Nonhost resistance to plant pathogens can be constitutive or induced by microbes. Successful pathogens suppress microbe-induced plant defences by delivering appropriate effectors, which are apparently not sufficiently effective on nonhost plant species, as can be concluded from the strong host specificity of many biotroph plant pathogens. Such effectors act on particular plant targets, such as promoters or motifs in expressed sequences. Despite much progress in the elucidation of the molecular aspects of nonhost resistance to plant pathogens, very little is known about the genes that determine whether effectors can or cannot suppress the basal defence. In hosts they can, in nonhosts they cannot. The targets determining the host status of plants can be identified in inheritance studies. Recent reports have indicated that nonhost resistance is inherited polygenically, and exhibits strong similarity and association with the basal resistance of plants to adapted pathogens.
Plant scientists have long considered nonhost resistance (Box 1, Glossary) to potential pathogens and pests to be a very important and interesting phenomenon because of its complete effect and apparent great durability (Box 1, Glossary). Exciting new insights have been summarized and discussed in recent review papers (for example, Mysore & Ryu, 2004; Nürnberger & Lipka, 2005; Ingle et al., 2006; Jones & Dangl, 2006; O’Connell & Panstruga, 2006; Bent & Mackay, 2007; Ryan et al., 2007; Schweizer, 2007; Lipka et al., 2008). From these reviews, it has become increasingly clear how adapted pathogens are perceived and how they reprogramme plant cells to establish an infection. However, it remains poorly understood how to explain the high degree of host specificity (Box 1, Glossary) of these pathogens. Why is it that many pathogens infect only one or a few related plant species, but not other related plant species?
Nonhost resistance to unadapted pathogens results from a continuum of layered defences (Heath, 1997; da Cunha et al., 2006; Ham et al., 2007), including constitutive and induced defence mechanisms. Constitutive barriers are more likely to contribute to nonhost resistance to pathogens of other plant families than to pathogens of plant species that are related to the nonhost. In this review, we focus on the induced component of nonhost resistance, which is probably the most relevant phenomenon if the nonhost plant species is related to the host of the would-be pathogen. We take most examples from mildew and rust pathosystems, where the formation of a haustorium (Box 1, Glossary) may or may not be prevented by the attacked plant cell. In rust and mildew fungal pathogens, specificity is a striking feature, as nonhost plants may be closely related to the host plant species of a particular rust or mildew species.
In this review, we integrate nonhost resistance and basal resistance concepts (Basic concepts section) in order to account for the specificity of defence suppression. We argue that: (1) nonhost resistance and basal resistance to adapted pathogens may rest on the same or similar principles; and (2) effective suppression of pathogen-associated molecular pattern (PAMP)-triggered immunity (Basic concepts section and Box 1, Glossary) requires sets of specific effectors, the plant targets of which should be revealed by inheritance studies.
Nonhost resistance is the resistance shown by an entire plant species to all genetic variants of a pathogen (Heath, 1997; Mysore & Ryu, 2004; Nürnberger & Lipka, 2005). However, presuming that pathogenic microbes co-evolve with radiating plant species during evolution (Heath, 1997; Inuma et al., 2007), we may expect that some plant species are currently in the process of losing or acquiring the host status (Box 1, Glossary) to a certain microbial species, taking some intermediate position between host and nonhost status, as reported for barley in response to Puccinia rust fungi (Atienza et al., 2004; Fig. 1).
Induced defence is prompted by the infection attempt of the would-be pathogen. In haustorium-forming specialized pathogens, one particularly common feature is defective haustorium formation on nonhost plant species, termed pre-haustorial or penetration resistance (Niks, 1987; Heath, 2002; Collins et al., 2007; Hardham et al., 2007). This defence typically leads to the formation of cell wall reinforcements, also called cell wall appositions or papillae (O’Connell & Panstruga, 2006; Hückelhoven, 2007). Frequently, pre-haustorial nonhost resistance is backed up by hypersensitive post-penetration resistance to those infection units that still succeed in penetrating the cell wall (Heath, 2002; Lipka et al., 2005). The process of this cell death in nonhost plants is not necessarily the same as that occurring during hypersensitive resistance of host species (Christopher-Kozjan & Heath, 2003), and is therefore not necessarily the result of a resistance–avirulence (R–Avr) interaction.
Basal resistance and basic compatibility
Many authors use the term ‘basal resistance’ in a qualitative manner to refer to completely effective nonhost resistance against potential pathogens (Heath, 1997). Basal resistance is the complement of the term ‘basic compatibility’, which results from the capacity of the microbe to effectively overcome the defence mechanisms that plant species mount against unadapted microbial intruders (Heath, 1997). Therefore, the relationships of barley–Puccinia hordei and wheat–P. triticina represent examples of basic compatibility, and the relationships of barley–P. triticina and wheat–P. hordei represent examples of qualitative basal resistance (Fig. 2a).
Dangl & Jones (2001) defined basal defence in a more quantitative manner, that is, defence that inhibits pathogen spread after successful infection and onset of disease, and is inferred from the identification of mutants that are more susceptible to a virulent pathogen than their parents. However, in the absence of mutagenesis, many, if not all, plant pathosystems exhibit naturally occurring gradations from fair to extreme susceptibility (Parlevliet, 1992). A substantial part of this quantitative resistance may be considered as quantitative basal resistance. Assuming that several genetic factors determine a plant species’ host status to a would-be pathogen (Fig. 2b), it can be expected that such genetic factors differ within a host plant species for that microorganism, making one host plant genotype a more suitable host individual than another genotype of the same species (Fig. 2c). Such differences may be a remnant of the nonhost status of a distant ancestor, or the start of the development of becoming a nonhost.
In light of this, we hypothesize that qualitative basal resistance leading to nonhost resistance and quantitative basal resistance may rest on the same or similar principles. For rust and powdery mildew pathosystems, this hypothesis is supported by the observation that both nonhost and host basal resistances are typically a result of a pre-haustorial defence reaction (Niks, 1986; Olesen et al., 2003).
Perception and suppression
For the host plant, a prerequisite to the activation of defence is the perception of the pathogenic threat. This can be either direct, via a microbe-associated molecular pattern (MAMP), or by plant receptor detection of microbe-induced molecular patterns (MIMPs) (Mackey & McFall, 2006; Bittel & Robatzek, 2007). These recognized factors, also designated by the acronym PAMP (Ingle et al., 2006), are highly conserved. Relatively few molecular motifs have been identified that contain MAMPs (reviewed in Nürnberger & Lipka, 2005; Ingle et al., 2006). O’Connell & Panstruga (2006) compared MAMPs with ‘identity cards’ of the pathogen. We presume that MAMPs are generally too conserved to allow, for example, barley to distinguish the unadapted wheat leaf rust fungus from the adapted barley leaf rust fungus.
In order to succeed in its infection attempt, a pathogen either evades recognition of its MAMPs (Andersen-Nissen et al., 2005; Sun et al., 2006) or, more commonly, suppresses all plant defences immediately after their elicitation (Ingle et al., 2006). As related adapted and unadapted pathogen species are likely to contain (near-) identical MAMPs, they induce basal defence in any plant attacked, regardless of whether the plants are hosts or nonhosts. Adapted pathogens, however, suppress this reaction in their host plant within hours (Li et al., 2005; Caldo et al., 2006; Truman et al., 2006). In addition, the observation that plant cells that are pre-infected with an adapted pathogen commonly show ‘induced accessibility’ to unadapted forms of these pathogens strongly argues that basic compatibility involves the suppression of defence (Holub & Cooper, 2004).
Important advances are being made in the understanding of the mechanisms of suppression of basal defence by pathogen effectors (Box 1, Glossary; Speth et al., 2007; Block et al., 2008; Göhre & Robatzek, 2008). This phenomenon is particularly well described for bacterial effectors, but recent examples support a similar virulence role of fungal effectors, such as AVRa10 and AVRk1 of the Blumeria graminis f.sp. hordei fungus on barley (Ridout et al., 2006), Avr1 of the Fusarium oxysporum f.sp. lycopersici fungus on tomato (Houterman et al., 2008) and Avr2 from the Cladiosporium fulvum fungus on tomato (van Esse et al., 2008; Shabab et al., 2008). Such effectors are delivered by the pathogen into either the apoplast or the plant cell cytoplasm. The predominant function of effectors is to reprogramme plant cell gene expression, either by downregulation of defence genes or upregulation of negative regulators of basal defence (Block et al., 2008). Effectors (O’Connell & Panstruga, 2006) and their operative targets in the plant (van der Hoorn & Kamoun, 2008) both seem to be under strong diversifying selection. van der Hoorn & Kamoun (2008) argued that selection forces on operative targets may result in decreased binding affinity with the effector to evade detection and manipulation by the effector. An alternative selection force results in the evolution of decoys, which mimic operative targets of pathogen effectors, but their manipulation does not result in enhanced pathogen fitness. Mackey & McFall (2006) compared the collection of effectors produced by a pathogen to a ‘tool kit’, in which some effectors might be redundant in combination with other effectors or may contribute to pathogenicity on different host species. However, it is unknown whether such effectors are also delivered in related nonhost plant species. If not, what plant factors induce the delivery of effectors in host plants? Moreover, if effectors are delivered in tissues of a related nonhost plant, why can they not effectively suppress basal defence there?
Host specificity-determining factors in the pathogen
The characterization of fungal pathogen effectors and their host targets is crucial in explaining the specificity of basal defence suppression. Which plant targets determine whether the basal resistance can be successfully suppressed (in a highly susceptible host), only partially suppressed (in a marginal host species or a host plant with a high level of quantitative basal resistance) or not suppressed at all (in a nonhost species) by a certain would-be pathogen?
Several pathogen factors have been suggested to assist in the neutralization of the plant's basal defence (O’Connell & Panstruga, 2006). Examples include the antioxidative proteins secreted by B. graminis that presumably cope with plant-derived oxidative stress (Zhang et al., 2004), and the coronatine produced by Pseudomonas to repress salicylic acid-mediated defence (DebRoy et al., 2004; Melotto et al., 2006; O’Connell & Panstruga, 2006). All such compounds, however, seem to be effective in a general, plant-nonspecific manner. The tomato pathogen C. fulvum produces an effector AVR4 that has been implicated to protect the fungal cell wall against hydrolysis by plant chitinases. However, heterologous expression of AVR4 in Arabidopsis demonstrates that it also protects against chitinases produced by this nonhost species (van Esse et al., 2007), but this is apparently insufficient to make Arabidopsis a host species. Such compounds are therefore not sufficient to explain why would-be pathogens can establish basic compatibility in a host plant species, but not in a relatively closely related nonhost plant species. Therefore, these pathogen delivered compounds, as such, are not likely to account for the specificity of defence suppression.
How to identify host status-determining genes?
Genes involved in basal resistance
Simple mutagenesis, serial mutagenesis, gene silencing and gene expression studies, mostly in Arabidopsis, but also in barley, have led to the identification of genes and gene networks that contribute to nonhost and/or basal resistance, or act as negative regulators of defence reactions. Key genes that have been implicated in these processes are very diverse (examples in Table 1), and gene expression profiles indicate a large overlap of plant responses towards different MAMPs (Bittel & Robatzek, 2007). Compilation of mutant genes may turn a nonhost plant into a susceptible plant, as shown for Arabidopsis in response to pea powdery mildew fungus Erysiphe pisi (Lipka et al., 2005, 2008), suggesting a central role of the involved genes in basal resistance. Nevertheless, such genes probably represent relatively conserved defence systems with conserved sequence motifs, even across monocotyledons and dicotyledons, as has been demonstrated, for example, for Ror2 in barley and Pen1 in Arabidopsis (Collins et al., 2003). Ror2 and Pen1 have an effect on powdery mildew fungi, but apparently they are unable to compromise the infection by an adapted powdery mildew species. We presume that adapted mildew species can successfully suppress such genes, or upstream regulators, but unadapted mildew cannot.
Table 1. Examples of plant genes implicated to play a role in basal and/or nonhost resistance to microbial pathogens and for which the sequences are known
Drug resistance (PDR) ATP-binding cassette (ABC) transporter
Bgh, Ep, Pi
Genes involved in the positive or negative regulation of basal defences
BAX inhibitor 1
Calcium-dependent protein kinases
Downy mildew resistant 6
Glycine-rich RNA-binding protein
Seven-transmembrane domain protein
Bgh, Mg, Cs
Seven-transmembrane domain protein
Ep, Bgh, Aa, Pi
Modifier of snc1,3
Nucleoside diphosphate hydrolase
Powdery mildew resistant 5
Powdery mildew resistant 6
AtPep precursor genes
RPM1-interacting protein 4
Brassinosteroid-associated kinase 1
Genes involved in salicylic acid signalling
Enhanced susceptibility 1
Hp, Pso, Psm, Pp
Ep, Bgh, Bgt
Enhanced susceptibility 5
Ep, Bgt, Psp
Senescence-associated gene 101
Nonexpressor of PR-genes 1
Homologues of NPR1
PMR4 (CalS12, GSL5)
Powdery mildew resistant 4
Gc, Go, Pp
Isochorismate synthase 1
Pp, Pso, Go
Uv, Ua, Psp
Genes involved in redox signalling
ADP-ribosylation factor 1
Class III peroxidase proteins
Transcription factors and signalling cascades
NAC transcription factors
NAC transcription factors
bZIP transcription factors
bZIP transcription factors
Group II WRKY transcription factors
Group II WRKY transcription factors
Pso, Bc, Go
Mitogen-activated protein kinases
Psm, Pso, Pp
Mitogen-activated protein kinases
Antifungal proteins and others
Pectin methylesterase inhibitor protein 1
Psp, Pss, Pst
Overexpressor of cationic peroxidase
Small secreted membrane proteins
Inheritance of natural variation in nonhost resistance
Genes that contribute to resistance and have been discovered by mutagenesis or gene expression studies, such as those mentioned in Table 1, do not necessarily explain why one plant species is a host and another a nonhost, as they may be too conserved within and among plant species and not sufficiently specific in their effectiveness when expressed. Nevertheless, such genes may differ in details of the expressed sequences or of the promoter region that make them prone to silencing by effectors of adapted pathogens, but not to those of unadapted pathogens. We argue that inheritance studies are helpful in identifying plant genes that determine specificity. In this section, we review the perspectives and results of some possible approaches (Table 2).
Table 2. Possible ways to study inheritance in basal defence to specialized plant pathogens in order to identify the genes responsible for natural variation
QTL, quantitative trait locus.
1. Crossing nonhost × host species
Lettuce, Lactuca sativa × L. saligna. The latter is nonhost to Bremia lactucae
Nonhost resistance in L. saligna is a result of c. 15 QTLs; great redundancy, as about three QTLs are sufficient to confer complete resistance
The overriding difficulty in inheritance studies for nonhost resistance is that they require, by definition, interspecific hybridization. Such crosses are typically associated with hybrid sterility, abnormal segregation and other artefacts, which hamper classical genetics. The Lactuca–Bremia interaction (Jeuken et al., 2008) is one of the few cases in which a host and a nonhost plant species are sufficiently compatible to allow classical genetics (Table 2).
A second possibility is to study the inheritance of quantitative differences in components of defence (Table 2). Such studies are hampered by the relatively small differences in the levels of components of the infection process and by the need for tedious microscopic observations.
In marginal host species, some odd genotypes have been found that demonstrate susceptibility to a pathogen to which the species is normally considered a nonhost. In some cases, this resistance is inherited qualitatively, often with the involvement of some additional minor genes (Table 2). For example, barley is a marginal host to at least nine rust fungal species of cereals and grasses (Fig. 1) (Atienza et al., 2004). This indicates that a few barley accessions still carry some genes for susceptibility to the wheat leaf rust fungus, as depicted in Fig. 2c (top right quadrant). None of the barley accessions were as susceptible as the respective host species of the rust fungus. Therefore, Atienza et al. (2004) accumulated susceptibility alleles by convergent crossing, resulting in an experimental line, SusPtrit, that is as highly susceptible to P. triticina as a typical susceptible wheat accession. This line was crossed with two barley cultivars with normal immunity to P. triticina to develop two mapping populations. The remarkable results were as follows:
• SusPtrit is not only exceptionally susceptible to P. triticina, but is also susceptible to several other unadapted rust fungi; however, it is fully resistant to several other grass rust fungi, such as the leaf rust fungus P. recondita of rye, suggesting that the nonhost defence mechanisms in SusPtrit are not totally impaired (Atienza et al., 2004).
• The immunity of the two cultivars to several unadapted rust fungi is based on a large number of quantitative trait loci (QTLs) with overlapping specificities for rust fungal species (Jafary et al., 2006, 2008).
• The two immune cultivars share hardly any QTLs for resistance to the same heterologous rust fungal species (see Box 1, Glossary), implying that immunity across the barley species to a particular heterologous rust fungus is a result of a high diversity of genes (Jafary et al., 2008).
• There is statistically significant co-localization of QTLs for resistance to heterologous rust fungi with QTLs for quantitative basal resistance to the adapted barley leaf rust pathogen P. hordei (Jafary et al., 2008).
• The QTLs for quantitative basal resistance to P. hordei and nonhost resistance to the heterologous rust fungi co-locate significantly with genes that are implicated in the basal resistance gene network (Marcel et al., 2007a; Jafary et al., 2008).
Basal resistance to an adapted pathogen as an alternative research phenomenon
If, as argued above, qualitative basal resistance, leading to nonhost resistance, and quantitative basal resistance rest on similar principles, the understanding of basal resistance to an adapted host (Fig. 2c, top left quadrant) is relevant for the understanding of nonhost resistance to related, but unadapted, pathogens. In barley, more than 20 QTLs have been mapped for quantitative basal resistance to the barley leaf rust fungus P. hordei (Qi et al., 1998; Marcel et al., 2007a, 2008; T. C. Marcel & R. E. Niks, unpublished). The loci tend not to co-locate with loci for hypersensitive resistance (Qi et al., 1998), but with loci for resistance to heterologous rust fungi (Jafary et al., 2008, see above). Following a positional cloning strategy, Marcel et al. (2007b) fine-mapped one QTL for quantitative resistance to P. hordei to an interval of 0.11 cM, corresponding to less than 200 kb (T. C. Marcel et al., unpublished). This suggests that positional cloning is feasible. Interestingly, evidence suggests that this QTL also contributes to resistance to the heterologous rust fungus P. persistens, which is pathogenic to couch grass, Elytrigia repens (Jafary et al., 2008).
Minor gene-for-minor gene interaction
Careful quantitative observations of basal resistance indicate small plant genotype × pathogen isolate interactions in barley to P. hordei (Parlevliet, 1978; Marcel et al., 2008) and other plant pathosystems. Based on such observations, Parlevliet & Zadoks (1977) proposed a minor gene-for-minor gene interaction between plants and pathogens. In molecular terms, this hypothesis implies that basal defence-promoting genes or compounds are specifically targeted by defence-suppressing effectors delivered by the would-be pathogen. If effectors reprogramme plant gene expression, the minor gene-for-minor gene interaction is consistent with the hypothesis that each effector can specifically block a certain promoter binding site, or splice a transcript or translation product of the plant gene as a result of a certain motif.
As the R–Avr gene-for-gene interaction is infamous for its lack of resistance durability (Flor, 1971; Keller et al., 2000), the question arises as to whether a minor gene-for-minor gene interaction is at odds with the experienced durability of quantitative basal resistance and nonhost resistance.
The durability aspect
Relevant aspects that explain the low durability of R-gene resistance include the following:
• Breaking the resistance requires only one simple, rather arbitrary, loss-of-function mutation in the cognate Avr gene of the pathogen. For such a mutation, there are numerous alternatives. De Wit (2000) listed six mutations in the Avr4 allele, all of which led to virulence of C. fulvum to Cf4-containing tomato.
• Although Avr determinants are supposed to be effectors, and hence contribute to the pathogenicity of the pathogen, a loss-of-function mutation or deletion is apparently easily tolerated by the pathogen, suggesting that many effectors are dispensable (Skamnioti & Ridout, 2005).
• The mutation resulting in the loss of the cognate Avr leads to a dramatically higher reproduction of the virulent pathogen compared with avirulent genotypes, especially where, in agricultural contexts, the corresponding R gene occurs in a large proportion of the crop acreage. Indeed, many R genes have been introduced into several popular cultivars.
We propose four arguments for the contention that the minor gene-for-minor gene hypothesis discussed above is compatible with the perceived durability of basal resistance.
• In order to reprogramme a certain plant defence gene to attenuate the defence response, the pathogen requires a specific gain-of-function sequence change in one or more of its effector genes, which should be rare.
• As nonhost plant genotypes may contain redundant defence-related genes [see the Lettuce–Bremia example (Table 2; M. J. W. Jeuken et al., unpublished)], neutralization of only one of them should not result in a selective advantage for the mutant pathogen.
• In the case of quantitative basal resistance, a mutation in the pathogen will result in only an incremental enhancement in its fitness.
• There is great diversity in genes for basal resistance between plant genotypes, at least in cultivated barley–P. hordei (Marcel et al., 2007a). Therefore, each basal defence gene that the mutant pathogen overcomes probably only occurs in a small proportion of the host population or crop acreage. This would further limit the selective advantage of the microbial mutant.
Therefore, when a minor gene-for-minor gene interaction exists between microbe effectors and the plant basal defence gene network, durability can be achieved without the need for invoking multilayered defence. Of course, this represents ‘durability’ on a time scale that can be observed by humans.
Integration of concepts
The concepts discussed above beg the question of why effectors delivered by a would-be pathogen succeed in reprogramming the plant gene expression to suppress defence in one plant species, but not in another related nonhost plant species? The key to answering this question should be specific motifs in the effector targets, and we propose that inheritance studies (Table 2) and subsequent cloning and allele mining may reveal these targets.
Several reviews consider and cite evidence that stacked R genes determine the nonhost status of a plant species to an unadapted pathogen (for example, Mysore & Ryu, 2004; Bent & Mackay, 2007; Schweizer, 2007). Another R-gene-related hypothesis proposes that some R genes have a residual effect on virulent isolates (Li et al. 1999; Dowkiw & Bastien, 2007), and that such defeated R genes may be perceived as QTLs for basal resistance. A third R-gene-related hypothesis, often confused with the previous one, is that quantitative resistance genes are small-effect allelic variants of R genes. In this case, the genes have not been ‘defeated’ by a mutation in the pathogen, but are allelic to R genes, and hence are likely to be of the nucleotide-binding site–leucine-rich repeat (NBS–LRR) type, demonstrating only a weak effect (Bai et al., 2003; Tan et al., 2008). These hypotheses are all plausible in certain cases, but are not supported in cases in which QTLs for basal resistance do not co-locate with R genes or R-gene analogues (Qi et al., 1998; Wisser et al., 2005), nor where nonhost resistance acts in the pre-haustorial stage of infection, whereas R genes mostly mediate a hypersensitivity response after haustorium formation (Collins et al., 2007). The current paradigm that would-be pathogens contain MAMPs that elicit basal defence, which, in turn, should be suppressed in a specific manner, also suggests the existence of a resistance mechanism that is not based on R genes.
In the present review, we propose that motif variation in defence network genes (like those listed in Table 1) or their regulatory regions may determine whether effectors of would-be pathogens will or will not alter the expression levels of such genes before, during or after transcription or translation. This hypothesis is consistent with the observation that many such defence network genes are located in confidence intervals of QTLs for quantitative basal resistance and nonhost resistance to specialized plant pathogens (Faris et al., 1999; Trognitz et al., 2002; Ramalingam et al., 2003; Liu et al., 2004; Wisser et al., 2005; Marcel et al., 2007a; Jafary et al., 2008). Some of these genes have been shown to play a role in basal resistance of barley to powdery mildew by transient induced gene silencing or transient overexpression (Douchkov et al. 2005; Schweizer, 2007). Furthermore, this hypothesis is in agreement with strong evidence for suppression of defence gene expression as a requirement for the establishment of a compatible interaction, and with the assumption that effector targets are under strong evolutionary constraints to escape pathogen recognition (Block et al., 2008; van der Hoorn & Kamoun, 2008). A very relevant and interesting research line may corroborate the role of effectors in host species specificity. Atypical Pseudomonas syringae pv. tomato isolate DC3000 can infect tomato (Solanaceae) and Arabidopsis thaliana (Brassicaceae). Typical pv. tomato isolates, such as T1, are not pathogenic on A. thaliana (Brassicaceae). There is evidence that resistance of Arabidopsis to the typical pv. tomato isolates is multigenic (Yan et al., 2008). Almeida et al. (2009) reported highly different, but overlapping, effector repertoires for T1 and DC3000. This indicates that, for suppression of defence in the two plant species, different sets of effectors are required. Finally, it is in agreement with the minor gene-for-minor gene interaction and the polygenic inheritance of basal defence and nonhost resistance.
At least three unexplained phenomena challenge our hypothesis that specificity is a result of specific reprogramming of defence genes by effectors.
• How can we explain the ability of some pathogens to infect a wide host range, such as P. coronata var. hordei, which can infect about 20 Hordeum species, including H. vulgare, and many other grass genera, such as Bromus, Agropyron, Aegilops, Phalaris and Secale (Jin & Steffenson, 1999)? Should we presume that this pathogen has a larger or more versatile array of effectors than an extreme specialist, such as the related P. hordei, which can only infect common barley H. vulgare/spontaneum (Anikster, 1989)?
• On a particular plant species, different but related would-be pathogens, such as different rust fungal species, should presumably all reprogramme the same set of basal defence genes in order to establish basic compatibility. However, in a barley mapping population, the genes for basal resistance to eight heterologous rust fungal species had only overlapping specificities, i.e. the large majority were only effective against one or two of them (Jafary et al., 2006, 2008). These results suggest great redundancy in basal defence genes, of which only a relatively few must be suppressed in order to lead to successful infection.
Only cloning, sequencing and comparison of effector alleles in the pathogen and their targets in the plant can provide a definitive answer to such questions regarding host ranges and specificity of defence suppression. An understanding of the plant factors responsible for basal resistance and the strategy of the adapted pathogen to reprogramme such factors is required to develop crop genotypes that behave as quasi-nonhosts to economically important pathogens, which is of great economic relevance.
Box 1 GlossaryBasal defence/resistance: qualitative: defence that plant species mount against unadapted microbial intruders. quantitative: defence that reduces pathogen spread after successful infection and onset of disease. Basic compatibility: state that results from the capacity of the microbe to deal effectively with the defence that plant species mount against unadapted microbial intruders. Durability of resistance: resistance that has remained effective for a long period in which it has been applied at large scale in an environment conducive to the pathogen. Effector: secreted pathogen protein that manipulates host cell functions. Haustorium: specialized organ formed by most biotrophic (pathogenic) fungi and oomycetes in a living plant cell for nutrient absorption and metabolism. Heterologous pathogen: pathogen species that is unadapted or maladapted to a particular (nonhost) plant species. Host specificity: the fact that a pathogen species is able to establish basic compatibility with only one or a few plant species. Host status: status of a plant being a suitable host to a particular pathogen species. If not, the plant is a marginal host or a nonhost. MAMP: microbe-associated molecular pattern; a molecular sequence or structure in any pathogen-derived molecule that is perceived via direct interaction with a host defence receptor (Mackey & McFall, 2006). Marginal host: plant species in which nearly all genotypes are fully resistant to a pathogen species, but a few odd genotypes show a level of susceptibility usually lower than that shown by the main host(s) of that pathogen species. MIMP: microbe-induced molecular pattern; a modification of a host-derived molecule that is induced by an intrinsic activity of a pathogen-derived effector and is perceived by a host defence receptor. Nonhost resistance: resistance occurring in all genotypes of a plant species to all genotypes of a pathogen species. Operative target: host target that, when manipulated by a pathogen effector, results in enhanced pathogen fitness. PAMP: pathogen-associated molecular pattern; a pathogen-specific molecular sequence or structure, often indispensable for the microbial lifestyle, that elicits an innate immune response on receptor-mediated perception (PAMPs are also called MAMPs or MIMPs). PAMP-triggered immunity (PTI): first line of active plant defence that relies on the recognition of pathogen-associated (or microbe-associated) molecular patterns (PAMPs/MAMPs) by pattern recognition receptors (PRRs).
T.C.M. was supported by the BIOEXPLOIT Integrated Project that resides under the 6th framework programme of the European Union. We thank Dr M. J. W. Jeuken for critical reading of the manuscript.