Decoding the molecular mechanisms driving host adaptation of yellow rust on cereal crops and grasses

Project Information

DeMMYR

Grant agreement ID: 715638

DOI

10.3030/715638

Project closed

EC signature date 17 October 2016

Start date 1 March 2017

End date 28 February 2023

Funded under

• EXCELLENT SCIENCE - European Research Council (ERC)

Total cost

€ 1 714 779,00

EU contribution

€ 1 714 779,00

Coordinated by

JOHN INNES CENTRE
United Kingdom

Periodic Reporting for period 4 - DeMMYR (Decoding the molecular mechanisms driving host adaptation of yellow rust on cereal crops and grasses)

Reporting period: 2021-09-01 to 2023-02-28

Summary of the context and overall objectives of the project

Yellow rust (YR) is a major disease of cereal crops and grasses worldwide, causing significant losses to the global wheat harvest each year. Wheat is an important food staple and is grown on more land area than any other food crop, contributing over 20 percent of the calorific and protein intake for humankind. YR frequently causes high yield losses, even in countries where resistant wheat varieties and/or fungicides are used. Furthermore, in the past two decades, new, more aggressive, YR strains that are adapted to warmer temperatures and are able to infect previously long-standing resistant wheat varieties have caused widespread epidemics. Therefore, it is imperative that we find new ways to protect this vital food crop from YR infection. The long-term aim of this research was to develop new varieties of wheat with enhanced resistance to YR. To do this, it is essential to understand host specificity - the ability of the pathogen to specialize on particular grass hosts, coupled with the ability of the host to resist infection by different strains of YR. To achieve this, this project brought together cutting-edge genomic-based tools, new innovative approaches to the study of rust-wheat interactions and strong links to the commercial sector. This ensures that new discoveries on rust resistance are fast-tracked for exploitation in the breeding pipeline to address our ultimate goal of reducing the severe threat posed by YR to cereal production worldwide.

Work performed from the beginning of the project to the end of the period covered by the report and main results achieved so far

In this research project, we focused on three key areas: (i) analysing the population structure and genetic diversity of YR isolates found across cereal and grass hosts, (ii) identifying key proteins used by the pathogen to manipulate its plant host and promote disease, and (iii) using comparative genomic studies to identify genes in the wheat host that generate proteins that are essential for the pathogen to cause disease and thereby can be utilised by our industrial partners to provide enhanced resistance to YR. Through this research we have uncovered new insight into how YR manipulates its host during the infection process across cereals and grasses. We also developed a new system in wheat for checking the function of pathogen proteins delivered by YR into its wheat host to manipulate the host plants circuitry to promote disease progression. We have also used an innovative comparative genomic based approach of field collected YR-infected wheat samples to compare the gene expression profiles of different wheat varieties with differing levels of susceptibility to YR. This enabled us to identify a series of genes linked to varietal-specific responses. We then made mutant wheat lines where the function of these wheat genes was disrupted. Evaluation of these wheat mutants showed that many display a severe reduction in disease symptoms. This indicates that the function of these genes in the plant host is essential for the pathogen to cause disease. Disrupting the function of these “susceptibility” genes in commercial wheat varieties could thereby provide new sources of resistance to YR disease.

Progress beyond the state of the art and expected potential impact (including the socio-economic impact and the wider societal implications of the project so far)

A central question in plant pathology is how pathogens cause infection and become adapted to infect specific host varieties or species. Adaptation to new hosts can be studied in depth by characterizing and analyzing pathogen genes encoding effector proteins. Plant pathogens deliver effector proteins to their hosts to reprogram plant defense circuitry and enable parasitic colonization. In this project, we trialled a new system for screening fungal effector protein function in wheat. This new system can now be used to further evaluate predicted YR effector proteins to identify their function and thereby generate new knowledge that will provide insight into how rust pathogens are recognized by and adapt to their hosts.

One major strategy employed to protect crops from disease is through the identification and incorporation of resistance genes that act to recognise specific pathogen effectors. However, pathogens can overcome this type of resistance rapidly by altering the sequence of the corresponding effector gene to evade recognition. Alternatively, susceptibility genes that are generally required for a successful pathogen infection can be manipulated to make the host incompatible with infection. The loss of susceptibility conferred can provide a much more durable resistance. One example is the barley Mlo gene that was discovered over 60 years ago and remains a valuable source of resistance and is still effective in the field after more than 30 years since its first introduction. In this study, we have identified a number of potential disease susceptibility genes that when manipulated confer partial or complete resistance to YR infection. This has provided valuable new insight into how YR manipulates its host during the infection process. For instance, identifying a previously unknown link between branched chain amino acid metabolism and salicylic acid-mediated defence responses. Whilst this research has also practically delivered new targets for manipulation in resistance breeding programmes that are now being explored by our industrial partners in several plant breeding companies.

Comparative genomic-based analysis of closely related host-specialized pathogen races can provide novel insight into how pathogens adapt to new hosts. This can help reveal the molecular components that underlie host adaptation, which can be used to generate new breeding strategies that take full advantage of this new knowledge. In addition, pathogen subpopulations in closely related hosts might act as rich reservoirs of genotypically diverse inoculum that could potentially overcome newly deployed resistance genes as a consequence of host adaptation. To address this, we conducted population structure analysis of YR isolates across the UK on different hosts, genome sequenced selected host-specific YR isolates and conducted gene expression profile analysis. This new information we have generated will be vital for testing the resilience of newly deployed resistance genes, taking into account a more complete YR population structure and mechanistic understanding of host specialisation.

Yellow rust on leaf