Direct protein interaction underlies gene-for-gene specificity and coevolution of the flax resistance genes and flax rust avirulence genes

Abstract

Plant resistance proteins (R proteins) recognize corresponding pathogen avirulence (Avr) proteins either indirectly through detection of changes in their host protein targets or through direct R-Avr protein interaction. Although indirect recognition imposes selection against Avr effector function, pathogen effector molecules recognized through direct interaction may overcome resistance through sequence diversification rather than loss of function. Here we show that the flax rust fungus AvrL567 genes, whose products are recognized by the L5, L6, and L7 R proteins of flax, are highly diverse, with 12 sequence variants identified from six rust strains. Seven AvrL567 variants derived from Avr alleles induce necrotic responses when expressed in flax plants containing corresponding resistance genes (R genes), whereas five variants from avr alleles do not. Differences in recognition specificity between AvrL567 variants and evidence for diversifying selection acting on these genes suggest they have been involved in a gene-specific arms race with the corresponding flax R genes. Yeast two-hybrid assays indicate that recognition is based on direct R-Avr protein interaction and recapitulate the interaction specificity observed in planta. Biochemical analysis of Escherichia coli-produced AvrL567 proteins shows that variants that escape recognition nevertheless maintain a conserved structure and stability, suggesting that the amino acid sequence differences directly affect the R-Avr protein interaction. We suggest that direct recognition associated with high genetic diversity at corresponding R and Avr gene loci represents an alternative outcome of plant-pathogen coevolution to indirect recognition associated with simple balanced polymorphisms for functional and nonfunctional R and Avr genes.avirulence protein ͉ resistance protein P lants resist disease through a variety of preformed and induced barriers to infection. Among these is a genetically determined pathogen recognition system controlled by host resistance genes (R genes). In this gene-for-gene resistance system, plant R genes confer resistance to pathogen strains carrying corresponding avirulence (Avr) genes (so-called because their presence prevents growth on resistant plants). The recognition event involving the products of the R and Avr genes triggers host defense responses, including a localized host cell death or hypersensitive response (HR) that limits the spread of the pathogen from the infection site. Most known plant resistance proteins (R proteins) contain nucleotide binding site (NBS) and leucine-rich repeat (LRR) domains, with the latter implicated in pathogen recognition (1). In contrast, Avr proteins are diverse, and many have pathogenicity effector functions that play important roles in enhancing infection (2). The antagonistic relationship between R and Avr genes results in coevolutionary conflict as selection favors evolution of resistance in plants and virulence in their pathogens.The Arabidopsis RPM1, RPS2, and RPS5 NBS-LRR-type R proteins confer r...

Third-party mutualists have contrasting effects on host invasion under the enemy-release and biotic-resistance hypotheses

“…If wild parsnips were to invade a habitat lacking the parsnip webworm, they would experience enemy release. Similar trait-matching systems are also found in feather lice and doves (Clayton et al 2003), red crossbills and lodgepole pine (Benkman et al 2003), the Japanese camellia and the camellia weevil (Toju and Sota 2005), and the gene-for-gene matching system between flax and flax rust (Dodds et al 2006). Trait matching can also underlie beneficial interactions.…”

“…In the most extreme cases, gene-for-gene interactions can determine whether or not two partners are able to interact (Dodds et al 2006;Yang et al 2010). By interacting with multiple partners via the same trait, plants serve as a link between above-and below-ground organisms.…”

Glycan moiety of flagellin inAcidovorax avenaeK1 prevents the recognition by rice that causes the induction of immune responses

“…1,2 The second layer immune system, termed effector-triggered immunity (ETI), is caused by recognition of effector proteins, which are injected into the host cell from bacteria cell through the Type III secretion system (T3SS). 3,4 By definition, PAPMs are conserved across a wide range of microbes, which may or may not be pathogenic. Because these molecules are essential for viability or lifestyle, microbes are less likely to evade host immunity through mutation or deletion of PAMPs, compared with virulence effectors.…”

Recognition and signal transduction in the expression of Phytophthora resistance in soybean [Glycine max (L) Merr]

“…Molecular evidence supporting this model has been shown only for four plant-pathogen interactions (Deslandes et al 2003;Dodds et al 2006;Scofield et al 1996;Tang et al 1996). Alternative guard hypothesis was put forward to explain the rareness of direct interactions between R and Avr proteins.…”

“…Despite the extensive efforts in validating this model, the available data imply that it is rather a rare case. Molecular evidence supporting this model has been obtained only from four plant-pathogen interactions (Deslandes et al, 2003;Dodds et al, 2006;Scofield et al, 1996;Tang et al, 1996). Accumulating data have indicated that multiple proteins participate in R gene-mediated disease resistance.…”