Figure 1. The different interaction types and layers of plant resistance.

Figure 2. R protein classes and their cellular location. The predicted domains of R proteins which confer either race-specific or race nonspecific resistance are presented schematically: CC, coiled-coil domain; TIR, Toll and Interleukin 1 receptor-like motif; NB, nucleotide binding site; LRD, leucine-rich domain; LRR, leucine-rich repeat; NLS, nuclear localization signal; ECS, endocytosis signal; PEST, Pro-Glu-Ser-Ther-like sequence; WRKY, motif characteristic of some plant transcription factors; 1, 2, 3, 4 – novel domains that lack significant homology to known proteins; 5, domain with homology to a B-lectin ; 6, structure with a weak similarity to a PAN domain; 7, structure with homology to epidermal growth factor (EGF)-like domain; Cf-2, Cf-4 and Cf-5 confer resistance to Cladosporium fulvum races expressing, respectively, Avr2, Avr4 and Avr5; L6 flax rust resistance 6; Mla10, resistance to Blumeria graminis f.sp. hordei expressing Avra10; RPM1, resistance to P. syringae pv. maculicola expressing AvrRpm1 or AvrB; RPP5, resistance to Hyaloperonospora parasitica expressing ATR5. Further details of all other named R protein are given in Table 2. The two Ve proteins differ slightly in protein structure. Ve1 contains a putative CC domain but no PEST sequence in the C terminus, whereas Ve2 lacks the CC domain at the N terminus but contains a C-terminal PEST sequence. The MLO protein has not been included in this figure because the absence/reduced levels of this protein is thought to confer resistance. Adapted from Hammond-Kosack KE and Parker JE (2003) Deciphering plant–pathogen communication: Fresh perspectives for molecular resistance breeding. Current Opinions in Biotechnology 14: 177–193. Reproduced by permission of Elsevier.

Figure 3. R proteins and defence activation (a) Tomato Pto is a polymorphic serine-threonine kinase. Pto directly binds the unrelated bacterial effector proteins AvrPto and AvrB. Both effectors are delivered to the interior of the plant cell by the type III secretion system (TTSS) (blue syringe). Defence activation by Pto requires the NB-LRR protein Prf. The N-terminus of the monomorphic Prf protein binds to Pto to form a molecular complex (right). Both the AvrPto and AvrB effector proteins contribute to virulence in pto mutant genotypes (left). Adapted from Jones and Dangl (2006) The plant immune system. Nature 444: 323–329. Reproduced by permission of Nature Publishing Group. (b) Arabidopsis RPM1 is a plasma membrane tethered NB-LRR protein. The bacterial effectors AvrB and AvrRpm1 are delivered to the plant cell cytoplasm by the TTSS, then modified by eukaryotic-specific acetylation and as a consequence targeted to the plasma membrane. The biochemical functions of AvrB and AvrRpm1 are unknown. Both target RIN4, which interacts with the cytoplasmically localized N-terminal portion of NDR1. RIN4 becomes phosphorylated (+P) and activates RPM1 (right). In the absence of RPM1, both effectors act on RIN4 and other host targets, which contribute to virulence (left). The brown ovoids in this panel represent as yet unknown proteins. Adapted from Jones and Dangl (2006) The plant immune system. Nature 444: 323–329. Reproduced by permission of Nature Publishing Group. (c) Barley Mla10 is an NB-LRR protein, which resides in both the host cell cytoplasm and the nucleus. The powdery mildew avirulence protein AVRa10 is delivered into the inside of the plant cell either via the haustorium and the extracellular haustoria matrix (ECM) or directly from fungal hyphae. In the presence of AVRa10, Mla10 protein in the nucleus interacts with specific transcription factors, WRKY1/2. The identified WRKY proteins act as repressors of MAMP-triggered basal defence. Neither AVRa10 nor Mla10 possess known nuclear localization signals. It is unknown whether recognition of the presence of AVRa10 first occurs in the plant cell cytoplasm or the nucleus (right). How AVRa10 contributes to mildew virulence is also unknown (left). This figure is drawn from data published by Shen et al. (2007) Nuclear activity of MLA immune receptors links isolate-specific and basal disease-resistance responses. Science 315: 1098–1103, as well as from unpublished data. (d) The receptor-like R protein Cf-4 in tomato activates defences to C. fulvum races producing the extracellular effector Avr4. Avr4 binds fungal chitin and protects C. fulvum hyphae from degradation by extracellular plant chitinases. Tomato Cf-4 either through indirect or direct recognition of Avr4 activates plant defences. Defence activation by Cf-4 and some other Cf proteins requires the NB-LRR protein NRC1. (e) Recessive resistance to potyviruses controlled by mutant alleles of an eukaryotic translation initiation factor 4e (eIF4E). Initiation of translation in plants (and other eukaryotes) uses a multi-protein complex comprising of initiation factors 3, 4A, 4B, 4E, 4G, poly(A)-binding proteins (PABPs), 40S ribosomal subunit and several other minor components. An interaction between the mRNA cap structure (m⁷GpppG) and eIF4E is required for efficient translation. Potyviruses produce a small protein called VPg, which is covalently attached to the 5′-end of their RNA genomes and is likely to play a role similar to the mRNA cap structure during translation initiation (left). Some naturally occurring structural variants of eIF4E confer resistance to potyviruses. This is thought to be caused by their inability to bind potyviral VPg and recruit potyviral RNA into the translation initiation complex (right).

Figure 4. Some possible mechanisms of R gene evolution. Novel R alleles can be generated by several different mechanisms. However, the frequency of their occurrence depends upon whether the plant species is maintained as an outbreeding (cross-pollinating) population (A) or an inbreeding (self-pollinating) population (B and C). The evolution of resistance in plants appears to occur primarily at the single-gene level so that novel specificities arising by way of intergenic recombination between similar genes (B1) are rare. The variant R alleles eventually selected encode proteins with increased effectiveness or confer a novel recognition capacity. The intergenic regions are shown in light blue. The genes highlighted by either a bracket or a double headed arrow represent different recombination products.

Figure 5. Plant disease control using R genes sequences. Designing plant genotypes based on information from pathogen avirulence (effector) genes. R genes imposing a high penalty to the pathogen for adaptation are likely to be durable.