Using field pathogenomics to study wheat yellow rust dispersal and population dynamics at a national and international scale

Wheat yellow rust caused by the fungus Puccinia striiformis f. sp tritici is a substantial threat to wheat production worldwide and recently re-emerged as a major constraint on UK agriculture. Its importance to global food security is reflected by the significant contribution of wheat to the calorific and protein intake of human kind (approximately 20%). The devastating impact of this disease gives a deep sense of urgency to breeders, farmers and end users to improve surveillance.

To address this, we recently developed a novel approach called "field pathogenomics" for pathogen population surveillance. This method, based on new gene sequencing technology, allows us to acquire data directly from field samples of rust-infected wheat. By implementing this approach we found that the yellow rust population across the UK underwent a major shift in recent years. Genetic analyses revealed four distinct lineages that correlated to the phenotypic groups determined through traditional pathology-based virulence assays.

The overall aim of this project is to apply gene-sequencing technology to the surveillance of yellow rust and undertake comprehensive global population genetic analyses of this important plant pathogen. Currently, the assessment of genotypic diversity is not included within UK national surveillance activities for wheat rust. Our new approach enables the integration of high-resolution genotypic data into pathogen surveillance activities that is vital to improve our understanding of the genetic sub-structure within a population. The proposed research aims to: (1) Analyze the threat of potential exotic incursions of wheat yellow rust to the UK by mapping the global population structure, (2) exploit the rust genotype data (Obj. 1) to confirm outbreaks on particular wheat varieties and look for associations between pathogen genotypes and host pedigrees, (3) generate information on whether genotypic diversity shifts over time at a locality and whether early appearing rust genotypes are predictive of late season genotypes and (4) develop appropriate open-source tools to ensure all data generated herein is released into the public domain as soon as possible and in a format that is suitable for breeders, pathologists and the wider demographic. This project aims to equip the UK with the latest genomic tools, facilitate more efficient varietal development by breeders, and help reduce the environmental and economic costs associated with fungicide applications, all of which will have a positive impact on the overall competitiveness and sustainability of the UK arable industry. This will be achieved through collaboration with 13 rust pathology laboratories across 6 continents and industrial support from 6 breeding, agronomy and chemical companies and the HGCA.

Wheat yellow rust disease, caused by the fungus Puccinia striiformis f. sp tritici (PST), is a devastating disease that affects wheat production worldwide. This gives a deep sense of urgency to breeders and farmers to improve surveillance. To this aim, we developed a novel approach called "field pathogenomics" for pathogen population surveillance based on high-resolution RNA-seq data acquired directly from field samples of PST-infected wheat. Our preliminary study of 39 PST-infected field samples revealed only a single PST genotype within each lesion using the distribution of read counts for biallelic single nucleotide polymorphisms. In addition we also generated genome sequence data from historical PST isolates. None of the 2013 PST field isolates showed genetic similarity to the older UK population indicating that the 2013 population is likely an exotic population that appears to have displaced the previous population. Transcriptome data was also aligned to wheat sequences flanking a set of 18,162 wheat SNPs, and for each sample we could confirm the wheat variety recorded at the point of sample collection as the most likely variety.

The proposed research builds on this preliminary study to apply gene-sequencing technology to the surveillance of PST and undertake comprehensive global population genetic analyses of this important plant pathogen. The central hypothesis is that current pathology-based virulence tests only reflect a small proportion of the yellow rust genetic variation at the field level. We hypothesize that "Field pathogenomics" provides the means to gain a better understanding of the yellow rust population dynamics at the genotype level and hasten decision-making from farmers, breeders and agronomists regarding the best wheat varieties and resistances to deploy in the field. This is possible through collaboration with 13 rust pathology laboratories across 6 continents and industrial support from 6 breeding, agronomy and chemical companies and HGCA

PI Saunders will lead the impact plan that will be an agenda item at monthly project meetings with Co-I's. All Co-I's have excellent track records in communicating the outcomes of their research to a broad audience and sharing tools, resources and code in a free and open manner. The PI and Co-I's also are regularly invited to speak about their research at national/international meetings and at various other venues.

Beneficiaries include:

Those involved in wheat yellow rust surveillance such as the UK cereal pathogen virulence survey (funded by Fera and the HGCA). They will benefit from development of high-resolution genotyping methods that will be incorporated into the UKCPVS. During the project, information will also be relayed to the UKCPVS as soon as relevant and reported in the NIAB-TAG's quarterly journal (Landmark) to reach the > 3000 NIAB-TAG members including agronomists, breeders and farmers.

Researchers working with wheat yellow rust disease. All data will be made freely available where practical, at the earliest opportunity. The data will initially be hosted via a modified version of the TGAC http://opendata.tgac.ac.uk website to ensure rapid release under a creative commons license. Once submitted for publication all data will be deposited in public repositories and linked to via the project-specific website.

Farmers, breeders, agronomists and wheat variety testing authorities will benefit from the rapid means of confirming whether previously resistant wheat varieties have been broken by virulent races of the pathogen. Our research will also confirm outbreaks on particular wheat varieties and look for associations between pathogen genotypes and host pedigrees. Participation of four major UK wheat breeders (KWS, Limagrain, Syngenta, RAGT) as partners reflects the urgency of the problem. Understanding the underlying variation and how this affects resistance breeding is essential for the strategic planning required to produce high-yielding wheat varieties that will be resistant when deployed in 10 years (considering time between initial crossing and variety release). This may also lead directly to management decisions on how to effectively manage the threat of PST to UK wheat production. This audience will be reached through publications in the farming press. For instance, results from our preliminary study have already been reported in EDP24, the HGCA newsletter, NIAB-TAG bulletin, world-grain.com, Farmers Guardian, Agrii company newsletter, EADT24 and the Crop Production Magazine.
Population geneticists. Where possible new tools and data analysis pipelines generated herein will be integrated into the interactive Galaxy user interface to ensure they are accessible to the widest demographic, that includes bench biologists. All tools and pipelines once verified will be publically released without delay.

The general public will benefit from interactions with the PI and Co-I's, who have given talks to public audiences on a variety of issues such as plant biosecurity. They will specifically focus on further educating the public on genome science and pathogen dispersal in relation to plant pathogens and the crops they infect. They will give at least one talk to a public audience relating to this project, at least once per year.

The PDRA's, programmer and RA recruited for this project will benefit from improved skills, knowledge and experience gained from the research and wider training. This will contribute to their future economic activity in the public and/or private sectors. The innovative nature of the project ensures these individuals will likely develop unique skills that should prove highly attractive in the marketplace. This proposal also brings together an array of disciplines that will provide an exciting training ground for a cadre of excellent young scientists. This will contribute to the next generation of skilled crop scientists, with benefits beyond the immediate outcomes of this project.