Recent co-evolution of two pandemic plant diseases in a multi-hybrid swarm

Authors: RAHNAMA, MOSTAFA - University Of Kentucky; CONDON, BRADFORD - University Of Kentucky; ASCARI, JOAO - Universidade Federal De Vicosa; DUPUIS, JULIAN - University Of Kentucky; DEL PONTE, EMERSON - Universidade Federal De Vicosa; Pedley, Kerry; MARTINEZ, SEBASTIAN - Instituto Nacional De Investigacion Argropecuaria, Urugary; VALENT, BARBARA - Kansas State University; FARMAN, MARK - University Of Kentucky

Submitted to: Nature Ecology and Evolution
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 9/28/2023
Publication Date: 11/9/2023
Citation: Rahnama, M., Condon, B., Ascari, J. P., Dupuis, J. R., Del Ponte, E. M., Pedley, K. F., Martinez, S., Valent, B., and Farman, M. L. 2023. Recent co-evolution of two pandemic plant diseases in a multi-hybrid swarm. Nat. Ecol. Evol. 7:2055-2066.
DOI: https://doi.org/10.1038/s41559-023-02237-z

Interpretive Summary: Wheat blast (WB) is a devastating disease caused by the fungus Pyricularia oryzae (Magnaporthe oryzae) and can result in 100% crop losses. The disease was first reported in 1985 in Brazil and has since spread to surrounding countries. The disease was, until recently, restricted to South America. However, major outbreaks in Asia in 2016 and 2017, and the pathogen’s arrival in Africa have elevated wheat blast as a major concern for global agriculture, especially because the crop possesses very little natural resistance to the disease. We have reconstructed the evolution of wheat blast and a related disease, gray leaf spot, and show that the two pathogen populations co-evolved from sequential matings between different host-specialized forms of the fungus starting in the 1960s or 1970s. Subsequent genetic diversification of the initial population resulted in lineages of the pathogen with expanded host ranges. These findings of this work shed new light on population genetic processes driving new disease emergence and enhances the ability of plant pathologists and epidemiologists to combat wheat blast through scientifically-informed cultural management decisions, resistance breeding, and pathogen surveillance.

Technical Abstract: Most plant pathogens exhibit host specificity but when former barriers to infection break down, new diseases can rapidly emerge. For a number of fungal diseases, there is increasing evidence that hybridization plays a major role in driving host jumps. However, the relative contributions of existing variation versus new mutations in adapting to new host(s) is unclear. Here we reconstruct the evolutionary history of two recently emerged populations of the fungus Pyricularia oryzae that are responsible for two new plant diseases: wheat blast and grey leaf spot of ryegrasses. We provide evidence that wheat blast/grey leaf spot evolved through two distinct mating episodes: the first occurred ~60 years ago, when a fungal individual adapted to Eleusine mated with another individual from Urochloa. Then, about 10 years later, a single progeny from this cross underwent a series of matings with a small number of individuals from three additional host-specialized populations. These matings introduced non-functional alleles of two key host-specificity factors, whose recombination in a multi-hybrid swarm probably facilitated the host jump. We show that very few mutations have arisen since the founding event and a majority are private to individual isolates. Thus, adaptation to the wheat or Lolium hosts appears to have been instantaneous, and driven entirely by selection on repartitioned standing variation, with no obvious role for newly formed mutations.