Recombination of standing variation in a multi-hybrid swarm drove adaptive radiation in a fungal pathogen and gave rise to two pandemic plant diseases

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 - Universidade Federal De Vicosa; VALENT, BARBARA - Kansas State University; FARMAN, MARK - University Of Kentucky

Submitted to: bioRxiv
Publication Type: Pre-print Publication
Publication Acceptance Date: 11/25/2021
Publication Date: 11/25/2021
Citation: Rahnama, M., Condon, B., Ascari, J., Dupuis, J., Del Ponte, E., Pedley, K.F., Martinez, S., Valent, B., Farman, M. 2021. Recombination of standing variation in a multi-hybrid swarm drove adaptive radiation in a fungal pathogen and gave rise to two pandemic plant diseases. bioRxiv. https://doi.org/10.1101/2021.11.24.469688.
DOI: https://doi.org/10.1101/2021.11.24.469688

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: Adaptive radiations fuel speciation and are characterized by rapid genetic diversification and expansion into new ecological niches. Historically, these processes were believed to be driven by selection on novel mutations but genomic analyses now indicate that standing variation and gene flow often have prominent roles. How “old” variation is combined, however, and its resulting genetic architecture within newly-adapted populations is not well understood. We reconstructed a recent radiation in the fungus, Pyricularia oryzae, that spawned a population pathogenic to eleven grass genera, and caused two new plant diseases: wheat blast - already a serious threat to global agriculture - and gray leaf spot of ryegrasses. We show that the new population evolved in a multi-hybrid swarm using only the standing variation that was present in seven individuals from five distinct, host-specialized lineages. Sexual and parasexual recombination within the swarm reassorted key host-specificity factors and generated more diversity in possibly just a few weeks than existing lineages had accumulated over hundreds to thousands of years. We suggest that the process was initiated by sexual opportunity arising when a fertile fungal strain was imported into Brazil on Urochloa introduced as forage for beef production; and we further contend that the host range expansion was largely fortuitous, with host selection playing little, if any, role in driving the process. Finally, we believe that our findings point to an overlooked role for happenstance in creating situations that allow organisms to skirt rules that would normally hold evolution in check.