Traditional plant breeders have relied on crosses between cultivars for the introgression of R-gene into susceptible crops. The response resulting from an incompatible interaction between a plant carrying a resistance protein and an avirulence gene product carried by the pathogen was described by Flor (1971) in his gene-for-gene model. In this model, Flor hypothesized that the interaction between a plant that possesses a resistance factor and a pathogen that has a cognate avirulence (Avr) factor would result in a resistance response. If the plant does not possess the R-gene or if the pathogens do not possess the Avr factor, the infection will prevail (Flor, 1971); this model fits with a receptor/ligand model. One important characteristic of poplar is that different poplar species can also be crossed to generate fertile F1 hybrids. This feature greatly increases gene flow in these obligate outcrossers, allowing new combinations of R-gene alleles and enhancing the potential of breeding for resistance (Bradshaw, 1996).
Although known Avrs are generally small molecules and R-proteins have a LRR domain believed to be involved in protein–protein interactions, only a few direct R/AVR interactions have been reported (Jia et al., 2000; Deslandes et al., 2003; Ueda et al., 2006), including Flor’s original flax-rust (or Melampsora lini/flax) model pathosystem (Dodds et al., 2006). A refinement to Flor’s hypothesis was suggested in which the role of the NB-LRR protein would be to guard or monitor the status of a host protein that is the target of an AVR. This refined model was initially used to describe the Prf/Pto/AvrPto interaction (Van der Biezen & Jones, 1998) and was later coined the guard model (Dangl & Jones, 2001). However, this model is also not perfect and another variant has emerged: the decoy model. In this new model, the plant protein targeted by the pathogen effector would have no function in host defence but would mimic a plant defence component (van der Hoorn & Kamoun, 2008). A good example of this would be Pto mimicking a defence component (such as the kinase domain of FLS2) to interact with AvrPto; and that this interaction is monitored by Prf (a NB-LRR), which subsequently triggers defence signalling (Xiang et al., 2008).
Regardless of these hypotheses, R-proteins remain at the centre stage of how plants perceive the pathogen. Most identified plant R-proteins belong to the large group of NB-LRR proteins in which NB is a nucleotide-binding site that is required for ATP binding and hydrolysis (Tameling et al., 2002) and LRR stands for leucine-rich repeat. NB-LRR can be further separated into two distinct groups based on their N-termini (Martin et al., 2003; Belkhadir et al., 2004). Group one includes the toll-interleukin receptor domain (TIR) and the second group has an N-terminal coiled-coil domain (CC). The NB domain also contains motifs that are specific to TNL and CNL (Meyers et al., 2003). A total of 51 CC-NB-LRRs (CNL) and 93 TIR-NB-LRRs (TNL) were found in the genome of A. thaliana ecotype Columbia (Meyers et al., 2003) (Fig. 1). The TIR resistance pathway is mediated by the EDS1/PAD4/SAG101 (enhanced disease susceptibility 1/phytoalexin-deficient 4/senescence-associated genes 101) complexes. EDS1 forms distinct cytosolic and nuclear protein complexes with PAD4 and SAG101 (Feys et al., 2001, 2005). The CC pathway signals through NDR1 (nonrace-specific disease resistance 1), which localizes to the plasma membrane via a C-terminal glycosylphosphatidyl-inositol (GPI) anchor (Century et al., 1997; Aarts et al., 1998; Coppinger et al., 2004). The CC and TIR pathways converge at the synthesis of the defence hormone SA (Fig. 1). Following biotrophic pathogen detection by R-protein, SA accumulates in the infected plants. This pathogen-triggered accumulation is dependent on ISOCHORISMATE SYNTHASE 2 (Wildermuth et al., 2001). SA is a sufficient and necessary signal for SAR (Vernooij et al., 1994), a broad-spectrum and long-lasting systemic resistance (Durrant & Dong, 2004) mediated by the positive regulator NPR1 (nonexpressor of PR-1 genes) (Dong, 2004). The SA-dependent defence signalling pathway is associated with interactions with biotrophic pathogens, while the ethylene and jasmonic acid pathways (ET and JA), which are generally thought to be antagonistic to the SA pathway, are associated with necrotrophic pathogens (Glazebrook, 2005). Recent evidence shows that this antagonistic effect would be mediated, at least in part, by the transcription factor EIN3 (ethylene insensitive 3), which can directly bind to the SID2 promoter (SA synthesis) (Chen et al., 2009). Consistent with these observations, the ein3eil1 double mutant accumulates very high concentrations of SA and the double mutant displays enhanced resistance to virulent and avirulent strains of Pseudomonas syringae (Chen et al., 2009). Recent results also show that the JA pathway can be made insensitive to SA suppression if the ET pathway is induced (Leon-Reyes et al., 2010). Despite a large and old consensus among the community regarding the antagonistic relationship and the selectivity of the JA and SA pathways for necrotrophic or biotrophic pathogens, it was recently demonstrated that the SA pathway can positively contribute to the response to necrotrophic pathogens and that the ET and the JA pathways can also positively contribute to the response to biotrophic pathogens (Tsuda et al., 2009). Using infection and genetic interaction, the Katagiri group made quantitative measurements using combinatorial mutants of the ET, JA and SA pathways to identify the role of the wild-type genes rather than to analyse the effect of the mutant phenotypes (Tsuda et al., 2009). There is now accumulating evidence that, upon activation, R-proteins can go the nucleus themselves (Burch-Smith et al., 2007; Shen et al., 2007; Wirthmueller et al., 2007; Cheng et al., 2009) and the nucleocytoplasmic shuttling of the defence components is highly reminiscent of NF-κB nuclear import (Wiermer et al., 2010).
Figure 1. Main actors of the R-protein pathway in Arabidopsis and their homologues in poplar. NDR1, nonrace-specific disease resistance 1; NPR1, nonexpressor of PR-1 genes; EDS1, enhanced disease susceptibility 1; SA, salicylic acid; PAD4, phytoalexin-deficient 4; BNL, BED-NB-LRR; CNL, CC-NB-LRR; TNL, TIR-NB-LRR.
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