs) and/or damage-associated molecular patterns (DAMPs). The latter are also known as danger-associated molecular patterns (Mazzotta and Kemmerling, 2011). MAMPs describe general microbe-derived molecules including those originating from beneficial microbes whereas PAMPs specifically describe molecules from pathogenic microbes such as fungi, oomycetes, and bacteria (Henry et al., 2012; Newman et al., 2013). Thus, PAMPS are a subgroup of MAMPs (Maffei et al., 2012). In contrast, DAMPs are typically plant-derived and are produced after, for example, wounding by insects or herbivores as well as degradation or perturbation of host molecules by microbes (Henry et al., 2012; Newman et al., 2013). All of these molecules, which could universally be described as “patterns that elicit immunity” (PEIs), are often recognized by transmembrane pattern recognition receptors (PRRs) in plant cells (Jones and Dangl, 2006; Maffei et al., 2012; Newman et al., 2013). Upon recognition of MAMP- or DAMP-derived patterns, PTI (PAMP- or pattern-triggered immunity) is activated in the plant and the perceived molecules could be described as immune elicitors. This defense reaction aims to restrict the growth of the intruder and can lead to systemic induced resistance leaving the plant less susceptible to subsequent pathogen attack (Henry et al., 2012).

FIGURE 1
www.frontiersin.org

Figure 1. Plants recognize chemical elicitors, Microbe-Associated Molecular Patterns (MAMPS) derived from non-pathogenic microbes, Pathogen-Associated Molecular Patterns (PAMPS) derived from pathogens and Damage-Associated Molecular Patterns (DAMPS) that are produced by plants upon insect, herbivore or pathogen attack, via transmembrane Pattern Recognition Receptors (PRRs). The recognition leads to the onset of defense mechanisms referred to as pattern-triggered immunity (PTI). Adapted pathogens secrete effectors that disturb plant defense mechanisms leading to effector-triggered susceptibility (ETS). Plant resistance (R) proteins recognize pathogen effectors and induce effector-triggered immunity (ETI). Treatment of plants with elicitor compounds (chemicals, MAMPs, DAMPs, or PAMPs) in the absence of adapted pathogen leads to priming and/or PTI-based immunity that put plants into an alerted stage of defense that provides some enhanced resistance toward otherwise virulent pathogens. Figure adapted from Henry et al. (2012), and Jones and Dangl (2006).

Systemic induced resistance can be divided into systemic acquired resistance (SAR) or induced systemic resistance (ISR). Systemic acquired resistance is often characterized by localized necrosis, expression of pathogenesis related (PR) protein genes, and involves the salicylic acid (SA) pathway whereas ISR is often triggered by plant growth-promoting rhizobacteria (PGPR) (Walters et al., 2013), is not associated with necrosis and involves the jasmonic acid (JA) and ethylene (ET) pathways (Walters and Heil, 2007; Henry et al., 2012). Typical responses of PTI include cell wall alterations and the production of reactive oxygen species (ROS) which can be directly cytotoxic but also play a role in signaling. Other responses comprise the production of phytoalexins, expression of PR proteins, activation of mitogen activated protein kinase (MAPK) pathways, and defense signaling involving calcium (Ca2+) influx from extracellular spaces and changes in free cytosolic Ca2+ concentrations (Garcion et al., 2007). To counteract the initial plant defense reaction, successful microbes have evolved specialized effectors that perturb recognition of defense elicitors or subsequent plant defense mechanisms to promote effector-triggered susceptibility (ETS). However, if these pathogen effectors are in turn recognized by cognate plant resistance (R) proteins, the second layer of inducible response, effector-triggered immunity (ETI), is initiated that often yields a hypersensitive resistance response (HR) (Jones and Dangl, 2006; Deslandes and Rivas, 2012).

The outcome of plant/microbe interactions can result in symbiosis, disease or disease resistance and is governed by further levels of sophisticated co-evolution. Indeed, it must be recognized that pathogen colonization of plants can generate dynamic pathogenic, mutualistic or parasitic interactions of varying magnitude and specificity. Furthermore, organisms recognized as pathogens in, for example, a crop context, could be benign or even beneficial in another context such as a different host or environment (Newton et al., 2010). It is thus essential for the plant to evaluate the scale of threat and to mount appropriate and proportionate responses. These may range from priming, being ready to respond faster to actual attack, or expression of PTI-based defense mechanisms to yield incompatibility if the microbe/pathogen is unable to suppress these responses. The use of elicitors in agriculture holds the potential to decrease the need for pesticide application by using the plant's own defense system. However, there is a need to understand this process on a molecular level to maximize the efficacy of the treatments.

Inducible Defense Response in the Absence of Pathogens

In agricultural practice, elicitor treatments of plants in the absence of virulent pathogens yields a defense response such as priming and/or PTI that is uncoupled from ETS and can provide some protection to subsequent pathogen challenges. Priming is defined as a physiological status of plants leading to faster and stronger activation of defense responses to subsequent biotic and abiotic stresses (reviewed in Conrath et al., 2006; Conrath, 2011; Pastor et al., 2013). Crucially, this is distinct from the level of resistance induction in response to the recognition of true pathogens that are potentially capable of causing disease and where recognition would cause resistance mechanism expression that is more costly to the plant but still proportionate to potential disease cost (Walters and Heil, 2007).

In primed plants, chromatin modifications in the form of methylation and acetylation of histones take place that impact on the interaction of DNA with histones and/or open binding sites for transcriptional co-activators such as WRKY22 and WRKY29 (Eulgem, 2005; Conrath, 2011; Po-Wen et al., 2013). These chromatin modifications in primed plants have been shown to lead to increased expression of transcription factors WRKY6, WRKY29, and WRKY53 after stress exposure (Jaskiewicz et al., 2011). In Arabidopsis thaliana, mRNA and inactive MPK3 and MPK6 accumulate in cells of elicitor-treated plants. Upon exposure to Pseudomonas syringae both MAP kinases are more strongly activated in primed plants than in non-primed plants (Beckers et al., 2009).

When PTI-associated mechanisms are primed by elicitor treatments plants often accumulate ROS and produce a stronger, secondary oxidative burst following pathogen challenge, activate MPKs and stimulate SA-, JA-, and abscisic acid (ABA)-pathways (Beckers et al., 2009; Pastor et al., 2013). Callose deposition, which is potentially also linked to the ABA-pathway, can be enhanced in elicitor-treated plants (Kohler et al., 2002; Flors et al., 2005; Pastor et al., 2013) and elicitor treatment often induces expression of phenylalanine ammonia lyase (PAL) which is required for the production of SA precursors (Chen et al., 2009). In line with SA involvement, pathogenesis-related genes such as PR-1, PR-2, and PR-5 have been implicated with elicitor treatments (Kohler et al., 2002; Conrath et al., 2006). Both priming and the activation of defense mechanisms due to elicitor treatment can lead to a reduction of disease severity when subsequent pathogen attack occurs. Biologically active defense elicitors that either prime plant defenses or initiate PTI responses have been identified from diverse sources. Molecular studies have provided clues to their mechanism and to the processes that govern specificity.

A Molecular Perspective of Elicitor Activity in Plant Immunity

Several studies have shown that elicitor-treated plants show lower infection rates following inoculation with virulent pathogens but responses can vary between plant species (Table 1). In addition to the observed disease reduction, molecular studies are revealing how the elicitor compounds affect gene expression levels in plants and therefore impact on defense responses (Section Plant Genes and Pathways Involved in Elicitor Recognition). Similarly, the diverse mechanisms by which pathogen effectors suppress PTI responses are emerging but, due to the complexity of this research, only selected examples are highlighted in this review.

Plant-derived Elicitors

Plant cell walls are composed of cellulose, hemicellulose (cross-linking glycans), pectic polysaccharides, protein, lignin, and a variety of lipids (Wei et al., 2009). Bacteria and fungi can produce cellulases, xylanases, and lignin peroxidases that break down plant cell wall components and common products are β-glucans, xylose, and phenylpropanoid-containing compounds. These break-down products function as plant-derived elicitors and several examples of disease reduction due to the application of plant-derived elicitors exist (Table 1). Well studied plant-derived elicitors include oligogalacturonides (OGs), which are structural components of plant cell walls and are released upon partial degradation of homogalacturonan by microbial polygalacturonases during infection or by plant polygalacturonases induced upon wounding (Ferrari et al., 2013). Plant cell wall-derived OGs are recognized by wall-associated kinase 1 (WAK1) and subsequent signaling is JA-, SA-, and ET-independent (Brutus et al., 2010; Ferrari et al., 2013). A MAP kinase cascade is triggered upon OG perception in A. thaliana, and MPK3 and MPK6 are phosphorylated. However, the importance of these signaling events remains elusive and it has been shown, for example, that lack of MPK3 increases basal susceptibility to Botrytis cinerea but elicitor-induced resistances are not affected (Galletti et al., 2011). In contrast, MPK6 is necessary for OG-induced resistance but does not play a role in basal resistance toward B. cinerea (Galletti et al., 2011).

Bacterial-derived Elicitors

In addition to plant-derived elicitors, the application of bacterial-derived elicitors has also been shown to reduce pathogen infection in plants (Table 1). Extracellular polysaccharides (EPS) produced by the bacterial wilt causing pathogen Ralstonia solanacearum have been shown to induce defense responses in tomato (Milling et al., 2011) and lipopolysaccharides (LPS) from Gram-negative bacteria also trigger induced resistance in several other plant species (Dow et al., 2000; Gerber et al., 2004; Desaki et al., 2006; Erbs and Newman, 2012). PGPRs (plant growth-promoting rhizobacteria) can induce resistance in plants by exudating elicitors (De Vleesschauwer and Höfte, 2009 and references therein) and filtrates from cultures of bacteria such as Bacillus subtilis can also elicit crop protection effects (Schönbeck et al., 1980, 1982), though these may be a combination of direct toxicity and/or elicitor recognition events.

The molecular background to bacterial MAMPs, effectors and their plant targets has been reviewed recently (Deslandes and Rivas, 2012) and two well-studied bacterial MAMPs are flagellin and the elongation factor Tu (EF-Tu). Flagellin is recognized in a variety of plant species whereas EF-Tu, one of the most abundant proteins in bacterial cells, and bacterial cold-shock proteins seem to be specifically recognized in Brassicaceae and Solanaceae plants, respectively (Gomez-Gomez and Boller, 2002; Felix and Boller, 2003; Bittel and Robatzek, 2007; Jeworutzki et al., 2010). In both proteins, the N-terminus contains the eliciting site which, for flagellin, can often be described as a 22 amino acid long epitope (flg22), whereas that for EF-Tu is 18 amino acids (Elf18). Flagellin and EF-Tu are recognized by two distinct plant receptors (Gomez-Gomez and Boller, 2002; Kunze et al., 2004). Flagellin is recognized by FLAGELLIN-SENSING 2 (FLS2) whereas EF-Tu is recognized by EF-Tu RECEPTOR (EFR) which has only been found in Brassicaceae (Gomez-Gomez and Boller, 2002; Zipfel et al., 2006). This provides molecular insight into the specificity of elicitors and emphasizes the need to assess candidate defense eliciting compounds in a diverse range of plant species. It is interesting to note that heterologous expression of EFR in Solanaceae plants provides some resistance to bacteria that express EF-Tu (Lacombe et al., 2010) which suggests that downstream signaling cascades could be conserved for different PRRs and in different plant species. Indeed, both FLS2 and EFR are leucine rich repeat receptor like kinases (LRR-RLK) and both interact with BRI1-associated receptor kinase 1 (BAK1) triggering SA-, JA-, and ET-independent signaling (Zipfel et al., 2004, 2006; Chinchilla et al., 2007). Recognition of flg22 and Elf18 leads to an increase in cytosolic Ca2+ and it has been show that early signaling is BAK1-dependent and involves calcium associated plasma membrane anion channel opening (Jeworutzki et al., 2010). Subsequently, a MAP kinase cascade involving MPK3, MPK4, MPK6 and MPK11, and other genes such as Ca2+-dependent proteinase kinases are activated to establish PTI (Zipfel et al., 2004, 2006; Chinchilla et al., 2007; Bethke et al., 2012).

Pathogenic bacteria secrete, amongst others, type III effectors into plant cells to supress PTI and this mechanism has been well studied in the plant pathogen P. syringae (reviewed by Block and Alfano, 2011; Deslandes and Rivas, 2012). These bacterial effectors target a variety of plant genes and metabolites including plasma membrane components like RPM1-interacting protein 4 (RIN4) in A. thaliana (Day et al., 2006). Similarly, host nuclear components are, for example, perturbed by effectors such as PopP2 as well as by transcription-activator like (TAL) type III effectors from Xanthomonas that directly bind to plant DNA and thereby activate gene expression changes that promote virulence and pathogen colonization (Boch et al., 2009; Deslandes and Rivas, 2012; Coll and Valls, 2013). Other examples include the effector HopAl1 that is widely conserved in bacterial plant pathogens and interferes with the MAPK signaling genes MPK3 and MPK6 to supress PTI (Zhang et al., 2007). Furthermore, chloroplast components are also modified by bacterial effectors such as HopI1 that causes remodeling of the chloroplast thylakoid structure and interferes with SA accumulation (Jelenska et al., 2007). As mentioned above, plants have a variety of R genes, the products of which, directly or indirectly, recognize some of these bacterial effectors to elicit ETI (reviewed by Block and Alfano, 2011; Deslandes and Rivas, 2012).

Oomycete-derived Elicitors

Oomycetes are taxonomically and structurally distinct from both plants and fungi. Several oomycetes are plant pathogenic and include those from the genus Phytophthora that are responsible for substantial yield losses in crops. Oomycete cell walls consist of cellulose, glycan, and hydroxyproline-rich proteins and several oomycete elicitors have been described (Table 1). For example, necrosis and ethylene-inducing peptide 1 (Nep1)-like proteins (NLP) are recognized in dicots and it has been shown that these proteins trigger a variety of defense responses in A. thaliana (Qutob et al., 2006). Similarly, P. infestans INF1 elicitin causes an HR response in Nicotiana benthamiana (Kamoun et al., 1998) that is dependent on the receptor-like kinase SERK3/BAK1 which, as a central regulator of innate immunity in plants, is required for multiple resistance responses, including those mediated through FLS2 (Heese et al., 2007). Other PTI eliciting molecules from Phytophthora include GP42, a member of the transglutaminase family, and for which the active peptide has been described as Pep-13 (Nürnberger et al., 1994; Brunner et al., 2002), as well as the cellulose binding elicitor lectin (CBEL) that is associated with adhesion to the plant cell (Gaulin et al., 2006; reviewed in Hein et al., 2009).

To suppress PTI during infection, Phytophthora, like other plant pathogens, secretes extracellular and intracellular effectors into plants. Some extracellular effectors encode protease or glucanase inhibitors to prevent, respectively, host protease or glucanase activity in the apoplast (reviewed in Hein et al., 2009; Schornack et al., 2009). Some intracellular effectors contain the canonical RXLR motif and contain an N-terminal signal peptide and a C-terminal effector activity site (Birch et al., 2009).

The modes of action of RXLR effectors in promoting virulence are diverse. For example, it has recently been shown that the P. infestans RXLR effector PexRD2 interacts with the kinase domain of the host MAPKKKε to perturb PTI signaling pathways and to yield ETS responses (King et al., 2014). The RXLR effector PITG_03192, on the other hand, targets two membrane-associated NAC transcription factors that rapidly accumulate following PTI elicitation (McLellan et al., 2013). The effector prevents the release of these NAC transcription factors from the endoplasmic reticulum and subsequent accumulation in the plant nucleus that is typically observed as part of a PTI response. In contrast, the P. infestans RXLR effector Avrblb2 prevents secretion of an immune-associated protease (Bozkurt et al., 2011), whereas two P. sojae RXLRs have been shown to act as silencing suppressors (Qiao et al., 2013). One of the best-characterized intracellular RXLR effectors is Avr3a from P. infestans. Avr3a interacts with and stabilizes the potato E3 ubiquitin ligase CMPG1 and thus perturbs cell death responses triggered by INF1 (Bos et al., 2010) and a range of other pathogen elicitors (Gilroy et al., 2011). Avr3a exists in two forms that both suppress INF1 responses but differ in two amino acids that determine recognition by the potato R gene R3 that subsequently triggers ETI (Armstrong et al., 2005). Finally, several RXLRs from P. infestans act redundantly to suppress flg22-mediated signal transduction and early transcriptional changes (Zheng et al., 2014).

Fungal-derived Elicitors

As with plant and oomycete cell walls, break-down products from fungal cell walls, which contain chitin, mannoproteins, and β-glucans, can elicit a range of defense responses as signals of potential colonization (Table 1). Yeast extracts, for example, have widely been used to study defense responses in plants (e.g., Hahn and Albersheim, 1978; Reglinski et al., 1994b, 1995; Suzuki et al., 2005; Khokon et al., 2010). Ergosterol, a fungal cell membrane component, induces defense responses in tobacco, and Cladosporium fulvum host and non-host plant necrosis inducer 1 (CfHNNI1), which shows high homologies to genes encoding bZIP transcription factors, has been shown to induce resistance in tomato and tobacco (Takken et al., 2000; Xu et al., 2012). Similarly, a proteinaceous elicitor called SCLEROTINIA CULTURE FILTRATE ELICITOR1 (SCFE1) has recently been identified from the necrotrophic fungal pathogen Sclerotinia sclerotiorum that induces BAK1-dependent PTI responses upon recognition by the A. thaliana RECEPTOR-LIKE PROTEIN30 (RLP30) (Zhang et al., 2013).

Two of the best studied fungal-derived elicitors are chitin and chitosan, a deacetylated derivative of chitin. Both have been well described as active components that increase resistance to bacterial and fungal pathogens in several plant species including crop plants (El Ghaouth et al., 1994; Copping and Duke, 2007; Kishimoto et al., 2010; El Hadrami et al., 2012; Kombrink et al., 2011). Chitin is detected in plants by a chitin elicitor receptor kinase (CERK1) which is also known as LysMRLK1 (Wan et al., 2008; Kombrink et al., 2011). In A. thaliana, chitin-induced dimerization of AtCERK1 has shown to be necessary for activation of PTI (Liu et al., 2012). In rice, OsCERK1 forms a complex with chitin elicitor binding protein (CEBiP) upon chitin perception and both proteins are critical for chitin-induced signaling (Shimizu et al., 2010). A homolog of OsCEBiP has been identified in barley and HvCEBiP has also been shown to play a role in responses to Magnaporthe oryzae (Tanaka et al., 2010). In contrast to rice, the homolog in A. thaliana, AtCEBiP, binds chitin but does not seem to be required for chitin-induced signaling (Shinya et al., 2012). Chitin-induced PTI is JA-, SA-, and ET-independent but a RING zinc-finger like protein (ATL9) has shown to be induced upon chitin treatment (Berrocal-Lobo et al., 2010).

To suppress these responses, the fungal pathogen C. fulvum has developed two distinct effectors that suppress chitin-induced PTI leading to ETS in planta (de Jonge and Thomma, 2009; de Jonge et al., 2010; Kombrink et al., 2011). The fungal chitin-binding protein Avr4 specifically binds chitin in fungal cell walls and thereby prevents the chitin from degradation by plant chitinases (van den Burg et al., 2006; Wan et al., 2008). Furthermore, the extracellular protein 6 (Ecp6), an effector protein with 3 LysM domains, binds chitin competitively to prevent recognition of chitin by CEBiP (de Jonge and Thomma, 2009; de Jonge et al., 2010). Homologs of Avr4 have been identified in fungi belonging to the class of Dothideomycetes and Ecp6-like genes are widespread within the fungal kingdom (Kombrink et al., 2011). The plant receptor Cf4 is a receptor-like protein (RLP) without kinase activity that recognizes Avr4 (Thomas et al., 1997) and it has recently been shown that SOBIR1, a receptor-like kinase (RLK) from tomato interacts with Cf4 and might be required for Cf4-mediated resistance (Liebrand et al., 2013).

Compared with bacterial and oomycete effectors, the biological function and the targets of fungal effectors remain more elusive (Rafiqi et al., 2012; Liu et al., 2013). This has partly been attributed to the fact that fungal effectors do not seem to have canonical amino acid domains that enable a rapid candidate effector discovery (Rafiqi et al., 2012). Recently, Doehlemann and Hemetsberger (2013) reviewed the current knowledge of effectors from filamentous plant pathogens and compiled a list of known apoplastic effectors and their function. Most fungal effectors are secreted through the fungal endoplasmic reticulum (ER) secretory pathway but the way by which cytoplasmic effector proteins enter the host cells remains unknown (Rafiqi et al., 2012). In the genome of Blumeria graminis, 491 potential effector proteins have been identified but their biological function remains unknown (Pedersen et al., 2012). Similarly, in M. oryzae 15 candidate effector proteins have been identified so far (Liu et al., 2013). An effector protein from Ustilago maydis has been identified as a chorismate mutase, Cmu1, which is required for full virulence. Cmu1 functions by diverting metabolic precursors of the shikimate pathway toward production of aromatic amino acids, and away from the production of SA (Djamei and Kahmann, 2012).

Plant Genes and Pathways Involved in Elicitor Recognition

Genes Up-regulated Due to Elicitor Treatments

In the elicitor research field, the response of plant genes to elicitor treatment is of great interest and several gene expression studies have been conducted. More recently, several microarray studies have been performed in different plant species to gain greater knowledge of the diversity of genes responsive to elicitors (e.g., Medeiros et al., 2009; Kano et al., 2011; Povero et al., 2011; Amelot et al., 2012), albeit knowledge on plant gene expression in response to elicitors has mainly been focused on A. thaliana. As mentioned previously, the presence of the cognate receptors can determine responsiveness to elicitors (Lacombe et al., 2010) and it is thus essential to investigate elicitor effects in diverse crop plants (Nguyen et al., 2010).

As part of this review, we aim to provide an overview of the current knowledge of differentially expressed plant genes following elicitor treatments and identify typically affected plant processes. This will facilitate identification of responses to elicitor application such as plant growth or nutrient metabolisms that are not directly linked to defense but impact on agriculture. For this we have combined over 50 publications to create a list of plant genes that are differentially expressed following the recognition of elicitors (Table S1). Reciprocal BLAST (Basic Local Alignment Search Tool; Altschul et al., 1990) has been used to identify the A. thaliana homologs when the original experiment was performed in a different plant species (>70% identity of nucleotide sequences, E-value < 0.0001). In addition to the publications, PathoPlant®, a database featuring compiled expression data and components of signal transduction pathways related to plant pathogenesis, has been used (Bülow et al., 2004, 2007). This database enables querying differential plant gene expression following diverse pathogen stimuli which, for this study, include Botrytis cinerea, chitin, Erysiphe orontii, Phytophthora infestans, Pseudomonas syringae pv. Maculicola, and Pseudomonas syringae pv. Phaseolicola.

A total of 1592 plant genes that were activated by the recognition of elicitors have been identified (Table S1). Ontological analysis was performed using agriGo (Du et al., 2010). In this analysis, genes of interest are grouped by gene ontology (GO) terms describing biological processes, molecular functions and cellular components (Ashburner et al., 2000). The list of genes of interest is compared to a defined background gene list which, in this study, included the whole genome of A. thaliana as provided by The Arabidopsis Information Resource (TAIR) (Lamesch et al., 2011) to identify GO terms that are significantly over-represented. A total of 762 shared GO terms were identified, comprising 474 biological processes, 206 molecular functions and 82 cellular components (Table S2).

The three most over-represented biological processes were “response to stimulus” (GO:0050896), “multi-organism process” (GO:0051704), and “immune system process” (GO:0002376). The GO term “response to stimulus” contained 36.5% of the elicitor responsive genes in comparison to 10.7% representation in the whole A. thaliana genome. The GO term “multi-organism process” contained 11.1% of the genes in the target gene list, compared to 2.1% of the whole genome, and 6.6% instead of 1% were classed in the GO term “immune system process” (Figure 2).

FIGURE 2
www.frontiersin.org

Figure 2. Highly significant shared biological processes within Arabidopsis thaliana genes that are induced and overrepresented following the recognition of elicitor compounds (black) in comparison to the whole genome of A. thaliana (gray).

Three of the over-represented molecular functions were “catalytic activity” (GO:0003824), “binding” (GO:0005488), and “molecular transducer activity” (GO:0060089). The GO term “catalytic activity” featured in 48.5% of the elicitor responsive genes in comparison to 25.5% of the whole A. thaliana genome. The GO term “binding” contained 37.8% of the genes in the target gene list in comparison to 29.8% of the whole genome and 3.1% instead of 1.1% were classed in the GO term “molecular transducer activity” (Figure 3).

FIGURE 3
www.frontiersin.org

Figure 3. Highly significant shared molecular functions within Arabidopsis thaliana genes that are induced and overrepresented following the recognition of elicitor compounds (black) in comparison to the whole genome of A. thaliana (gray).

The relationships of all over-represented genes in the classification “biological processes” are shown in Figure S1. These include metabolic processes such as amine-, phosphate-, and phytoalexin metabolism; immune system processes and cell death, including regulation of defense response; plant-type hypersensitive response and apoptosis; response to stimuli including JA and SA; systemic acquired resistance and defense responses to fungi and bacteria (Figure S1).

The relationship of all genes over-represented in the GO term “molecular functions” are shown in Figure S2. These functions contain catalytic activity including oxidoreductase, lyase, and kinase activities; and binding activities including ATP and sugar binding (Figure S2). The relationships of all over-represented genes in the classification “cellular components” are shown in Figure S3. All cell parts are involved but the involvements of cell wall and plasma membranes are highly significant (Figure S3).

Targets of Pathogen Effectors

As noted above, pathogens produce effector molecules to interfere with plant defense responses. An analysis of plant-pathogen protein-protein interactions using A. thaliana and two pathogens, P. syringae and the obligate biotrophic oomycete Hyaloperonospora arabidopsidis revealed 137 A. thaliana proteins that were potentially targeted by pathogen effectors (Mukhtar et al., 2011). A recent review on bacterial effectors listed an additional 22 plant proteins targeted by several bacterial effectors (Deslandes and Rivas, 2012). In the analysis here, genes encoding these 159 proteins were used to search for overlap with the plant genes differentially induced upon elicitor recognition. A total of 23 genes were identified that are both induced by elicitors and targeted by pathogen effectors (Table S3). These comprise receptors such as FLS2 and EFR, genes involved in MAPK cascades like RIPK, MPK3, MPK4, and MPK6, R protein-guarded host proteins such as RIN4 and genes involved in L-phenylalanine biosynthetic process like ADT4 and ADT5 (Table S3). These overlapping genes are grouped into several biological processes, molecular functions and cell parts and their involvements are highlighted with stars in Figures S1–S3. This analysis highlights the complexity of priming and plant immune responses, and the sophisticated interactions with pathogen effectors. It shows that the plant response to elicitor compounds does not only involve genes that are annotated as defense-related but that other metabolic pathways are also involved. We know that elicitor treatments result in positive and negative trade-offs (Walters and Heil, 2007) and therefore expression profiling of some of these genes should result in a better understanding of these responses and how they might be exploited.

“Non-defense” Effects of Elicitors

As mentioned above, for successful use of elicitors in agriculture it is important to understand their effects not only on plant defense but also on other aspects of plant development and environmental responses. The activation of defense pathways as part of PTI can be very costly to plants but should be less than the potential loss caused by disease if no defense was mounted. However, in the context of crop protection, such costs are unlikely to be acceptable in the absence of known pathogen challenges of a high order. Crop protectants are preferred that enhance the efficacy of PTI assisting a quicker and more effective response when an actual pathogen challenge occurs and therefore is more efficient in its use of resources. This can be achieved through priming if priming is either not costly to the plant or its costs are mitigated by other beneficial means.

Some of the known priming genes are generally regulatory but not necessarily restricted to defense pathways. They regulate signal transduction events, particularly those identified in stress responses or in the GO terms “response to stimulus,” “multi-organism processes,” and “immune system processes,” i.e., the genes disproportionately up-regulated by elicitors highlighted above (see Figures S1, S2). Thus, many non-defense mechanism processes will be affected in their expression by elicitors. These might result in additional costs above those incurred by defense gene expression, but they may also have benefits. An example of a non-defense effect of an elicitor is reduced water use of pepper plants upon treatment with chitosan (Bittelli et al., 2001). Chitosan was also found to affect the net photosynthetic rate of soybean and maize after application (Khan et al., 2002). More general effects on yield, not directly attributable to disease control, were also found from applications of B. subtilis culture filtrates (Dehne et al., 1984; Steiner et al., 1988). Similar effects were recorded for some treatments of yeast cell wall-derived extracts (Reglinski et al., 1994a).

Indeed, on a molecular level, there is evidence of cross talk between the MAPKs involved in PTI and abiotic stress responses. For example, the transcription of MEKK1 is induced by diverse stresses including cold, salt, drought and wounding (Mizoguchi et al., 1998). Conversely, the activation of EDS1/PAD4-dependent signaling during ETI responses can rapidly antagonize ABA signal transduction at the level of Ca2+ signaling (Kim et al., 2011). The overexpression of the gene ACTIVATED DISEASE RESISTANCE1 (ADS1) in A. thaliana, a member of the nucleotide-binding (NB) and leucine-rich repeat (LRR) containing NB-LRR genes, confers both disease resistance (Grant et al., 2003) and drought tolerance, requiring SA, EDS1 and ABA-INSENSITIVE1 (ABI1) (Chini et al., 2004).

Much depends on the basis of determination of costs as we tend to calculate these from an end-user yield perspective. We should also recognize that each of these pathways, whether defense-related or not, is in a complex expression and metabolic network of cross-talk and feedback mechanisms and thus affected by many environmental factors. Those that can be manipulated beneficially and perhaps synergistically fall in the category of nutrition (Walters and Bingham, 2007). Primed plants showed considerably higher fitness than non-primed plants when they were challenged by pathogens without major trade-off effects on growth and seed set (Conrath et al., 2006; van Hulten et al., 2006). Correlation of priming benefits with gene expression profiles may lead to very practical means for developing elicitor-based crop protectants that either off-set any direct costs, increase some aspect of resource use efficiency or specifically enhance other processes beneficial to yield or quality.

Conflict of Interest Statement

The authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest.

Acknowledgments

The authors are grateful for financial support for this work in part from the Rural & Environment Science & Analytical Services Division of the Scottish Government. Lea Wiesel is supported by the Technology Strategy Board and its Knowledge Transfer Partnership grant KTP008814 with Omex Agriculture Limited.

Supplementary Material

The Supplementary Material for this article can be found online at: http://www.frontiersin.org/journal/10.3389/fpls.2014.00655/abstract

References

Altschul, S. F., Gish, W., Miller, W., Myers, E. W., and Lipman, D. J. (1990). Basic local alignment search tool. J. Mol. Biol. 215, 403–410. doi: 10.1016/S0022-2836(05)80360-2

Pubmed Abstract | Pubmed Full Text | CrossRef Full Text | Google Scholar

Amelot, N., de Borne, F. D., Clemente, H. S., Mazars, C., Grima-Pettenati, J., and Briere, C. (2012). Transcriptome analysis of tobacco BY-2 cells elicited by cryptogein reveals new potential actors of calcium-dependent and calcium-independent plant defense pathways. Cell Calcium 51, 117–130. doi: 10.1016/j.ceca.2011.11.010

Pubmed Abstract | Pubmed Full Text | CrossRef Full Text | Google Scholar

Armstrong, M. R., Whisson, S. C., Pritchard, L., Bos, J. I., Venter, E., Avrova, A. O., et al. (2005). An ancestral oomycete locus contains late blight avirulence gene Avr3a, encoding a protein that is recognized in the host cytoplasm. Proc. Natl. Acad. Sci. U.S.A. 102, 7766–7771. doi: 10.1073/pnas.0500113102

Pubmed Abstract | Pubmed Full Text | CrossRef Full Text | Google Scholar

Ashburner, M., Ball, C. A., Blake, J. A., Botstein, D., Butler, H., Cherry, J. M., et al. (2000). Gene Ontology: tool for the unification of biology. Nat. Genet. 25, 25–29. doi: 10.1038/75556

Pubmed Abstract | Pubmed Full Text | CrossRef Full Text | Google Scholar

Aziz, A., Gauthier, A., Bézier, A., Poinssot, B., Joubert, J. M., Pugin, A., et al. (2007). Elicitor and resistance-inducing activities of β-1,4 cellodextrins in grapevine, comparison with β-1,3 glucans and α-1,4 oligogalacturonides. J. Exp. Bot. 58, 1463–1472. doi: 10.1093/jxb/erm008

Pubmed Abstract | Pubmed Full Text | CrossRef Full Text | Google Scholar

Beckers, G. J., Jaskiewicz, M., Liu, Y., Underwood, W. R., He, S. Y., Zhang, S., et al. (2009). Mitogen-activated protein kinases 3 and 6 are required for full priming of stress responses in Arabidopsis thaliana. Plant Cell 21, 944–953. doi: 10.1105/tpc.108.062158

Pubmed Abstract | Pubmed Full Text | CrossRef Full Text | Google Scholar

Berrocal-Lobo, M., Stone, S., Yang, X., Antico, J., Callis, J., Ramonell, K. M., et al. (2010). ATL9, a RING zinc finger protein with E3 ubiquitin ligase activity implicated in chitin- and NADPH oxidase-mediated defense responses. PLoS ONE 5:e14426. doi: 10.1371/journal.pone.0014426

Pubmed Abstract | Pubmed Full Text | CrossRef Full Text | Google Scholar

Bethke, G., Pecher, P., Eschen-Lippold, L., Tsuda, K., Katagiri, F., Glazebrook, J., et al. (2012). Activation of the Arabidopsis thaliana mitogen-activated protein kinase MPK11 by the flagellin-derived elicitor peptide, flg22. Mol. Plant Microbe Interact. 25, 471–480. doi: 10.1094/MPMI-11-11-0281

Pubmed Abstract | Pubmed Full Text | CrossRef Full Text | Google Scholar

Birch, P. R., Armstrong, M., Bos, J., Boevink, P., Gilroy, E. M., Taylor, R. M., et al. (2009). Towards understanding the virulence functions of RXLR effectors of the oomycete plant pathogen Phytophthora infestans. J. Exp. Bot. 60, 1133–1140. doi: 10.1093/jxb/ern353

Pubmed Abstract | Pubmed Full Text | CrossRef Full Text | Google Scholar

Bishop, G. J., and Koncz, C. (2002). Brassinosteroids and plant steroid hormone signaling. Plant Cell 14, S97–S110. doi: 10.1105/tpc.001461

Pubmed Abstract | Pubmed Full Text | CrossRef Full Text | Google Scholar

Bittel, P., and Robatzek, S. (2007). Microbe-associated molecular patterns (MAMPs) probe plant immunity. Curr. Opin. Plant Biol. 10, 335–341. doi: 10.1016/j.pbi.2007.04.021

Pubmed Abstract | Pubmed Full Text | CrossRef Full Text | Google Scholar

Bittelli, M., Flury, M., Campbell, G. S., and Nichols, E. J. (2001). Reduction of transpiration through foliar application of chitosan. Agr. Forest Meteorol. 107, 167–175. doi: 10.1016/S0168-1923(00)00242-2

CrossRef Full Text | Google Scholar

Block, A., and Alfano, J. R. (2011). Plant targets for Pseudomonas syringae type III effectors: virulence targets or guarded decoys? Curr. Opin. Plant Biol. 14, 39–46. doi: 10.1016/j.mib.2010.12.011

Pubmed Abstract | Pubmed Full Text | CrossRef Full Text | Google Scholar

Boch, J., Scholze, H., Schornack, S., Landgraf, A., Hahn, S., Kay, S., et al. (2009). Breaking the code of DNA binding specificity of TAL-type III effectors. Science 326, 1509–1512. doi: 10.1126/science.1178811

Pubmed Abstract | Pubmed Full Text | CrossRef Full Text | Google Scholar

Bonnet, P., Bourdon, E., Ponchet, M., Blein, J. P., and Ricci, P. (1996). Acquired resistance triggered by elicitins in tobacco and other plants. Eur. J. Plant Pathol. 102, 181–192. doi: 10.1007/BF01877105

CrossRef Full Text | Google Scholar

Bos, J. I. B., Armstrong, M. R., Gilroy, E. M., Boevink, P. C., Hein, I., Taylor, R. M., et al. (2010). Phytophthora infestans effector AVR3a is essential for virulence and manipulates plant immunity by stabilizing host E3 ligase CMPG1. Proc. Natl. Acad. Sci. U.S.A. 107, 9909–9914. doi: 10.1073/pnas.0914408107

Pubmed Abstract | Pubmed Full Text | CrossRef Full Text | Google Scholar

Bourque, S., Dutartre, A., Hammoudi, V., Blanc, S., Dahan, J., Jeandroz, S., et al. (2011). Type-2 histone deacetylases as new regulators of elicitor-induced cell death in plants. New Phytol. 192, 127–139. doi: 10.1111/j.1469-8137.2011.03788.x

Pubmed Abstract | Pubmed Full Text | CrossRef Full Text | Google Scholar

Bozkurt, T. O., Schornack, S., Win, J., Shindo, T., Ilyas, M., Oliva, R., et al. (2011). Phytophthora infestans effector Avrblb2 prevents secretion of a plant immune protease at the haustorial interface. Proc. Natl. Acad. Sci. U.S.A. 108, 20832–20837. doi: 10.1073/pnas.1112708109

Pubmed Abstract | Pubmed Full Text | CrossRef Full Text | Google Scholar

Brunner, F., Rosahl, S., Lee, J., Rudd, J. J., Geiler, C., Kauppinen, S., et al. (2002). Pep-13, a plant defense-inducing pathogen-associated pattern from Phytophthora transglutaminases. EMBO J. 21, 6681–6688. doi: 10.1093/emboj/cdf667

Pubmed Abstract | Pubmed Full Text | CrossRef Full Text | Google Scholar

Brutus, A., Sicilia, F., Macone, A., Cervone, F., and De Lorenzo, G. (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. U.S.A. 107, 9452–9457. doi: 10.1073/pnas.1000675107

Pubmed Abstract | Pubmed Full Text | CrossRef Full Text | Google Scholar

Bülow, L., Schindler, M., Choi, C., and Hehl, R. (2004). PathoPlant®: a database on plant-pathogen interactions. In Silico Biol. 4, 529–536.

Pubmed Abstract | Pubmed Full Text | Google Scholar

Bülow, L., Schindler, M., and Hehl, R. (2007). PathoPlant®: a platform for microarray expression data to analyze co-regulated genes involved in plant defense responses. Nucleic Acids Res. 35, D841–D845. doi: 10.1093/nar/gkl835

Pubmed Abstract | Pubmed Full Text | CrossRef Full Text | Google Scholar

Chen, M., Zeng, H., Qiu, D., Guo, L., Yang, X., Shi, H., et al. (2012). Purification and characterization of a novel hypersensitive response-inducing elicitor from Magnaporthe oryzae that triggers defense response in rice. PLoS ONE 7:e37654. doi: 10.1371/journal.pone.0037654

Pubmed Abstract | Pubmed Full Text | CrossRef Full Text | Google Scholar

Chen, Z., Zheng, Z., Huang, J., Lai, Z., and Fan, B. (2009). Biosynthesis of salicylic acid in plants. Plant Signal. Behav. 4, 493–496. doi: 10.4161/psb.4.6.8392

Pubmed Abstract | Pubmed Full Text | CrossRef Full Text | Google Scholar

Chinchilla, D., Zipfel, C., Robatzek, S., Kemmerling, B., Nürnberger, T., Jones, J. D. G., et al. (2007). A flagellin-induced complex of the receptor FLS2 and BAK1 initiates plant defence. Nature 448, 497–500. doi: 10.1038/nature05999

Pubmed Abstract | Pubmed Full Text | CrossRef Full Text | Google Scholar

Chini, A., Grant, J. J., Seki, M., Shinozaki, K., and Loake, G. J. (2004). Drought tolerance established by enhanced expression of the CC-NBS-LRR gene, ADR1, requires salicylic acid, EDS1 and ABI1. Plant J. 385, 810–822. doi: 10.1111/j.1365-313X.2004.02086.x

Pubmed Abstract | Pubmed Full Text | CrossRef Full Text | Google Scholar

Cluzet, S., Torregrosa, C., Jacquet, C., Lafitte, C., Fournier, J., Mercier, L., et al. (2004). Gene expression profiling and protection of Medicago truncatula against a fungal infection in response to an elicitor from green algae Ulva spp. Plant Cell Environ. 27, 917–928. doi: 10.1111/j.1365-3040.2004.01197.x

CrossRef Full Text | Google Scholar

Coll, N. S., and Valls, M. (2013). Current knowledge on the Ralstonia solanacearum type III secretion system. Microb. Biotechnol. 6, 614–620. doi: 10.1111/1751-7915.12056

Pubmed Abstract | Pubmed Full Text | CrossRef Full Text | Google Scholar

Conrath, U. (2011). Molecular aspects of defence priming. Trends Plant Sci. 16, 524–531. doi: 10.1016/j.tplants.2011.06.004

Pubmed Abstract | Pubmed Full Text | CrossRef Full Text | Google Scholar

Conrath, U., Beckers, G. J., Flors, V., Garcia-Agustin, P., Jakab, G., Mauch, F., et al. (2006). Priming: getting ready for battle. Mol. Plant Microbe Interact. 19, 1062–1071. doi: 10.1094/MPMI-19-1062

Pubmed Abstract | Pubmed Full Text | CrossRef Full Text | Google Scholar

Copping, L. G., and Duke, S. O. (2007). Natural products that have been used commercially as crop protection agents. Pest Manag. Sci. 63, 524–554. doi: 10.1002/ps.1378

Pubmed Abstract | Pubmed Full Text | CrossRef Full Text | Google Scholar

Craigie, J. S. (2011). Seaweed extract stimuli in plant science and agriculture. J. Appl. Phycol. 23, 371–393. doi: 10.1007/s10811-010-9560-4

CrossRef Full Text | Google Scholar

Daayf, F., Ongena, M., Boulanger, R., El Hadrami, I., and Bélanger, R. R. (2000). Induction of phenolic compounds in two cultivars of cucumber by treatment of healthy and powdery mildew-infected plants with extracts of Reynoutria sachalinensis. J. Chem. Ecol. 26, 1579–1593. doi: 10.1023/A:1005578510954

CrossRef Full Text | Google Scholar

Daayf, F., Schmitt, A., and Belanger, R. R. (1997). Evidence of phytoalexins in cucumber leaves infected with powdery mildew following treatment with leaf extracts of Reynoutria sachalinensis. Plant Physiol. 113, 719–727.

Pubmed Abstract | Pubmed Full Text | Google Scholar

Danna, C. H., Millet, Y. A., Koller, T., Han, S. W., Bent, A. F., Ronald, P. C., et al. (2011). The Arabidopsis flagellin receptor FLS2 mediates the perception of Xanthomonas Ax21 secreted peptides. Proc. Natl. Acad. Sci. U.S.A. 108, 9286–9291. doi: 10.1073/pnas.1106366108

Pubmed Abstract | Pubmed Full Text | CrossRef Full Text | Google Scholar

Day, B., Dahlbeck, D., and Staskawicz, B. J. (2006). NDR1 interaction with RIN4 mediates the differential activation of multiple disease resistance pathways in Arabidopsis. Plant Cell 18, 2782–2791. doi: 10.1105/tpc.106.044693

Pubmed Abstract | Pubmed Full Text | CrossRef Full Text | Google Scholar

Dehne, H.-W., Stenzel, K., and Schönbeck, F. (1984). Zur Wirksamkeit induzierter Resistenz unter praktischen Anbaubedingungen III. Reproduktion echter Mehltaupilze auf induziert resistenten Pflanzen. Z. Pflanzenk. Pflanzen. 91, 258–265.

de Jonge, R., Peter van Esse, H., Kombrink, A., Shinya, T., Desaki, Y., Bours, R., et al. (2010). Conserved fungal LysM effector Ecp6 prevents chitin-triggered immunity in plants. Science 329, 953–955. doi: 10.1126/science.1190859

Pubmed Abstract | Pubmed Full Text | CrossRef Full Text | Google Scholar

de Jonge, R., and Thomma, B. P. (2009). Fungal LysM effectors: extinguishers of host immunity? Trends Microbiol. 17, 151–157. doi: 10.1016/j.tim.2009.01.002

Pubmed Abstract | Pubmed Full Text | CrossRef Full Text | Google Scholar

de Oliveira, A. L., Gallo, M., Pazzagli, L., Benedetti, C. E., Cappugi, G., Scala, A., 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. 286, 17560–17568. doi: 10.1074/jbc.M111.223644

Pubmed Abstract | Pubmed Full Text | CrossRef Full Text | Google Scholar

Desaki, Y., Miya, A., Venkatesh, B., Tsuyumu, S., Yamane, H., Kaku, H., et al. (2006). Bacterial lipopolysaccharides induce defense responses associated with programmed cell death in rice cells. Plant Cell Physiol. 47, 1530–1540. doi: 10.1093/pcp/pcl019

Pubmed Abstract | Pubmed Full Text | CrossRef Full Text | Google Scholar

Deslandes, L., and Rivas, S. (2012). Catch me if you can: bacterial effectors and plant targets. Trends Plant Sci. 17, 644–655. doi: 10.1016/j.tplants.2012.06.011

Pubmed Abstract | Pubmed Full Text | CrossRef Full Text | Google Scholar

De Vleesschauwer, D., and Höfte, M. (2009). Rhizobacteria-induced systemic resistance. Adv. Bot. Res. 51, 223–281. doi: 10.1016/S0065-2296(09)51006-3

CrossRef Full Text | Google Scholar

Djamei, A., and Kahmann, R. (2012). Ustilago maydis: dissecting the molecular interface between pathogen and plant. PLoS Pathog. 8:e1002955. doi: 10.1371/journal.ppat.1002955

Pubmed Abstract | Pubmed Full Text | CrossRef Full Text | Google Scholar

Djonoviç, S., Vargas, W. A., Kolomiets, M. V., Horndeski, M., Wiest, A., and Kenerley, C. M. (2007). A proteinaceous elicitor Sm1 from the beneficial fungus Trichoderma virens is required for induced systemic resistance in maize. Plant Physiol. 145, 875–889. doi: 10.1104/pp.107.103689

Pubmed Abstract | Pubmed Full Text | CrossRef Full Text | Google Scholar

Doehlemann, G., and Hemetsberger, C. (2013). Apoplastic immunity and its suppression by filamentous plant pathogens. New Phytol. 198, 1001–1016. doi: 10.1111/nph.12277

Pubmed Abstract | Pubmed Full Text | CrossRef Full Text | Google Scholar

Dow, M., Newman, M. A., and von Roepenack, E. (2000). The induction and modulation of plant defense responses by bacterial lipopolysaccharides. Annu. Rev. Phytopathol. 38, 241–261. doi: 10.1146/annurev.phyto.38.1.241

Pubmed Abstract | Pubmed Full Text | CrossRef Full Text | Google Scholar

Du, Z., Zhou, X., Ling, Y., Zhang, Z., and Su, Z. (2010). agriGO: a GO analysis toolkit for the agricultural community. Nucleic Acids Res. 38, W64–W70. doi: 10.1093/nar/gkq310

Pubmed Abstract | Pubmed Full Text | CrossRef Full Text | Google Scholar

El Ghaouth, A., Arul, J., Grenier, J., Benhamou, N., Asselin, A., and Bélanger, R. (1994). Effect of chitosan on cucumber plants: suppression of Pythium aphanidermatum and induction of defense reactions. Phytopathology 84, 313–320. doi: 10.1094/Phyto-84-313

CrossRef Full Text | Google Scholar

El Hadrami, A., Adam, L. R., El Hadrami, I., and Daayf, F. (2012). Chitosan in plant protection. Mar. Drugs 8, 968–987. doi: 10.3390/md8040968

Pubmed Abstract | Pubmed Full Text | CrossRef Full Text | Google Scholar

Erbs, G., and Newman, M. A. (2012). The role of lipopolysaccharide and peptidoglycan, two glycosylated bacterial microbe-associated molecular patterns (MAMPs), in plant innate immunity. Mol. Plant Pathol. 13, 95–104. doi: 10.1111/j.1364-3703.2011.00730.x

Pubmed Abstract | Pubmed Full Text | CrossRef Full Text | Google Scholar

Eshraghi, L., Anderson, J., Aryamanesh, N., Shearer, B., McComb, J., Hardy, G. E. S., et al. (2011). Phosphite primed defence responses and enhanced expression of defence genes in Arabidopsis thaliana infected with Phytophthora cinnamomi. Plant Pathol. 60, 1086–1095. doi: 10.1111/j.1365-3059.2011.02471.x

CrossRef Full Text | Google Scholar

Eulgem, T. (2005). Regulation of the Arabidopsis defense transcriptome. Trends Plant Sci. 10, 71–78. doi: 10.1016/j.tplants.2004.12.006

Pubmed Abstract | Pubmed Full Text | CrossRef Full Text | Google Scholar

Falcón-Rodríguez, A. B., Wegria, G., and Cabrera, J.-C. (2012). “Exploiting plant innate immunity to protect crops against biotic stress: chitosaccharides as natural and suitable candidates for this purpose,” in New Perspectives in Plant Protection, ed A. R. Bandani (Rijeka: In Tech Croatia), 139–166.

Google Scholar

Felix, G., and Boller, T. (2003). Molecular sensing of bacteria in plants. The highly conserved RNA-binding motif RNP-1 of bacterial cold shock proteins is recognized as an elicitor signal in tobacco. J. Biol. Chem. 278, 6201–6208. doi: 10.1074/jbc.M209880200

Pubmed Abstract | Pubmed Full Text | CrossRef Full Text | Google Scholar

Ferrari, S., Savatin, D. V., Sicilia, F., Gramegna, G., Cervone, F., and De Lorenzo, G. (2013). Oligogalacturonides: plant damage-associated molecular patterns and regulators of growth and development. Front. Plant Sci. 4:49. doi: 10.3389/fpls.2013.00049

Pubmed Abstract | Pubmed Full Text | CrossRef Full Text | Google Scholar

Flors, V., Ton, J., Jakab, G., and Mauch-Mani, B. (2005). Abscisic acid and callose: team players in defence against pathogens? J. Phytopathol. 153, 377–383. doi: 10.1111/j.1439-0434.2005.00987.x

CrossRef Full Text | Google Scholar

Fu, Y., Yin, H., Wang, W., Wang, M., Zhang, H., Zhao, X., et al. (2011). β-1,3-glucan with different degree of polymerization induced different defense responses in tobacco. Carbohyd. Polym. 86, 774–782. doi: 10.1016/j.carbpol.2011.05.022

CrossRef Full Text | Google Scholar

Galletti, R., Ferrari, S., and De Lorenzo, G. (2011). Arabidopsis MPK3 and MPK6 play different roles in basal and oligogalacturonide- or flagellin-induced resistance against Botrytis cinerea. Plant Physiol. 157, 804–814. doi: 10.1104/pp.111.174003

Pubmed Abstract | Pubmed Full Text | CrossRef Full Text | Google Scholar

Garcion, C., Lamotte, O., and Métraux, J.-P. (2007). “Mechanisms of defense to pathogens: biochemistry and physiology,” in Induced Resistance for Plant Defence, eds D. R. Walters, A.C. Newton, and G. D. Lyon (Oxford: Blackwell Publishing), 109–132. doi: 10.1002/9780470995983.ch6

CrossRef Full Text

Gaulin, E., Dramé, N., Lafitte, C., Torto-Alalibo, T., Martinez, Y., Ameline-Torregrosa, C., et al. (2006). Cellulose binding domains of a Phytophthora cell wall protein are novel pathogen-associated molecular patterns. Plant Cell 18, 1766–1777. doi: 10.1105/tpc.105.038687

Pubmed Abstract | Pubmed Full Text | CrossRef Full Text | Google Scholar

Gerber, I., Zeidler, D., Durner, J., and Dubery, I. (2004). Early perception responses of Nicotiana tabacum cells in response to lipopolysaccharides from Burkholderia cepacia. Planta 218, 647–657. doi: 10.1007/s00425-003-1142-0

Pubmed Abstract | Pubmed Full Text | CrossRef Full Text | Google Scholar

Gilroy, E. M., Taylor, R. M., Hein, I., Boevink, P., Sadanandom, A., and Birch, P. R. J. (2011). CMPG1-dependent cell death follows perception of diverse pathogen elicitors at the host plasma membrane and is suppressed by Phytophthora infestans RXLR effector AVR3a. New Phytol. 190, 653–666. doi: 10.1111/j.1469-8137.2011.03643.x

Pubmed Abstract | Pubmed Full Text | CrossRef Full Text | Google Scholar

Gomez-Gomez, L., and Boller, T. (2002). Flagellin perception: a paradigm for innate immunity. Trends Plant Sci. 7, 251–256. doi: 10.1016/S1360-1385(02)02261-6

Pubmed Abstract | Pubmed Full Text | CrossRef Full Text | Google Scholar

Goupil, P., Benouaret, R., Charrier, O., Ter Halle, A., Richard, C., Eyheraguibel, B., et al. (2012). Grape marc extract acts as elicitor of plant defence responses. Ecotoxicology 21, 1541–1549. doi: 10.1007/s10646-012-0908-1

Pubmed Abstract | Pubmed Full Text | CrossRef Full Text | Google Scholar

Grant, J. J., Chini, A., Basu, D., and Loake, G. J. (2003). Targeted activation tagging of the Arabidopsis NBS-LRR gene, ADR1, conveys resistance to virulent pathogens. Mol. Plant Microbe Interact. 16, 669–680. doi: 10.1094/MPMI.2003.16.8.669

Pubmed Abstract | Pubmed Full Text | CrossRef Full Text | Google Scholar

Guo, M., Chen, K., and Zhang, P. (2012). Transcriptome profile analysis of resistance induced by burdock fructooligosaccharide in tobacco. J. Plant Physiol. 169, 1511–1519. doi: 10.1016/j.jplph.2012.06.019

Pubmed Abstract | Pubmed Full Text | CrossRef Full Text | Google Scholar

Hahn, M. G., and Albersheim, P. (1978). Host-pathogen interactions: XIV. isolation and partial characterization of an elicitor from yeast extract. Plant Physiol. 62, 107–111. doi: 10.1104/pp.62.1.107

Pubmed Abstract | Pubmed Full Text | CrossRef Full Text | Google Scholar

Heese, A., Hann, D. R., Gimenez-Ibanez, S., Jones, A. M., He, K., Li, J., et al. (2007). The receptor-like kinase SERK3/BAK1 is a central regulator of innate immunity in plants. Proc. Natl. Acad. Sci. U.S.A. 104, 12217–12222. doi: 10.1073/pnas.0705306104

Pubmed Abstract | Pubmed Full Text | CrossRef Full Text | Google Scholar

Hein, I., Gilroy, E. M., Armstrong, M. R., and Birch, P. R. J. (2009). The zig-zag-zig in oomycete?plant interactions. Mol. Plant Pathol. 10, 547–562. doi: 10.1111/j.1364-3703.2009.00547.x

Pubmed Abstract | Pubmed Full Text | CrossRef Full Text | Google Scholar

Henriquez, M. A., Wolski, E. A., Molina, O. I., Adam, L. R., Andreu, A. B., and Daayf, F. (2012). Effects of glucans and eicosapentaenoic acid on differential regulation of phenylpropanoid and mevalonic pathways during potato response to Phytophthora infestans. Plant Physiol. Biochem. 60, 119–128. doi: 10.1016/j.plaphy.2012.07.027

Pubmed Abstract | Pubmed Full Text | CrossRef Full Text | Google Scholar

Henry, G., Thonart, P., and Ongena, M. (2012). PAMPs, MAMPs, DAMPs and others: an update on the diversity of plant immunity elicitors. Biotechnol. Agron. Soc. Environ. 16, 257–268.

Google Scholar

Huang, C.-J., Tsay, J.-F., Chang, S.-Y., Yang, H.-P., Wu, W.-S., and Chen, C.-Y. (2012). Dimethyl disulfide is an induced systemic resistance elicitor produced by Bacillus cereus C1L. Pest Manag. Sci. 68, 1306–1310. doi: 10.1002/ps.3301

Pubmed Abstract | Pubmed Full Text | CrossRef Full Text | Google Scholar

Huffaker, A., Dafoe, N. J., and Schmelz, E. A. (2011). ZmPep1, an ortholog of Arabidopsis elicitor peptide 1, regulates maize innate immunity and enhances disease resistance. Plant Physiol. 155, 1325–1338. doi: 10.1104/pp.110.166710

Pubmed Abstract | Pubmed Full Text | CrossRef Full Text | Google Scholar

Igarashi, D., Takeda, T., Narusaka, Y., and Totsuka, K. (2010). Glutamate fermentation by-product activates plant defence responses and confers resistance against pathogen infection. J. Phytopathol. 158, 668–675. doi: 10.1111/j.1439-0434.2010.01678.x

CrossRef Full Text | Google Scholar

Jaskiewicz, M., Conrath, U., and Peterhaensel, C. (2011). Chromatin modification acts as a memory for systemic acquired resistance in the plant stress response. EMBO Rep. 12, 50–55. doi: 10.1038/embor.2010.186

Pubmed Abstract | Pubmed Full Text | CrossRef Full Text | Google Scholar

Jaulneau, V., Lafitte, C., Corio-Costet, M. F., Stadnik, M. J., Salamagne, S., Briand, X., et al. (2011). An Ulva armoricana extract protects plants against three powdery mildew pathogens. Eur. J. Plant Pathol. 131, 393–401. doi: 10.1007/s10658-011-9816-0

CrossRef Full Text | Google Scholar

Jelenska, J., Yao, N., Vinatzer, B. A., Wright, C. M., Brodsky, J. L., and Greenberg, J. T. (2007). A J domain virulence effector of Pseudomonas syringae remodels host chloroplasts and suppresses defenses. Curr. Biol. 17, 499–508. doi: 10.1016/j.cub.2007.02.028

Pubmed Abstract | Pubmed Full Text | CrossRef Full Text | Google Scholar

Jeworutzki, E., Roelfsema, M., Anschütz, U., Krol, E., Elzenga, J., Felix, G., et al. (2010). Early signaling through the Arabidopsis pattern recognition receptors FLS2 and EFR involves Ca2+-associated opening of plasma membrane anion channels. Plant J. 62, 367–378. doi: 10.1111/j.1365-313X.2010.04155.x

Pubmed Abstract | Pubmed Full Text | CrossRef Full Text | Google Scholar

Jin, W., Wu, F., Xiao, L., Liang, G., Zhen, Y., Guo, Z., et al. (2012). Microarray-based analysis of tomato miRNA regulated by Botrytis cinerea. J. Plant Growth Regul. 31, 38–46. doi: 10.1007/s00344-011-9217-9

CrossRef Full Text | Google Scholar

Jones, J. D., and Dangl, J. L. (2006). The plant immune system. Nature 444, 323–329. doi: 10.1038/nature05286

Pubmed Abstract | Pubmed Full Text | CrossRef Full Text | Google Scholar

Kamoun, S., van West, P., Vleeshouwers, V. G. A. A., de Groot, K. E., and Govers, F. (1998). Resistance of Nicotiana benthamiana to Phytophthora infestans is mediated by the recognition of the elicitor protein INF1. Plant Cell 10, 1413–1425. doi: 10.1105/tpc.10.9.1413

Pubmed Abstract | Pubmed Full Text | CrossRef Full Text | Google Scholar

Kano, A., Hosotani, K., Gomi, K., Yamasaki-Kokudo, Y., Shirakawa, C., Fukumoto, T., et al. (2011). D-Psicose induces upregulation of defense-related genes and resistance in rice against bacterial blight. J. Plant Physiol. 168, 1852–1857. doi: 10.1016/j.jplph.2011.04.003

Pubmed Abstract | Pubmed Full Text | CrossRef Full Text | Google Scholar

Kawaguchi, Y., Nishiuchi, T., Kodama, H., Nakano, T., Nishimura, K., Shimamura, K., et al. (2012). Fungal elicitor-induced retardation and its restoration of root growth in tobacco seedlings. Plant Growth Regul. 66, 59–68. doi: 10.1007/s10725-011-9629-3

CrossRef Full Text | Google Scholar

Kawamura, Y., Hase, S., Takenaka, S., Kanayama, Y., Yoshioka, H., Kamoun, S., et al. (2009). INF1 elicitin activates jasmonic acid- and ethylene-mediated signalling pathways and induces resistance to bacterial wilt disease in tomato. J. Phytopathol. 157, 287–297. doi: 10.1111/j.1439-0434.2008.01489.x

CrossRef Full Text | Google Scholar

Khan, W. M., Prithiviraj, B., and Smith, D. L. (2002). Effect of foliar application of chitin and chitosan oligosaccharides on photosynthesis of maize and soybean. Photosynthetica 40, 621–624. doi: 10.1023/A:1024320606812

CrossRef Full Text | Google Scholar

Khatib, M., Lafitte, C., Esquerré-Tugayé, M.-T., Bottin, A., and Rickauer, M. (2004). The CBEL elicitor of Phytophthora parasitica var. nicotianae activates defence in Arabidopsis thaliana via three different signalling pathways. New Phytol. 162, 501–510. doi: 10.1111/j.1469-8137.2004.01043.x

CrossRef Full Text | Google Scholar

Khokon, M., Hossain, M. A., Munemasa, S., Uraji, M., Nakamura, Y., Mori, I. C., et al. (2010). Yeast elicitor-induced stomatal closure and peroxidase-mediated ROS production in Arabidopsis. Plant Cell Physiol. 51, 1915–1921. doi: 10.1093/pcp/pcq145

Pubmed Abstract | Pubmed Full Text | CrossRef Full Text | Google Scholar

Kim, T. H., Hauser, F., Ha, T., Xue, S., Böhmer, M., Nishimura, N., et al. (2011). Chemical genetics reveals negative regulation of abscisic acid signaling by a plant immune response pathway. Curr. Biol. 21, 990–997. doi: 10.1016/j.cub.2011.04.045

Pubmed Abstract | Pubmed Full Text | CrossRef Full Text | Google Scholar

King, S. R. F., McLellan, H., Boevink, P. C., Armstrong, M. R., Bukharova, T., Sukarta, O., et al. (2014). Phytophthora infestans RXLR effector PexRD2 interacts with host MAPKKK? to suppress plant immune signaling. Plant Cell 26, 1345–1359. doi: 10.1105/tpc.113.120055

Pubmed Abstract | Pubmed Full Text | CrossRef Full Text | Google Scholar

Kishimoto, K., Kouzai, Y., Kaku, H., Shibuya, N., Minami, E., and Nishizawa, Y. (2010). Perception of the chitin oligosaccharides contributes to disease resistance to blast fungus Magnaporthe oryzae in rice. Plant J. 64, 343–354. doi: 10.1111/j.1365-313X.2010.04328.x

Pubmed Abstract | Pubmed Full Text | CrossRef Full Text | Google Scholar

Knoth, C., Salus, M. S., Girke, T., and Eulgem, T. (2009). The synthetic elicitor 3,5-dichloroanthranilic acid induces NPR1-dependent and NPR1-independent mechanisms of disease resistance in Arabidopsis. Plant Physiol. 150, 333–347. doi: 10.1104/pp.108.133678

Pubmed Abstract | Pubmed Full Text | CrossRef Full Text | Google Scholar

Kohler, A., Schwindling, S., and Conrath, U. (2002). Benzothiadiazole-induced priming for potentiated responses to pathogen infection, wounding, and infiltration of water into leaves requires the NPR1/NIM1 gene in Arabidopsis. Plant Physiol. 128, 1046–1056. doi: 10.1104/pp.010744

Pubmed Abstract | Pubmed Full Text | CrossRef Full Text | Google Scholar

Kombrink, A., Sanchez-Vallet, A., and Thomma, B. P. (2011). The role of chitin detection in plant-pathogen interactions. Microb. Infect. 13, 1168–1176. doi: 10.1016/j.micinf.2011.07.010

Pubmed Abstract | Pubmed Full Text | CrossRef Full Text | Google Scholar

Konstantinidou-Doltsinis, S., Markellou, E., Kasselaki, A. M., Fanouraki, M. N., Koumaki, C. M., Schmitt, A., et al. (2006). Efficacy of Milsana®, a formulated plant extract from Reynoutria sachalinensis, against powdery mildew of tomato (Leveillula taurica). Biocontrol 51, 375–392. doi: 10.1007/s10526-005-5247-1

CrossRef Full Text | Google Scholar

Koschmann, J., Machens, F., Becker, M., Niemeyer, J., Schulze, J., Bülow, L., et al. (2012). Integration of bioinformatics and synthetic promoters leads to the discovery of novel elicitor-responsive cis-regulatory sequences in Arabidopsis. Plant Physiol. 160, 178–191. doi: 10.1104/pp.112.198259

Pubmed Abstract | Pubmed Full Text | CrossRef Full Text | Google Scholar

Kulye, M., Liu, H., Zhang, Y., Zeng, H., Yang, X., and Qiu, D. (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. 35, 2104–2120. doi: 10.1111/j.1365-3040.2012.02539.x

Pubmed Abstract | Pubmed Full Text | CrossRef Full Text | Google Scholar

Kunze, G., Zipfel, C., Robatzek, S., Niehaus, K., Boller, T., and Felix, G. (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

Pubmed Abstract | Pubmed Full Text | CrossRef Full Text | Google Scholar

Lacombe, S., Rougon-Cardoso, A., Sherwood, E., Peeters, N., Dahlbeck, D., van Esse, H. P., et al. (2010). Interfamily transfer of a plant pattern-recognition receptor confers broad-spectrum bacterial resistance. Nat. Biotechnol. 28, 365–369. doi: 10.1038/nbt.1613

Pubmed Abstract | Pubmed Full Text | CrossRef Full Text | Google Scholar

Lamesch, P., Berardini, T. Z., Li, D., Swarbreck, D., Wilks, C., Sasidharan, R., et al. (2011). The Arabidopsis Information Resource (TAIR): improved gene annotation and new tools. Nucleic Acids Res. 40, D1202–D1210. doi: 10.1093/nar/gkr1090

Pubmed Abstract | Pubmed Full Text | CrossRef Full Text | Google Scholar

Laquitaine, L., Gomès, E., François, J., Marchive, C., Pascal, S., Hamdi, S., et al. (2006). Molecular basis of ergosterol-induced protection of grape against Botrytis cinerea: induction of type I LTP promoter activity, WRKY, and stilbene synthase gene expression. Mol. Plant Microbe Interact. 19, 1103–1112. doi: 10.1094/MPMI-19-1103

Pubmed Abstract | Pubmed Full Text | CrossRef Full Text | Google Scholar

Lee, J., Klessig, D. F., and Nürnberger, T. (2001). A harpin binding site in tobacco plasma membranes mediates activation of the pathogenesis-related gene HIN1 independent of extracellular calcium but dependent on mitogen-activated protein kinase activity. Plant Cell 13, 1079–1093. doi: 10.1105/tpc.13.5.1079

Pubmed Abstract | Pubmed Full Text | CrossRef Full Text | Google Scholar

Li, W., Shao, M., Zhong, W., Yang, J., Okada, K., Yamane, H., et al. (2012). Ectopic expression of Hrf1 enhances bacterial resistance via regulation of diterpene phytoalexins, silicon and reactive oxygen species burst in rice. PLoS ONE 7:e43914. doi: 10.1371/journal.pone.0043914

Pubmed Abstract | Pubmed Full Text | CrossRef Full Text | Google Scholar

Libault, M., Wan, J., Czechowski, T., Udvardi, M., and Stacey, G. (2007). Identification of 118 Arabidopsis transcription factor and 30 ubiquitin-ligase genes responding to chitin, a plant-defense elicitor. Mol. Plant Microbe Interact. 20, 900–911. doi: 10.1094/MPMI-20-8-0900

Pubmed Abstract | Pubmed Full Text | CrossRef Full Text | Google Scholar

Liebrand, T. W. H., van den Berg, G. C. M., Zhang, Z., Smit, P., Cordewener, J. H. G., America, A. H. P., et al. (2013). Receptor-like kinase SOBIR1/EVR interacts with receptor-like proteins in plant immunity against fungal infection. Proc. Natl. Acad. Sci. U.S.A. 110, 10010–10015. doi: 10.1073/pnas.1220015110

Pubmed Abstract | Pubmed Full Text | CrossRef Full Text | Google Scholar

Liu, T., Liu, Z., Song, C., Hu, Y., Han, Z., She, J., et al. (2012). Chitin-induced dimerization activates a plant immune receptor. Science 336, 1160–1164. doi: 10.1126/science.1218867

Pubmed Abstract | Pubmed Full Text | CrossRef Full Text | Google Scholar

Liu, W., Liu, J., Ning, Y., Ding, B., Wang, X., Wang, Z., et al. (2013). Recent progress in understanding PAMP- and effector-triggered immunity against the rice blast fungus Magnaporthe oryzae. Mol. Plant 6, 605–620. doi: 10.1093/mp/sst015

Pubmed Abstract | Pubmed Full Text | CrossRef Full Text | Google Scholar

Livaja, M., Palmieri, M., von Rad, U., and Durner, J. (2008a). The effect of the bacterial effector protein harpin on transcriptional profile and mitochondrial proteins of Arabidopsis thaliana. J. Proteomics 71, 148–159. doi: 10.1016/j.jprot.2008.04.002

Pubmed Abstract | Pubmed Full Text | CrossRef Full Text | Google Scholar

Livaja, M., Zeidler, D., von Rad, U., and Durner, J. (2008b). Transcriptional responses of Arabidopsis thaliana to the bacteria-derived PAMPs harpin and lipopolysaccharide. Immunobiology 213, 161–171. doi: 10.1016/j.imbio.2007.10.004

Pubmed Abstract | Pubmed Full Text | CrossRef Full Text | Google Scholar

Lochman, J., and Mikes, V. (2006). Ergosterol treatment leads to the expression of a specific set of defence-related genes in tobacco. Plant Mol. Biol. 62, 43–51. doi: 10.1007/s11103-006-9002-5

Pubmed Abstract | Pubmed Full Text | CrossRef Full Text | Google Scholar

Maffei, M. E., Arimura, G. I., and Mithoefer, A. (2012). Natural elicitors, effectors and modulators of plant responses. Nat. Prod. Rep. 29, 1288–1303. doi: 10.1039/c2np20053h

Pubmed Abstract | Pubmed Full Text | CrossRef Full Text | Google Scholar

Mateos, F. V., Rickauer, M., and Esquerré-Tugayé, M.-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. 10, 1045–1053. doi: 10.1094/MPMI.1997.10.9.1045

Pubmed Abstract | Pubmed Full Text | CrossRef Full Text | Google Scholar

Mazzotta, S., and Kemmerling, B. (2011). Pattern recognition in plant innate immunity. J. Plant Pathol. 93, 7–17.

Google Scholar

McLellan, H., Boevink, P. C., Armstrong, M. R., Pritchard, L., Gomez, S., Morales, J., et al. (2013). An RxLR effector from Phytophthora infestans prevents re-localisation of two plant NAC transcription factors from the endoplasmic reticulum to the nucleus. PLoS Pathog. 9:e1003670. doi: 10.1371/journal.ppat.1003670

Pubmed Abstract | Pubmed Full Text | CrossRef Full Text | Google Scholar

Medeiros, F., Resende, M., Medeiros, F., Zhang, H., and Pare, P. (2009). Defense gene expression induced by a coffee-leaf extract formulation in tomato. Physiol. Mol. Plant P. 74, 175–183. doi: 10.1016/j.pmpp.2009.11.004

CrossRef Full Text | Google Scholar

Mercier, L., Lafitte, C., Borderies, G., Briand, X., Esquerré-Tugayé, M.-T., and Fournier, J. (2001). The algal polysaccharide carrageenans can act as an elicitor of plant defence. New Phytol. 149, 43–51. doi: 10.1046/j.1469-8137.2001.00011.x

CrossRef Full Text | Google Scholar

Milling, A., Babujee, L., and Allen, C. (2011). Ralstonia solanacearum extracellular polysaccharide is a specific elicitor of defense responses in wilt-resistant tomato plants. PLoS ONE 6:e15853. doi: 10.1371/journal.pone.0015853

Pubmed Abstract | Pubmed Full Text | CrossRef Full Text | Google Scholar

Mizoguchi, T., Ichimura, K., Irie, K., Morris, P., Giraudat, J., Matsumoto, K., et al. (1998). Identification of a possible MAP kinase cascade in Arabidopsis thaliana based on pairwise yeast two-hybrid analysis and functional complementation tests of yeast mutants. FEBS Lett. 437, 56–60. doi: 10.1016/S0014-5793(98)01197-1

Pubmed Abstract | Pubmed Full Text | CrossRef Full Text | Google Scholar

Mukhtar, M. S., Carvunis, A. R., Dreze, M., Epple, P., Steinbrenner, J., Moore, J., et al. (2011). Independently evolved virulence effectors converge onto hubs in a plant immune system network. Science 333, 596–601. doi: 10.1126/science.1203659

Pubmed Abstract | Pubmed Full Text | CrossRef Full Text | Google Scholar

Newman, M. A., Sundelin, T., Nielsen, J. T., and Erbs, G. (2013). MAMP (microbe-associated molecular pattern) triggered immunity in plants. Front. Plant Sci. 4:139. doi: 10.3389/fpls.2013.00139

Pubmed Abstract | Pubmed Full Text | CrossRef Full Text | Google Scholar

Newton, A. C., Fitt, B. D. L., Atkins, S. D., Walters, D. R., and Daniell, T. J. (2010). Pathogenesis, parasitism and mutualism in the trophic space of microbeplant interactions. Trends Microbiol. 18, 365–373. doi: 10.1016/j.tim.2010.06.002

Pubmed Abstract | Pubmed Full Text | CrossRef Full Text | Google Scholar

Nguyen, H. P., Chakravarthy, S., Velásquez, A. C., Mclane, H. L., Zeng, L. R., Nakayashiki, H., et al. (2010). Methods to study PAMP-triggered immunity using tomato and Nicotiana benthamiana. Mol. Plant Microbe Interact. 23, 991–999. doi: 10.1094/MPMI-23-8-0991

Pubmed Abstract | Pubmed Full Text | CrossRef Full Text | Google Scholar

Nürnberger, T., Nennstiel, D., Jabs, T., Sacks, W. R., Hahlbrock, K., and Scheel, D. (1994). High affinity binding of a fungal oligopeptide elicitor to parsley plasma membranes triggers multiple defense responses. Cell 78, 449–460. doi: 10.1016/0092-8674(94)90423-5

Pubmed Abstract | Pubmed Full Text | CrossRef Full Text | Google Scholar

Parker, J. E. (2003). Plant recognition of microbial patterns. Trends Plant Sci. 8, 245–247. doi: 10.1016/S1360-1385(03)00105-5

Pubmed Abstract | Pubmed Full Text | CrossRef Full Text | Google Scholar

Pastor, V., Luna, E., Mauch-Mani, B., Ton, J., and Flors, V. (2013). Primed plants do not forget. Environ. Exp. Bot. 94, 46–56. doi: 10.1016/j.envexpbot.2012.02.013

CrossRef Full Text | Google Scholar

Pedersen, C., van Themaat, E. V. L., McGuffin, L. J., Abbott, J. C., Burgis, T. A., Barton, G., et al. (2012). Structure and evolution of barley powdery mildew effector candidates. BMC Genomics 13:694. doi: 10.1186/1471-2164-13-694

Pubmed Abstract | Pubmed Full Text | CrossRef Full Text | Google Scholar

Peng, D. H., Qiu, D. W., Ruan, L. F., Zhou, C. F., and Sun, M. (2011). Protein elicitor PemG1 from Magnaporthe grisea induces systemic acquired resistance (SAR) in plants. Mol. Plant Microbe Interact. 24, 1239–1246. doi: 10.1094/MPMI-01-11-0003

Pubmed Abstract | Pubmed Full Text | CrossRef Full Text | Google Scholar

Povero, G., Loreti, E., Pucciariello, C., Santaniello, A., Di Tommaso, D., Di Tommaso, G., et al. (2011). Transcript profiling of chitosan-treated Arabidopsis seedlings. J. Plant Res. 124, 619–629. doi: 10.1007/s10265-010-0399-1

Pubmed Abstract | Pubmed Full Text | CrossRef Full Text | Google Scholar

Po-Wen, C., Singh, P., and Zimmerli, L. (2013). Priming of the Arabidopsis pattern-triggered immunity response upon infection by necrotrophic Pectobacterium carotovorum bacteria. Mol. Plant Pathol. 14, 58–70. doi: 10.1111/j.1364-3703.2012.00827.x

Pubmed Abstract | Pubmed Full Text | CrossRef Full Text | Google Scholar

Qiao, Y., Liu, L., Xiong, Q., Flores, C., Wong, J., Shi, J., et al. (2013). Oomycete pathogens encode silencing suppressors. Nat. Genet. 45, 330–333. doi: 10.1038/ng.2525

Pubmed Abstract | Pubmed Full Text | CrossRef Full Text | Google Scholar

Qiu, D., Mao, J., Yang, X., and Zeng, H. (2009). Expression of an elicitor-encoding gene from Magnaporthe grisea enhances resistance against blast disease in transgenic rice. Plant Cell Rep. 28, 925–933. doi: 10.1007/s00299-009-0698-y

Pubmed Abstract | Pubmed Full Text | CrossRef Full Text | Google Scholar

Qutob, D., Kemmerling, B., Brunner, F., Küfner, I., Engelhardt, S., Gust, A. A., et al. (2006). Phytotoxicity and innate immune responses induced by Nep1-like proteins. Plant Cell 18, 3721–3744. doi: 10.1105/tpc.106.044180

Pubmed Abstract | Pubmed Full Text | CrossRef Full Text | Google Scholar

Rafiqi, M., Ellis, J. G., Ludowici, V. A., Hardham, A. R., and Dodds, P. N. (2012). Challenges and progress towards understanding the role of effectors in plant-fungal interactions. Curr. Opin. Plant Biol. 15, 477–482. doi: 10.1016/j.pbi.2012.05.003

Pubmed Abstract | Pubmed Full Text | CrossRef Full Text | Google Scholar

Randoux, B., Renard-Merlier, D., Mulard, G., Rossard, S., Duyme, F., Sanssené, J., et al. (2010). Distinct defenses induced in wheat against powdery mildew by acetylated and nonacetylated oligogalacturonides. Phytopathology 100, 1352–1363. doi: 10.1094/PHYTO-03-10-0086

Pubmed Abstract | Pubmed Full Text | CrossRef Full Text | Google Scholar

Reglinski, T., Lyon, G. D., and Newton, A. C. (1994a). Assessment of the ability of yeast-derived elicitors to control barley powdery mildew in the field. Z. Pflanzenk. Pflanzen. 101, 1–10.

Google Scholar

Reglinski, T., Lyon, G. D., and Newton, A. C. (1994b). Induction of resistance mechanisms in barley by yeast-derived elicitors. Ann. Appl. Biol. 124, 509–517. doi: 10.1111/j.1744-7348.1994.tb04155.x

CrossRef Full Text | Google Scholar

Reglinski, T., Lyon, G. D., and Newton, A. C. (1995). The control of Botrytis cinerea and Rhizoctonia solani on lettuce using elicitors extracted from yeast cell walls. Z. Pflanzenk. Pflanzen. 102, 257–266.

Google Scholar

Ron, M., and Avni, A. (2004). The receptor for the fungal elicitor ethylene-inducing xylanase is a member of a resistance-like gene family in tomato. Plant Cell 16, 1604–1615. doi: 10.1105/tpc.022475

Pubmed Abstract | Pubmed Full Text | CrossRef Full Text | Google Scholar

Sangha, J. S., Ravichandran, S., Prithiviraj, K., Critchley, A. T., and Prithiviraj, B. (2010). Sulfated macroalgal polysaccharides lambda-carrageenan and iota-carrageenan differentially alter Arabidopsis thaliana resistance to Sclerotinia sclerotiorum. Physiol. Mol. Plant P. 75, 38–45. doi: 10.1016/j.pmpp.2010.08.003

CrossRef Full Text | Google Scholar

Schönbeck, F., Dehne, H.-W., and Balder, H. (1982). Zur Wirksamkeit induzierter Resistenz unter praktischen Anbaubedingungen I. Echter Mehltau an Reben, Gurken und Weizen. Z. Pflanzenk. Pflanzen. 89, 177–184.

Schönbeck, F., Dehne, H.-W., and Beicht, W. (1980). Untersuchungen zur Aktivierung unspeziefischer Resistenzmechanismen in Pflanzen. Z. Pflanzenk. Pflanzen. 87, 654–666.

Schornack, S., Huitema, E., Cano, L. M., Bozkurt, T. O., Oliva, R., Van Damme, M., et al. (2009). Ten things to know about oomycete effectors. Mol. Plant Pathol. 10, 795–803. doi: 10.1111/j.1364-3703.2009.00593.x

Pubmed Abstract | Pubmed Full Text | CrossRef Full Text | Google Scholar

Shimizu, T., Nakano, T., Takamizawa, D., Desaki, Y., Ishii-Minami, N., Nishizawa, Y., et al. (2010). Two LysM receptor molecules, CEBiP and OsCERK1, cooperatively regulate chitin elicitor signaling in rice. Plant J. 64, 204–214. doi: 10.1111/j.1365-313X.2010.04324.x

Pubmed Abstract | Pubmed Full Text | CrossRef Full Text | Google Scholar

Shinya, T., Gális, I., Narisawa, T., Sasaki, M., Fukuda, H., Matsuoka, H., et al. (2007). Comprehensive analysis of glucan elicitor-regulated gene expression in tobacco BY-2 cells reveals a novel MYB transcription factor involved in the regulation of phenylpropanoid metabolism. Plant Cell Physiol. 48, 1404–1413. doi: 10.1093/pcp/pcm115

Pubmed Abstract | Pubmed Full Text | CrossRef Full Text | Google Scholar

Shinya, T., Motoyama, N., Ikeda, A., Wada, M., Kamiya, K., Hayafune, M., et al. (2012). Functional characterization of CEBiP and CERK1 homologs in Arabidopsis and rice reveals the presence of different chitin receptor systems in plants. Plant Cell Physiol. 53, 1696–1706. doi: 10.1093/pcp/pcs113

Pubmed Abstract | Pubmed Full Text | CrossRef Full Text | Google Scholar

Shoresh, M., Yedidia, I., and Chet, I. (2005). Involvement of jasmonic acid/ethylene signaling pathway in the systemic resistance induced in cucumber by Trichoderma asperellum T203. Phytopathology 95, 76–84. doi: 10.1094/PHYTO-95-0076

Pubmed Abstract | Pubmed Full Text | CrossRef Full Text | Google Scholar

Steiner, U., Oerke, E.-C., and Schönbeck, F. (1988). Zur Wirksamkeit der induzierten Resistenz unter praktischen Anbaubedingungen IV. Befall und Ertrag von Wintergerstensorten mit induzierter Resistenz und nach Fungizidbehandlung. Z. Pflanzenk. Pflanzen. 95, 506–517.

Pubmed Abstract | Pubmed Full Text

Suzuki, H., Reddy, M. S. S., Naoumkina, M., Aziz, N., May, G. D., Huhman, D. V., et al. (2005). Methyl jasmonate and yeast elicitor induce differential transcriptional and metabolic re-programming in cell suspension cultures of the model legume Medicago truncatula. Planta 220, 696–707. doi: 10.1007/s00425-004-1387-2

Pubmed Abstract | Pubmed Full Text | CrossRef Full Text | Google Scholar

Takahashi, Y., Nasir, K. H. B., Ito, A., Kanzaki, H., Matsumura, H., Saitoh, H., et al. (2007). A high-throughput screen of cell-death-inducing factors in Nicotiana benthamiana identifies a novel MAPKK that mediates INF1-induced cell death signaling and non-host resistance to Pseudomonas cichorii. Plant J. 49, 1030–1040. doi: 10.1111/j.1365-313X.2006.03022.x

CrossRef Full Text | Google Scholar

Takken, F. L. W., Luderer, R., Gabriëls, S. H. E. J., Westerink, N., Lu, R., De Wit, P. J. G. M., et al. (2000). A functional cloning strategy, based on a binary PVX-expression vector, to isolate HR-inducing cDNAs of plant pathogens. Plant J. 24, 275–283. doi: 10.1046/j.1365-313x.2000.00866.x

Pubmed Abstract | Pubmed Full Text | CrossRef Full Text | Google Scholar

Tanaka, S., Ichikawa, A., Yamada, K., Tsuji, G., Nishiuchi, T., Mori, M., et al. (2010). HvCEBiP, a gene homologous to rice chitin receptor CEBiP, contributes to basal resistance of barley to Magnaporthe oryzae. BMC Plant Biol. 10:288. doi: 10.1186/1471-2229-10-288

Pubmed Abstract | Pubmed Full Text | CrossRef Full Text | Google Scholar

Thomas, C. M., Jones, D. A., Parniske, M., Harrison, K., Balint-Kurti, P. J., Hatzixanthis, K., et al. (1997). Characterization of the tomato Cf-4 gene for resistance to Cladosporium fulvum identifies sequences that determine recognitional specificity in Cf-4 and Cf-9. Plant Cell 9, 2209–2224. doi: 10.1105/tpc.9.12.2209

Pubmed Abstract | Pubmed Full Text | CrossRef Full Text | Google Scholar

Umemura, K., Tanino, S., Nagatsuka, T., Koga, J., Iwata, M., Nagashima, K., et al. (2004). Cerebroside elicitor confers resistance to Fusarium disease in various plant species. Phytopathology 94, 813–818. doi: 10.1094/PHYTO.2004.94.8.813

Pubmed Abstract | Pubmed Full Text | CrossRef Full Text | Google Scholar

Underwood, W. (2012). The plant cell wall: a dynamic barrier against pathogen invasion. Front. Plant Sci. 3:85. doi: 10.3389/fpls.2012.00085

Pubmed Abstract | Pubmed Full Text | CrossRef Full Text | Google Scholar

van den Burg, H. A., Harrison, S. J., Joosten, M. H. A. J., Vervoort, J., and De Wit, P. J. G. M. (2006). Cladosporium fulvum Avr4 protects fungal cell walls against hydrolysis by plant chitinases accumulating during infection. Mol. Plant Microbe Interact. 19, 1420–1430. doi: 10.1094/MPMI-19-1420

Pubmed Abstract | Pubmed Full Text | CrossRef Full Text | Google Scholar

van Hulten, M., Pelser, M., van Loon, L. C., Pieterse, C. M. J., and Ton, J. (2006). Costs and benefits of priming for defense in Arabidopsis. Proc. Natl. Acad. Sci. U.S.A. 103, 5602–5607. doi: 10.1073/pnas.0510213103

Pubmed Abstract | Pubmed Full Text | CrossRef Full Text | Google Scholar

Vatsa, P., Chiltz, A., Luini, E., Vandelle, E., Pugin, A., and Roblin, G. (2011). Cytosolic calcium rises and related events in ergosterol-treated Nicotiana cells. Plant Physiol. Biochem. 49, 764–773. doi: 10.1016/j.plaphy.2011.04.002

Pubmed Abstract | Pubmed Full Text | CrossRef Full Text | Google Scholar

Vera, J., Castro, J., Gonzalez, A., and Moenne, A. (2011). Seaweed polysaccharides and derived oligosaccharides stimulate defense responses and protection against pathogens in plants. Mar. Drugs 9, 2514–2525. doi: 10.3390/md9122514

Pubmed Abstract | Pubmed Full Text | CrossRef Full Text | Google Scholar

Viterbo, A. D. A., Wiest, A. R. I. C., Brotman, Y. A. R. I., Chet, I. L. A. N., and Kenerley, C. H. A. R. (2007). The 18mer peptaibols from Trichoderma virens elicit plant defence responses. Mol. Plant Pathol. 8, 737–746. doi: 10.1111/j.1364-3703.2007.00430.x

Pubmed Abstract | Pubmed Full Text | CrossRef Full Text | Google Scholar

Walters, D., and Bingham, I. (2007). Influence of nutrition on disease development caused by fungal pathogens: implications for plant disease control. Ann. Appl. Biol. 151, 307–324. doi: 10.1111/j.1744-7348.2007.00176.x

CrossRef Full Text | Google Scholar

Walters, D., and Heil, M. (2007). Costs and trade-offs associated with induced resistance. Physiol. Mol. Plant P. 71, 3–17. doi: 10.1016/j.pmpp.2007.09.008

CrossRef Full Text | Google Scholar

Walters, D. R., Ratsep, J., and Havis, N. D. (2013). Controlling crop diseases using induced resistance: challenges for the future. J. Exp. Bot. 64, 1263–1280. doi: 10.1093/jxb/ert026

Pubmed Abstract | Pubmed Full Text | CrossRef Full Text | Google Scholar

Wan, J., Zhang, X. C., Neece, D., Ramonell, K. M., Clough, S., Kim, S., et al. (2008). A LysM receptor-like kinase plays a critical role in chitin signaling and fungal resistance in Arabidopsis. Plant Cell 20, 471–481. doi: 10.1105/tpc.107.056754

Pubmed Abstract | Pubmed Full Text | CrossRef Full Text | Google Scholar

Wang, B., Wang, S., Tan, B., Qiu, D., and Yang, X. (2012a). Systemic acquired resistance to Tobacco mosaic virus (TMV) induced by protein elicitor from Verticillium dahliae (PevD1) and its mechanisms in tobacco. J. Agr. Biotechnol. 20, 188–195.

Pubmed Abstract | Pubmed Full Text | Google Scholar

Wang, B., Yang, X., Zeng, H., Liu, H., Zhou, T., Tan, B., et al. (2012b). The purification and characterization of a novel hypersensitive-like response-inducing elicitor from Verticillium dahliae that induces resistance responses in tobacco. App. Microbiol. Biotechnol. 93, 191–201. doi: 10.1007/s00253-011-3405-1

Pubmed Abstract | Pubmed Full Text | CrossRef Full Text | Google Scholar

Wang, F., Feng, G., and Chen, K. (2009). Burdock fructooligosaccharide induces resistance to tobacco mosaic virus in tobacco seedlings. Physiol. Mol. Plant P. 74, 34–40. doi: 10.1016/j.pmpp.2009.08.002

CrossRef Full Text | Google Scholar

Wang, S., Durrant, W. E., Song, J., Spivey, N. W., and Dong, X. (2010). Arabidopsis BRCA2 and RAD51 proteins are specifically involved in defense gene transcription during plant immune responses. Proc. Natl. Acad. Sci. U.S.A. 107, 22716–22721. doi: 10.1073/pnas.1005978107

Pubmed Abstract | Pubmed Full Text | CrossRef Full Text | Google Scholar

Wei, H., Xu, Q., Taylor, L. E. 2nd., Baker, J. O., Tucker, M. P., and Ding, S. Y. (2009). Natural paradigms of plant cell wall degradation. Curr. Opin. Biotechnol. 20, 330–338. doi: 10.1016/j.copbio.2009.05.008

Pubmed Abstract | Pubmed Full Text | CrossRef Full Text | Google Scholar

Xu, Y., Chen, H., Zhou, X., and Cai, X. (2012). Induction of hypersensitive response and nonhost resistance by a Cladosporium fulvum elicitor CfHNNI1 is dose-dependent and negatively regulated by salicylic acid. J. Integr. Agri. 11, 1665–1674. doi: 10.1016/S2095-3119(12)60169-5

CrossRef Full Text | Google Scholar

Yang, D. H., Hettenhausen, C., Baldwin, I. T., and Wu, J. (2011). The multifaceted function of BAK1/SERK3: plant immunity to pathogens and responses to insect herbivores. Plant Signal. Behav. 6, 1322–1324. doi: 10.4161/psb.6.9.16438

Pubmed Abstract | Pubmed Full Text | CrossRef Full Text | Google Scholar

Yang, Y., Zhang, H., Li, G., Li, W., Wang, X., and Song, F. (2009). Ectopic expression of MgSM1, a Cerato-platanin family protein from Magnaporthe grisea, confers broad-spectrum disease resistance in Arabidopsis. Plant Biotechnol. J. 7, 763–777. doi: 10.1111/j.1467-7652.2009.00442.x

Pubmed Abstract | Pubmed Full Text | CrossRef Full Text | Google Scholar

Zhang, J., Shao, F., Li, Y., Cui, H., Chen, L., Li, H., et al. (2007). A Pseudomonas syringae effector inactivates MAPKs to suppress PAMP-induced immunity in plants. Cell Host Microbe 1, 175–185. doi: 10.1016/j.chom.2007.03.006

Pubmed Abstract | Pubmed Full Text | CrossRef Full Text | Google Scholar

Zhang, J., Tong, Z., Gao, Z., Luo, C., Qu, S., and Zhang, Z. (2011a). Expression of MhWRKY1 gene induced by the elicitors SA, MeJA, ACC and the apple ring spot pathogen. Sci. Agric. Sin. 44, 990–999.

Google Scholar

Zhang, W., Yang, X., Qiu, D., Guo, L., Zeng, H., Mao, J., et al. (2011b). PeaT1-induced systemic acquired resistance in tobacco follows salicylic acid-dependent pathway. Mol. Biol. Rep. 38, 2549–2556. doi: 10.1007/s11033-010-0393-7

Pubmed Abstract | Pubmed Full Text | CrossRef Full Text | Google Scholar

Zhang, W., Fraiture, M., Kolb, D., Löffelhardt, B., Desaki, Y., Boutrot, F. F., et al. (2013). Arabidopsis receptor-like protein30 and receptor-like kinase suppressor of BIR1-1/EVERSHED mediate innate immunity to necrotrophic fungi. Plant Cell 25, 4227–4241. doi: 10.1105/tpc.113.117010

Pubmed Abstract | Pubmed Full Text | CrossRef Full Text | Google Scholar

Zhang, Y., Yang, X., Liu, Q., Qiu, D., Zhang, Y., Zeng, H., et al. (2010). Purification of novel protein elicitor from Botrytis cinerea that induces disease resistance and drought tolerance in plants. Microbiol. Res. 165, 142–151. doi: 10.1016/j.micres.2009.03.004

Pubmed Abstract | Pubmed Full Text | CrossRef Full Text | Google Scholar

Zheng, X., McLellan, H., Fraiture, M., Liu, X., Boevink, P. C., Gilroy, E. M., et al. (2014). Functionally redundant RXLR effectors from Phytophthora infestans act at different steps to suppress early flg22-triggered immunity. PLoS Pathog. 10:e1004057. doi: 10.1371/journal.ppat.1004057

Pubmed Abstract | Pubmed Full Text | CrossRef Full Text | Google Scholar

Zipfel, C., Kunze, G., Chinchilla, D., Caniard, A., Jones, J. D. G., Boller, T., 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

Pubmed Abstract | Pubmed Full Text | CrossRef Full Text | Google Scholar

Zipfel, C., Robatzek, S., Navarro, L., Oakeley, E. J., Jones, J. D. G., Felix, G., et al. (2004). Bacterial disease resistance in Arabidopsis through flagellin perception. Nature 428, 764–767. doi: 10.1038/nature02485

Pubmed Abstract | Pubmed Full Text | CrossRef Full Text | Google Scholar

Keywords: crop protection, elicitors, pathogen effectors, priming, disease resistance

Citation: Wiesel L, Newton AC, Elliott I, Booty D, Gilroy EM, Birch PRJ and Hein I (2014) Molecular effects of resistance elicitors from biological origin and their potential for crop protection. Front. Plant Sci. 5:655. doi: 10.3389/fpls.2014.00655

Received: 12 September 2014; Accepted: 04 November 2014;
Published online: 21 November 2014.

Edited by:

Rebecca Bart, Donald Danforth Plant Science Center, USA

Reviewed by:

Dale Ronald Walters, Scotland's Rural College, UK
Simone Ferrari, Sapienza Università di Roma, Italy

Copyright © 2014 Wiesel, Newton, Elliott, Booty, Gilroy, Birch and Hein. This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) or licensor are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.

*Correspondence: Ingo Hein, The James Hutton Institute, Errol Road, Invergowrie, Dundee DD2 5DA, UK e-mail: ingo.hein@hutton.ac.uk