Host plant resistance has been used extensively for disease control in many crop species; however, the resistance conferred by many sources is not durable as a result of rapid changes in the pathogen. Although many resistance genes have been identified in plant germplasm, there is no easy way to predict the quality or durability of these resistance genes. In this review, we revisit the hypothesis that resistance genes imposing a high penalty to the pathogen for adaptation will likely be durable. By elucidating the molecular changes involved in pathogen adaptation and the associated fitness cost, a proactive approach may be developed to predict the durability of resistance genes available for deployment.

Candidate genes involved in both recognition (resistance gene analogs [RGAs]) and general plant defense (putative defense response [DR]) were used as molecular markers to test for association with resistance in rice to blast, bacterial blight (BB), sheath blight, and brown plant-hopper (BPH). The 118 marker loci were either polymerase chain reaction-based RGA markers or restriction fragment length polymorphism (RFLP) markers that included RGAs or putative DR genes from rice, barley, and maize. The markers were placed on an existing RFLP map generated from a mapping population of 116 doubled haploid (DH) lines derived from a cross between an improved indica rice cultivar, IR64, and a traditional japonica cultivar, Azucena. Most of the RGAs and DR genes detected a single locus with variable copy number and mapped on different chromosomes. Clusters of RGAs were observed, most notably on chromosome 11 where many known blast and BB resistance genes and quantitative trait loci (QTL) for blast, BB, sheath blight, and BPH were located. Major resistance genes and QTL for blast and BB resistance located on different chromosomes were associated with several candidate genes. Six putative QTL for BB were located on chromosomes 2, 3, 5, 7, and 8 and nine QTL for BPH resistance were located to chromosomes 3, 4, 6, 11, and 12. The alleles of QTL for BPH resistance were mostly from IR64 and each explained between 11.3 and 20.6% of the phenotypic variance. The alleles for BB resistance were only from the Azucena parent and each explained at least 8.4% of the variation. Several candidate RGA and DR gene markers were associated with QTL from the pathogens and pest. Several RGAs were mapped to BB QTL. Dihydrofolate reductase thymidylate synthase co-localized with two BPH QTL associated with plant response to feeding and also to blast QTL. Blast QTL also were associated with aldose reductase, oxalate oxidase, JAMyb (a jasmonic acid-induced Myb transcription factor), and peroxidase markers. The frame map provides reference points to select candidate genes for cosegregation analysis using other mapping populations, isogenic lines, and mutants.

Durability of plant disease resistance (R) genes may be predicted if the cost of pathogen adaptation to overcome resistance is understood. Adaptation of the bacterial blight pathogen, Xanthomonas oryzae pv. oryzae (Xoo), to virulence in rice is the result of the loss of pathogen avirulence gene function, but little is known about its effect on aggressiveness under field conditions. We evaluated the cost in pathogenic fitness (aggressiveness and persistence) associated with adaptation of Xoo to virulence on near-isogenic rice lines with single R genes (Xa7, Xa10, and Xa4) at two field sites endemic for bacterial blight. Disease severity was high in all 3 years on all lines except the line with Xa7. Of two Xoo lineages (groups of strains inferred to be clonally related based on DNA fingerprinting) detected, one, lineage C, dominated the pathogen population at both sites. All Xoo strains were virulent to Xa4, whereas only lineage C strains were virulent to Xa10. Only a few strains of lineage C were virulent to Xa7. Adaptation to virulence on Xa7 occurred through at least four different pathways and was associated with a reduction in aggressiveness. Loss of avirulence and reduced aggressiveness were associated with mutations at the 3 terminus of the avrXa7 allele. Strains most aggressive to Xa7 were not detected after the second year, suggesting they were less persistent than less aggressive strains. These experiments support the prediction that Xa7 would be a durable R gene because of a fitness penalty in Xoo associated with adaptation to Xa7.