Genome evolution of a pandemic clonal lineage of the wheat blast fungus

Magnaporthe oryzae pathotype Triticum, the causal agent of wheat blast, is a fungus with devastating implications for the wheat crop. The International Maize and Wheat Improvement Center (CIMMYT) has described wheat blast in a Priority Brief as a "deadly and baffling foe". "Global monitoring of disease appearances, movement, and evolution" and "Genetic and epidemiological research" are two of the four priorities listed by CIMMYT.

The disease was originally detected in Brazilian wheat fields in 1985 and quickly spread over most of the South American continent in the following years. In 2016, the first wheat blast pandemic beyond South America hit Bangladesh and affected more than 15 000 hectares of fields, causing huge losses in wheat yield. Less than two years later, Zambian farmers were also struck by the wheat blast pandemic, a first for the African continent. Until recently, there has been no confirmation if this pandemic was caused by the same pathogen which had travelled between the continents or if they were the result of other Magnaporthe oryzae pathogen strains shifting their host species to wheat.

To answer this question, our teams at The Sainsbury Laboratory, University College London, and several collaborators throughout the world processed and analysed samples of pandemic wheat blast from the three continents through the OpenWheatBlast open science initiative. Molecular analyses linked the pathogen populations in Zambia and Bangladesh to a single pandemic clone called B71 that originated in South America.

Our preliminary analyses revealed that this pandemic clone of the wheat blast fungus is evolving. This project will continue and expand wheat blast genomic surveillance in Africa over the coming years and generate genomics-informed knowledge to guide the response to the pandemic. More specifically, we will rapidly identify the emergence of new variants, determine the precise nature of the underpinning genetic changes, and evaluate the impact of these variants on disease severity.

A better understanding of how the pandemic wheat blast fungus evolves should inform knowledge-guided disease management and breeding wheat plants that are better able to resist diseases. Our long-term aim is to fully integrate genomic surveillance in the response to plant health emergencies to improve our capacity to protect plants against crop diseases.

Our team was commissioned by CIMMYT to investigate the genetic identity of the African wheat blast pathogen that was first reported in September 2020. We rapidly processed samples from Zambia and released them to the community as open science resources through the OpenWheatBlast initiative (samples received on 21 January 2021; first dataset published on 15 March 2021). Analyses of the genetic data by our teams and others linked the pathogen populations in South America, South East Asia and Zambia to a single pandemic clone of the fungus Magnaporthe oryzae, we called B71. All the samples from Zambia collected from 2018 to 2020 were the same clone indicating that there was probably only a single introduction to the country.

The aim of this project is to map the genome evolution of the pandemic B71 clonal lineage of the wheat blast fungus and determine the evolutionary potential of newly emerged variants. Our approach combines genomics surveillance of field isolates with laboratory experiments that will test specific hypotheses about the impact of sequence and structural variation on the fungus biology and pathology. The central hypothesis of the proposed research, based on preliminary data, is that the B71 clonal lineage of the wheat blast fungus undergoes genetic changes that impact its capacity to cause disease and resist chemical control. We hypothesize that novel mutations and structural variants will impact virulence and other important traits that are relevant to disease management.

We aim to introduce the concept of Variants of Concern (VOC), popularised during the COVID19 pandemic, to plant pathology. At the completion of this study, we will have determined the extent to which VOC carry mutations that impact virulence and response to chemical control, and therefore affect disease epidemiology. We will generate a model on the evolutionary potential of the pathogen that should prove useful for guiding disease management and plant breeding strategie