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Stepwise Arms Race Between AvrPik and Pik Alleles in the Rice Blast Pathosystem

¹National Key Laboratory for Conservation and Utilization of Subtropical Agrobioresurces and Guangdong Provincial Key Laboratory for Microbe Signals and Crop Disease Control, South China Agricultural University, Guangzhou, 510642, China; ²Hainan Key Laboratory for Monitoring and Control of Tropical Agricultural Pests, Environment and Plant Protection Institute, Chinese Academy of Tropical Agricultural Sciences, Haikou, Hainan 571101, China

A stepwise mutation that occurred in both pathogens and their respective hosts has played a seminal role in the co-evolutionary arms race evolution in diverse pathosystems. The process driven by rice blast AvrPik and Pik alleles was investigated through population genetic and evolutionary approaches. The genetic diversity of the non-signal domain of AvrPik was higher than that in its signal peptide domain. Positive selection for particular AvrPik alleles in the northeastern region of China was stronger than in the south. The perfect relationship between the functional lineages and AvrPik allele-specific pathotypes was established by ruling out the nonfunctional lineages derived from additional copies. Only four alleles conditioning stepwise pathotypes were detected in natural populations, which were likely created by only one evolutionary pathway with three recognizable mutation steps. Two non-stepwise pathotypes were determined by two blocks in a network constructed by all 16 possible alleles, indicating that a natural evolution process can be artificially changed by a combination of specific single-nucleotide polymorphisms. Assuming that AvrPik evolution has been largely driven by host selection, the co-evolutionary stepwise relationships between AvrPik and Pik was established. The experimental validation of stepwise mutation is required for the development of sustainable management strategies against plant disease.