The emergence of the rice blast fungus (Pyricularia oryzae) coincides with the evolutionary divergence of rice

Abstract

Rice blast, caused by Pyricularia oryzae, is one of the most destructive diseases threatening global rice production. Reconstructing the evolutionary history of P. oryzae in the context of the well-documented history of rice dispersal provides a powerful framework for predicting the coevolutionary dynamics of crops and their pathogens. However, the absence of fossil evidence has precluded robust estimation of the pathogen's origin and evolutionary timescale. Here, we inferred genome-wide divergence times for P. oryzae using archaeological constraints derived from the emergence and spread of rice cultivation. Our analyses indicate that P. oryzae originated approximately 18,300 years ago, coincident with the divergence of Oryza sativa L. from its ancestral lineage rather than with rice domestication itself. Calibrating the evolutionary history of the pathogen against this host divergence further indicates that P. oryzae reached the Japanese archipelago 2,590 years ago based on nucleotide sequences and 3,030 years ago based on amino acid sequences, closely matching archaeological estimates for the arrival of rice agriculture in Japan. Contrary to the prevailing view that rice blast emerged with rice domestication approximately 10,000 years ago, our results place the origin of P. oryzae before domestication and link its subsequent spread to the expansion of cultivated rice. These findings redefine the evolutionary history of one of the world's most important crop pathogens and establish a temporal framework for understanding crop-pathogen coevolution over millennial timescales.