A Re-evaluation of phylogenomic data reveals that current understanding in wheat blast population biology and epidemiology is obfuscated by oversights in population sampling

Abstract

Wheat blast, caused by the Triticum lineage of Pyricularia oryzae (PoT), is a serious disease that first emerged in Brazil and quickly spread to neighboring countries. The recent appearance of this disease in Bangladesh and Zambia highlights a need to understand the population biology and epidemiology of the disease so as to mitigate pandemic outbreaks. Current knowledge in these areas is largely based on analyses of wheat blast isolates collected in Brazil, and their comparison with isolates from non-wheat, endemic grasses. Those studies concluded that wheat blast is caused by a highly diverse P. oryzae population that lacks host specificity and, as a result, undergoes extensive gene flow with populations infecting non-wheat hosts. Additionally, based on genetic similarity between wheat blast and isolates infecting Urochloa species, it was proposed that the disease originally emerged via a host jump from this grass, and the widespread use of Urochloa as a pasture grass likely plays a central role in wheat blast epidemiology. Inconsistencies with earlier phylogenetic studies prompted us to re-analyze the Brazilian data in the context of a comprehensive, global, phylogenomic dataset. We now show that the seminal studies failed to sample the P. oryzae populations normally found on endemic grasses and, instead, repeatedly sampled PoT and P. oryzae Lolium (PoL) members that happened to be present in these hosts. The resulting lack of accurate and representative information about the grass-infecting populations in Brazil means that current conclusions about wheat blasts evolution, population biology and epidemiology are unsubstantiated and could be equivocal.