Predicting durability of disease resistance genes based on assessment of the fitness function of avirulence genes

Durability of plant disease resistance genes may be predicted if the cost of pathogen adaptation to overcome resistance is understood. In the laboratory study, genomic copies of three Xanthomonas oryzae pv. oryzae (Xoo) avirulence (avr) genes, avrXa7, avrXa10 and avrxa5, and four of their homologs were mutagenized individually or in combination to study the roles of avr genes in pathogen aggressiveness. Compared to PXO86, all mutations except on avrXa10 caused shorter lesions on the susceptible cultivar, IR24. The contribution of each homolog to lesion length varied, with most contributing less than avrXa7. The functional, cosmid-borne copies of avrXa7 or avrxa5 only restored aggressiveness to strains with their respective mutations. Furthermore, mutations in avrXa7 were not complemented by cosmids carrying avrxa5, avrXa10 or other avr homologs. These data indicate that some, but not all, avr homologs contribute to pathogen aggressiveness and that the contributions are quantitatively different, with avrXa7 contributes the most. In addition, despite their sequence similarity, the aggressiveness functions of the avr genes are not interchangeable. In the field study, we evaluated the cost in pathogenic fitness (aggressiveness and persistence) associated with adaptation of Xoo to virulence on near-isogenic rice lines with single resistance genes (Xa7, Xa10 and Xa4) in two field sites endemic in the Philippines. Resistance genes Xa7 and Xa10 had not been deployed, whereas Xa4 had been used for over 25 years. Disease severity was assessed over three years (six cropping seasons) and was high on all lines except the line with Xa7. Adaptation to virulence on Xa7 was associated with a reduction in overall aggressiveness. The mutant phenotypes, including loss of avirulence function and reduced aggressiveness, of race 9c and 9b strains were associated with the 3′ termini of the avrXa7 alleles. Strains most aggressive to Xa7 (race 9a, 9c and 9d) were not detected after the second year, suggesting they were less persistent than less aggressive strains (race 9b). Based on the amounts of disease on lines with Xa7 and Xa10 and the cost in fitness to Xoo associated with adaptation to Xa7, we predict that Xa7 would be more durable than Xa10.