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

Lead Research Organisation: National Inst of Agricultural Botany
Department Name: Centre for Research

Abstract

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.

Technical Summary

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

Planned Impact

The impact of this proposal relates to the detailed understanding of the population structure of a major wheat pathogen, yellow rust. Project outputs will impact on wheat producers, plant breeders, regulatory and testing authorities, and pathogen surveillance projects. As yellow rust is a global disease, project outcomes will have national and far-reaching international impacts. In the UK, yellow rust control is reliant on a combination of resistance and fungicide use. The latter is under increasing pressure from withdrawal of actives, or tightening regulations on use. The importance of host plant resistance is therefore likely to increase, but it must be at a reasonably high level, and reliable. This project will increase, by several orders of magnitude, the ability of surveillance projects such as the UK Cereal Pathogen Virulence Survey, to detect and characterise damaging yellow rust variants at an early stage. Such information will have immediate impacts for growers, enabling them to change variety choice, or react in season with different fungicide programmes to counter epidemics. A detailed regional understanding of virulence structure will enhance the potential for diversification of varieties, where different resistances could be deployed on a landscape scale to decrease inoculum pressure and preserve the durability of resistance traits. Plant breeders will benefit from earlier and more detailed knowledge of pathogen population structure so that alternative resistance sources can be incorporated into breeding material, and sudden "breakdown" of resistance can be avoided during commercialisation. Testing and regulatory authorities will benefit by having improved information on pathotypes for use in testing programmes. Surveillance projects, such as UKCPVS, would change approaches to use the new technologies devised in the project, becoming more efficient and of greater value to end users. The project outputs will be tested immediately in this survey work at the end of the grant, and could be implemented in routine work within a further three year period. Plant breeders would also benefit in the short term as more comprehensive and in depth undertsanding of yellow rust population structures would be immediately available.

Though targeted at yellow rust in this project, field pathogenomics could be applied to many other plant pathogens which have variable pathotypes interacting with host resistance. Virulence monitoring in cereal rusts is an international effort, with research in the US, China, Australia, Africa and Europe, and the techniques and sampling strategies investigated in the current proposal would be of value wherever cereal rusts occur.

Publications

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Description Initial data on genotypic and phenotypic descriptors of outbreaks of yellow rust in wheat fields. Intensive sampling of yellow rust in wheat fields has revealed new information on genotypic and pathotypic diversity which will ultimately feed into practical sampling strategies for routine surveillance work. Highly complex populations of yellow rust were recorded in small (<0.3 ha) areas of susceptile wheat cultivars in all years of monitoring. Pathotype testing revealed multiple pathotypes within an area, with some temporal changes occurring as well. Different pathotypes were present on the same leaf in some cases. This has implications both for the timing of sampling and its extent within the United Kingdom Cereal Pathogen Virulence Survey project. samplers, who mat be farmers, agronomists/advisors, breeders and researchers, are encouraged to send at least two samples from an infected field over the season, and to include leaves from different foci of infection. While this generates many more samples than can be tested pathotypically, it provides an essential resource for genotyping. Genotyping has now been included for the first time (2019) in the UKCPVS project and is aimed at identifying genotypic variants which may indicate new pathotypes, and thus be targeted for priority testing. Results will be reported in the AHDB UKCPVS 2020 report. In addition, a "short rotation" DTP student has been investigating gentotyping using the "MinION" Oxford Nanopore platform, to investigate closely related pathotypes, and this may lead to a PhD project in the autumn. Collaboration with JIC (lead partner in Pathogenomics) continues within the UKCPVS, and in an H2020 project "Rustwatch" coordinated by Aarhuis University which builds further on outcomes of the original project.
Exploitation Route Eventual use in routine rust survey programmes. The initial steps have already been taken with UKCPVS in 2019, and further research is underway in an H2020 project and the approach may be widely adopted in Europe
Sectors Agriculture, Food and Drink

 
Description The findings have been used to ecourage improved sampling of yellow rust in the field for routine surveillance by industry stakeholders. Improed sampling leads to more precise information, for use by plant breeders in screening material, and for growers in understanding variety risk from yellow rust, and avoiding economic losses
First Year Of Impact 2019
Sector Agriculture, Food and Drink
Impact Types Economic

 
Title practical application 
Description The outcomes of field pathogenomics have now been incorporated into a new rust surveillance project in the UK, commencing April 2019 
Type Of Material Improvements to research infrastructure 
Year Produced 2018 
Provided To Others? Yes  
Impact More rapid identification of novel and potentially damaging yellow rust races 
 
Description h2020 Rustwatch (multiple partners in EU) 
Organisation Aarhus University
Country Denmark 
Sector Academic/University 
PI Contribution provision of yellow rust isolates for genotyping, testing of wide germplams resources in wheat, integrated control of yellow rust in wheat, provision of pathotype data or Gloal Rust reference Centre databases, grower and researcher workshops
Collaborator Contribution A similar set of activities to the above is carried out by all partneers, with some focusing on brown rust and stem rust
Impact Outputs re limited as yet, but pathotype data hasbeen provided to the central rust database and to date a single trial in UK has been complted screening a panel of European varieties and landraces, and a single trial on alternative control products. Outputs have been summarised at a number of workshops and agronomist conferences, and at the UKCPVS stakeholder meeting (summary level)
Start Year 2018