Direct protein interaction underlies gene-for-gene specificity and coevolution of the flax resistance genes and flax rust avirulence genes.
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.
Dodds
Peter N
PN
Commonwealth Scientific and Industrial Research Organization Plant Industry, GPO Box 1600, Canberra ACT 2601, Australia. peter.dodds@csiro.au
Lawrence
Gregory J
GJ
Catanzariti
Ann-Maree
AM
Teh
Trazel
T
Wang
Ching-I A
CI
Ayliffe
Michael A
MA
Kobe
Bostjan
B
Ellis
Jeffrey G
JG
D000595:Amino Acid Sequence; D000596:Amino Acids / Q000235:genetics; D001665:Binding Sites / Q000235:genetics; D019143:Evolution, Molecular; D019597:Flax / Q000235:genetics*; D005658:Fungi / Q000235:genetics* / Q000472:pathogenicity; D017343:Genes, Plant / Q000235:genetics*; D008969:Molecular Sequence Data; D009154:Mutation / Q000235:genetics; D010935:Plant Diseases / Q000235:genetics* / Q000382:microbiology*; D010940:Plant Proteins / Q000737:chemistry; D011485:Protein Binding; D012641:Selection, Genetic; D013045:Species Specificity; D014774:Virulence / Q000235:genetics
D000596:Amino Acids; D010940:Plant Proteins