Yellowhammer: A multi-locus strategy for durable yellow rust resistance in wheat, in the face of a rapidly changing pathogen landscape

Wheat is the UK's major food crop. A major constraint on wheat production is the disease yellow rust (YR), caused by the fungus Puccinia striiformis f.sp. tritici (Pst), with yield losses up to 50% in untreated crops. The two major control measures for this disease, used in combination, are use of resistant varieties and application of fungicides. Fungicide application is effective but expensive, limited by weather conditions and increasingly restricted in use due to environmental concerns. Host (i.e. wheat) resistance can also be very effective, with several known resistance genes conferring immunity to known races of Pst. However, populations of the pathogen regularly change and resistance genes suddenly become ineffective when the pathogen mutates.

In Europe, there was a recent rapid incursion of an exotic Pst population, which is much more diverse than the established population it has displaced. As a result, there have been dramatic and ongoing changes in the patterns of YR resistance in commercial wheat varieties. In 2016 alone, seven varieties on the UK wheat Recommended List had their resistance ratings substantially reduced, with significant cost impact on growers. Breeding improved wheat varieties with effective, long-lasting YR resistance to withstand current and future incursions is now a top priority for northern European (NE) wheat breeders.

In Yellowhammer, we will employ a strategy based on detecting and utilizing multiple race non-specific adult plant resistance (APR) genes, for long-term genetic control of the disease. These genes usually confer partial resistance, are characterized by reduced and slower pathogen growth, and can be 'stacked' with each other or with 'major" genes in the same plant to provide effective long-lasting resistance. We previously identified several APR genes - but finding the most effective combinations is challenging as different genes interact with each other in complex ways. To address this challenge, we are collaborating with seven NE breeding companies and the UK's Agriculture and Horticulture Development Board to develop experimental wheat populations based on elite European varieties, but which differ in the combinations of YR APR genes they carry. We will use these to:

1. Identify the most effective combinations of APR genes, and the times of the season they become effective, in field tests at twelve sites in NE over four years. We will investigate what is the most effective combination of strong and weak APR genes to achieve YR resistance in wheat. We will also determine the effectiveness of APR genes in hybrid wheat and any side-effects APR genes have on grain yield.

2. Determine, using 'microphenotyping', the timing and location of action in the plant of different APR genes involved in the pathogen-host interaction, helping us select functionally complementary APR genes to combine.

3. Identify which wheat genes and genetic pathways are switched on or off in response to the pathogen in the presence of different APR gene combinations in order to understand how to best assemble APR gene combinations with complementary molecular genetic mechanisms of resistance.

We will also conduct field pathology trials of newly available populations and varieties to identify new APR genes.

The results will allow us to determine the best combinations of resistance alleles to stack, and provide new genetic markers to aid the process. Results will be validated in active commercial breeding material and will immediately be translatable into the breeding programs of our commercial partners, enabling them to breed more durably resistant wheat varieties equipped to resist the current Pst population and potential future incursions. This will improve UK arable production and food security, and reduce environmental harm, as farmers benefit from having access to more consistently performing, longer-lasting varieties with reduced fungicide requirements.

In collaboration with the UK-Northern European (NE) wheat breeding industry, we will develop tools and knowledge to enable breeding of effective long-lasting yellow rust (YR) resistant wheat varieties, via stacking of complementary adult plant resistance (APR) loci.

We previously detected and validated several APR loci in NE germplasm via genome-wide association scans (GWAS). In this project we will pursue novel resistance sources by field testing several newly-created bi-parental mapping populations for YR resistance. However, the main aim of Yellowhammer is to investigate the resistance effects of combinations of the most effective validated resistance alleles using near-isogenic lines (NILs) for different allelic combinations, along with a bespoke GWAS panel. Resistance will be quantified in multi-year multi-site field trials across NE, testing the hypothesis that combining weak APR loci with one strong APR locus is the most effective approach to achieve YR resistance. Resistance alleles will also be tested in heterozygous state, for application to hybrid breeding programs, and pleiotropic effects on yield investigated by meta-analysis of breeder yield trials.

We will identify functionally complementary APR loci to combine using microphenotyping to examine the mechanism, within-plant location and timing of action of different APR loci. Similarly, we will test the hypothesis that the most effective resistance is achieved by combining APR loci which achieve resistance through varied genetic pathways, by conducting a differential gene expression analysis of the response of +/- NIL pairs (in a +/- background of other resistance alleles) to pathogen inoculation. The transcriptome data will enable development of new tightly-linked markers for use in breeding varieties with stacked resistance alleles.

Synthesis of all data sets will determine the best allelic combinations for durable YR resistance, with project results validated in active breeding programs.

Wheat is the UK's major crop, with an annual grain yield of 14m tonnes. Yellow rust (YR) resistance is a key wheat breeding priority, and has become increasingly critical due to exotic YR pathogen incursions, with an associated loss of wheat resistance. In close collaboration between NIAB and 8 industrial partners, this project will develop new tools and knowledge to help breeders deliver more resilient varieties equipped to resist existing and potential new YR races. The project has benefits at all stages of the agricultural supply chain, from breeders and farmers, to food processors and the general public, through increased food security and reduced environmental impact. In this way, Yellowhammer addresses BBSRC's key strategic priority of 'Sustainably enhancing agricultural production'.

1. Private sector wheat breeding (short to medium term impact)

Our industrial wheat breeding partners will gain significant benefits via immediate access to genetic markers, knowledge and resources, which they will implement in their current breeding programmes within the project duration. Impact will be maintained in the medium term, as the germplasm advanced within the project duration is released and marketed for sale, and via continued use of the project outputs in ongoing varietal development.

2. Farmers, agriculture and supply chain (medium to long term impact)

Development of new wheat varieties with improved YR resistance will have significant impact on farmers: the rapidly changing pathogen population has recently resulted in dramatic host resistance changes, with 7 UK wheat Recommended List (RL) varieties in 2016 having ratings reduced by more than two points (on a 9 point scale). This would have significant impact on growers: failure to adapt to this change in-season by a grower would have resulted in losses of >£100/ha. Furthermore, use of resistant varieties helps reduce spraying throughout the season, enabling growers to plan fungicide regimes around the occurrence of other diseases, with YR largely controlled by varietal resistance. This gives an immediate financial benefit to farmers who could see fungicide spending reduce from £120/ha for a more susceptible variety, to £80/ha when using a more robust variety. Improvement in varietal resilience will result in a longer lifetime of productive use for varieties on farm and hence greater stability of preferred variety availability to the supply chain, e.g. end users such as millers and bakers.

3. Wider UK public, policy makers and environment (medium to long term impact)

This project will increase food security by reducing the potential for substantial crop losses when resistances are lost. Reduced fungicide use by growers will reduce the environmental impact of wheat production, via lower carbon emissions, less environmental damage and less polluted water supplies. Project outcomes will help inform future government policy making processes on food security and biosciences.

4. UK biosciences (short to medium term impact)

At the interface between crop research and its practical translation, this project provides a model for effective integration of public and industrial resources for the benefit of UK translational research. This integrated model will help raise the international profile and impact of UK biosciences, as well as providing the PDRA and technician with training in multiple academic and industrial sectors. Specifically, this project will provide greater scientific understanding of the mechanisms and genetic control of YR resistance, by synthesizing results from the field, microphenotyping and genetic expression analyses for a specific set of germplasm with characterized resistance alleles. Such knowledge has worldwide applicability to the control of rust disease, especially in less developed parts of the world with a large wheat industry, e.g. South Asia, where fungicide treatments are not affordable, and crop losses to YR can be catastrophic.