The role of the sexual cycle in escalating wheat rust diversity in the UK

Lead Research Organisation: John Innes Centre
Department Name: Crop Genetics

Abstract

Wheat rusts are a major threat to cereal production worldwide. As is common among rust pathogens, the wheat rusts require two hosts to complete their life cycles; stem and yellow rust undertake asexual reproduction on wheat and complete sexual reproduction on barberry (Berberis), where recombination can lead to emergence of novel genotypes. The eradication of barberry in the UK drove stem rust to almost complete extinction. However, over the past decade, barberry planting has been reinitiated and is advancing at speed in many major wheat growing regions. In the UK, this is largely driven by the habitat conservation programme for the endangered barberry carpet moth, Pareulype berberata. This is worrying because in the same time period we have seen an increasing number of sporadic stem rust epidemics in Europe, including severe outbreaks as far apart as Sweden and Sicily. Here in the UK in our preliminary study, we identified one wheat plant infected by stem rust in 2013 which illustrates the potential for stem rust to infect wheat crops in the UK. Furthermore, in 2017 we recorded for the first time in decades stem rust aecia on barberry in the UK. In parallel our collaborators in Sweden in the same year identified the first sexual population of wheat stem rust derived from barberry.

The overall aim of this project is to characterize the composition of rust on Berberis to determine if this mass re-planting could be facilitating the future re-emergence of stem rust in the UK, whilst also enhancing wheat yellow rust diversity. This will provide vital information for the future design and deployment of surveillance and management strategies that fully consider the threat of Berberis. However, it must also carefully balance the desire to minimise the risk of intensifying wheat rust diversity with (where possible) protecting habitat for the barberry carpet moth.

The proposed research aims to: (1) define the composition of rust on Berberis in the UK, (2), determine the risk of barberry-derived sexual rust populations to UK wheat and barley production, and (3) develop a UK risk model for wheat rust dispersal from Berberis and associated management actions. This research project will provide a wealth of information regarding the role of the sexual cycle in exacerbating the diversity of cereal rusts. Furthermore, it will provide vital information that will directly inform policy regarding the re-planting programme for Berberis across the UK and identify areas of high risk that should be avoided or (if plants are already present) regularly monitored. Herein, we aim to achieve a careful balance that manages the immediate needs of the farming community, ensures future resilience in UK wheat by accessing the susceptibility of breeding material to wheat stem rust, whilst conserving the biodiversity of UK fauna.

Technical Summary

Stem and yellow rust are major threats to cereal production worldwide. Like many rust pathogens, they require two hosts to complete their life cycles, undertaking asexual reproduction on cereals and complete sexual reproduction on barberry, where recombination can lead to emergence of novel genotypes. The eradication of barberry in the UK drove stem rust to almost complete extinction. However, over the past decade, barberry planting has reinitiated in many major wheat growing regions. In the UK, this is largely driven by the habitat conservation programme for the endangered barberry carpet moth, Pareulype berberata. This research aims to characterize the composition of rust on barberry to determine if mass re-planting could facilitate the future re-emergence of stem rust in the UK, whilst also enhancing wheat yellow rust diversity.

The central hypothesis is that, in contrast to the position since c.1850, there is potential for rust aecia to play a significant role in generating new races, enhancing pathogen diversity and generating epidemics of wheat rust in the UK. The rationale is based on a preliminary study that provided the first evidence for many decades that wheat stem rust is present in the UK and could potentially be overwintering and infecting barberry. Furthermore, Sweden also witnessed the first report in Europe for decades in 2017 of a highly diverse sexual wheat stem rust epidemic that originated from barberry.

The proposed research will: (1) define the composition of rust on Berberis in the UK, (2), determine the risk of barberry-derived sexual rust populations to UK wheat production, and (3) develop a UK risk model for wheat rust dispersal from Berberis and associated management actions. Herein, we aim to achieve a careful balance that manages the immediate needs of the farming community, ensures future resilience in UK wheat by accessing the susceptibility of breeding material to wheat stem rust, whilst conserving the biodiversity of UK fauna.

Planned Impact

PI Saunders will take the lead in managing the impact plan that will be an agenda item at monthly project meetings with Co-I Brown. Both researchers have excellent track records in communicating the outcomes of their research to a broad audience and sharing tools, resources and associated code in a free and open manner (e.g. crowdsourcing of ash dieback genomics). The PI and Co-I are regularly invited to speak about their research at national/international meetings and at various other venues.

Beneficiaries will include:

Those involved in wheat rust surveillance and management such as the UK Cereal Pathogen Virulence Survey (UKCPVS), which is funded by AHDB. They will benefit from establishing the role of the sexual cycle in generating new rust races in the UK. Throughout the project, information will be relayed to the UKCPVS as soon as relevant. PI Saunders is a regular speaker at their annual stakeholder meeting and Co-I Brown chairs the UKCPVS.

Researchers working with wheat rust disease. All data will be made freely available where practical, at the earliest possible opportunity for use by the wider scientific community. The data will initially be hosted via a project-specific website to ensure rapid release under a creative commons license (CC BY-NC-SA 3.0). Once submitted for publication all data will be deposited in public repositories and linked to via the project-specific website.

Breeders, farmers, agronomists and wheat variety testing authorities will benefit from new information regarding the resilience of current and future wheat varieties to rust infection through screens carried out in South Africa and Pakistan. In particular, assessments regarding general susceptibility to wheat stem rust in South Africa and for susceptibility to the more diverse populations of wheat yellow rust located in the Himalayan region. This may lead directly to decisions regarding the selection of future breeding material. This audience will also benefit from assessment of the risk to rust control posed by replanting of barberry and climate change. They will be reached as participants in our annual project meeting and through communication of results via relevant farming press outlets.

Researchers studying cereal rusts. The development of markers for Puccinia striiformis and P. graminis that are specific to the various formae speciales will be especially valuable. In particular, the KASPar markers (that can be more readily adopted by our breeding partners) will be of great interest to national pathogen surveillance programmes and rust researchers that are increasingly interested in evaluating the role of the sexual cycle in generating diversity for cereal rusts.

The general public, which will benefit from interactions with the PI and Co-I, who have given talks to public audiences (e.g. CropTec and Friends of JIC) 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 aim to give one talk to a public audience (e.g. Science Café, Friends of John Innes) relating to this project, at least once per year throughout the project.

The PDRA's 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 is such that 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. The resulting innovation and training will provide the next generation of skilled crop scientists, with benefits beyond the immediate outcomes of this project.
 
Description We have undertaken an extensive survey of wheat rust on their alternate host common barberry in the UK. This is the first survey of common barberry for rust infection across the UK and has identified many sites where barberry infected by stem rust can be found adjacent to cereal crops. Stem and yellow rust pathogens require two hosts to complete their life cycles, undertaking asexual reproduction on cereals and sexual reproduction on Berberis (including Mahonia), where recombination can lead to emergence of novel genotypes. Eradication of common barberry (B. vulgaris) in the UK drove stem rust to almost complete extinction. However, over the past decade, barberry planting has reinitiated and is advancing in many major wheat growing regions. Part of this is due to active re-planting to enhance habitat for the endangered Barberry Carpet moth (Pareulype berberata), whose current only known food source is B. vulgaris. We have also initiated an iCASE studentship (start date Oct-19) to evaluate alternate food sources, with the aim of maintaining habitat and thereby biodiversity without posing any increased risk to cereal production, if wheat stem rust does re-emerge in the UK.
We have developed the first theoretical model that explains the ejection mechanics of aeciospore liberation in the stem rust plant pathogen Puccinia graminis (Pg). As part of this work, we developed a publicly available 'point-and-click' web interface (https://aeciospore-dispersal-model.com) that enables users to generate local estimates of spore dispersal, which can guide plantings and identify high risk locations for stem rust spread from Berberis to adjacent cereal crops. To assist with the identification of Berberis sites we also initiated an additional objective and carried out a detailed study with two landscape historians at UEA to evaluate the historical prevalence of barberry and stem rust across the UK that was published in Plant Pathology in 2020. This in-turn has helped identify numerous previously unknown associations with landscape markers to guide future barberry surveys.
Exploitation Route Knowing the location of stem rust infected Berberis bushes can help identify those that need careful monitoring and in conjunction with our 'point-and-click' web tool determine their likely risk to neighbouring crops. This will hopefully help to curtail future stem rust epidemics originating on Berberis in the UK
Sectors Agriculture, Food and Drink,Education

URL https://aeciospore-dispersal-model.com
 
Description Our findings are being used to guide planting strategies for Berberis vulgaris to ensure habitat can be maintained for the barberry carpet moth without causing increased concern regarding its potential to escalate stem rust diversity in light of its re-emergence in the UK.
First Year Of Impact 2020
Sector Agriculture, Food and Drink,Leisure Activities, including Sports, Recreation and Tourism
Impact Types Societal

 
Description UKCPVS steering committee
Geographic Reach National 
Policy Influence Type Membership of a guideline committee
 
Description BSPP Undergraduate Vacation Bursary
Amount £2,500 (GBP)
Organisation The British Society of Plant Pathology 
Sector Charity/Non Profit
Country United Kingdom
Start 07/2020 
End 09/2020
 
Description BSPP Undergraduate Vacation Bursary
Amount £2,500 (GBP)
Organisation The British Society of Plant Pathology 
Sector Charity/Non Profit
Country United Kingdom
Start 07/2021 
End 08/2021
 
Description Using a multi-disciplinary approach to tackle a formidable foe - wheat stem rust
Amount £3,500 (GBP)
Organisation Royal Society of Biology (RSB) 
Sector Charity/Non Profit
Country United Kingdom
Start 07/2019 
End 09/2019
 
Description Wheat Disease Early Warning Advisory System (DEWAS) - MARPLE Diagnostics
Amount $3,000,000 (USD)
Organisation International Centre for Maize and Wheat Improvement (CIMMYT) 
Sector Charity/Non Profit
Country Mexico
Start 02/2023 
End 02/2026
 
Title Aeciospore Dispersal Model 
Description We developed a model for simulating aeciospore dispersal gradients for the notorious wheat stem rust pathogen. 
Type Of Material Computer model/algorithm 
Year Produced 2021 
Provided To Others? Yes  
Impact It has just been released so it is too early to measure impact at this stage. 
URL https://aeciospore-dispersal-model.com
 
Title Wheat rust genomics 
Description This website brings together all the current genomic resources and tools available for the three wheat rust pathogens: Puccinia graminis f. sp. tritici, P. striiformis f. sp. tritici and P. triticina. It also provides a forum to connect researchers who may have fungal isolates they would like to share with those interested in collaborating to sequence them. Wheat rust are known as the "polio of agriculture" due to the severe threat these diseases pose to wheat production worldwide and have been associated with many crop failures and famine throughout history. There are three types of wheat rust (stem, yellow and leaf) that are all caused by different species of parasitic fungi. Despite looking different, all three of these fungi are closely related and have a lot of similarities. 
Type Of Material Database/Collection of data 
Year Produced 2021 
Provided To Others? Yes  
Impact The website has yet to be publicised so it is to early to measure impact. 
URL https://www.wheat-rust-genomics.com
 
Description iCASE studentship with Drayton Manor Park 
Organisation Drayton Manor Park
Country United Kingdom 
Sector Private 
PI Contribution This partnership involves the appointment of an iCASE student who is based in my lab and carrying out collaborative research with Drayton Manor Park.
Collaborator Contribution Our partner is providing expertise in conservation biology and land to undertake plantings.
Impact The studentship has just begun, so no measurable outcomes at this stage.
Start Year 2018
 
Description BGRI workshop 
Form Of Engagement Activity A talk or presentation
Part Of Official Scheme? No
Geographic Reach International
Primary Audience Professional Practitioners
Results and Impact Talk on the MARPLE diagnostics methodology and status of wheat stem rust in the UK that led to further discussion.
Year(s) Of Engagement Activity 2021
 
Description BGRI workshop conference 
Form Of Engagement Activity A talk or presentation
Part Of Official Scheme? No
Geographic Reach International
Primary Audience Professional Practitioners
Results and Impact BGRI conference - I was an invited Keynote speaker and three further talks were given by my group. This led to many follow-up conversations.
Year(s) Of Engagement Activity 2020
 
Description BIAZA Field Conservation and Native Species Conference 
Form Of Engagement Activity A talk or presentation
Part Of Official Scheme? No
Geographic Reach National
Primary Audience Professional Practitioners
Results and Impact Presentation to raise awareness of the barberry carpet moth.
Year(s) Of Engagement Activity 2019
 
Description BSPP Plant Health conference 
Form Of Engagement Activity A talk or presentation
Part Of Official Scheme? No
Geographic Reach International
Primary Audience Professional Practitioners
Results and Impact A conference presentation on the status of wheat stem rust in the UK that led to further discussion.
Year(s) Of Engagement Activity 2021
 
Description BarbRE project launch 
Form Of Engagement Activity A talk or presentation
Part Of Official Scheme? No
Geographic Reach Regional
Primary Audience Public/other audiences
Results and Impact Annual project event to raise awareness of the role of Berberis in the life cycle of the wheat rust pathogens.
Year(s) Of Engagement Activity 2019
URL https://www.jic.ac.uk/event/barberry-rust-explorer-launch-evening/
 
Description Bioinformatics & Wheat Genomics workshop - South Africa 
Form Of Engagement Activity Participation in an activity, workshop or similar
Part Of Official Scheme? No
Geographic Reach International
Primary Audience Professional Practitioners
Results and Impact To train partners in South Africa in bioinformatics skills.
Year(s) Of Engagement Activity 2019
 
Description Horticultural Association of Kenya - workshop 
Form Of Engagement Activity A talk or presentation
Part Of Official Scheme? No
Geographic Reach International
Primary Audience Professional Practitioners
Results and Impact A workshop organised by the Horticultural Association of Kenya where I was invited to give a Keynote talk. This led to further interactions.
Year(s) Of Engagement Activity 2020
 
Description Invited talk - India 
Form Of Engagement Activity A talk or presentation
Part Of Official Scheme? No
Geographic Reach International
Primary Audience Professional Practitioners
Results and Impact An invited talk that led to further interest in adoption of some of the methodology we have developed in the lab.
Year(s) Of Engagement Activity 2020
 
Description Invited talk - University of Nebraska Lincoln 
Form Of Engagement Activity A talk or presentation
Part Of Official Scheme? No
Geographic Reach International
Primary Audience Professional Practitioners
Results and Impact A presentation as part of the department seminar series that led to further discussion with postgraduate students on interest in joining JIC for post-doc opportunities.
Year(s) Of Engagement Activity 2022
 
Description Monogram 
Form Of Engagement Activity A talk or presentation
Part Of Official Scheme? No
Geographic Reach National
Primary Audience Professional Practitioners
Results and Impact Provided an invited talk around the issues of stem rust re-emergence in the UK.
Year(s) Of Engagement Activity 2022
 
Description Oxford Nanopore webinar 
Form Of Engagement Activity A talk or presentation
Part Of Official Scheme? No
Geographic Reach International
Primary Audience Professional Practitioners
Results and Impact Invited talk for a webinar organised by Oxford Nanopore that led to further discussion for support of our MARPLE diagnostics project.
Year(s) Of Engagement Activity 2020
 
Description Royal Society: Rosalind Franklin Lecture 
Form Of Engagement Activity A talk or presentation
Part Of Official Scheme? No
Geographic Reach International
Primary Audience Public/other audiences
Results and Impact Invited talk at the Royal Society.
Year(s) Of Engagement Activity 2022
 
Description Syngenta - invited lecture 
Form Of Engagement Activity A talk or presentation
Part Of Official Scheme? No
Geographic Reach International
Primary Audience Professional Practitioners
Results and Impact An invited lecture for Syngenta staff around the re-emergence of stem rust in the UK.
Year(s) Of Engagement Activity 2022
 
Description UKCPVS - invited speaker 
Form Of Engagement Activity A talk or presentation
Part Of Official Scheme? No
Geographic Reach National
Primary Audience Professional Practitioners
Results and Impact An invited talk to share new discoveries from the lab regarding disease surveillance and improving wheat rust resistance with industry.
Year(s) Of Engagement Activity 2020
 
Description UKCPVS stakeholder meeting 
Form Of Engagement Activity A talk or presentation
Part Of Official Scheme? No
Geographic Reach Regional
Primary Audience Professional Practitioners
Results and Impact UKCPVS stakeholder event.
Year(s) Of Engagement Activity 2019
 
Description UKCPVS stakeholder meeting 2022 
Form Of Engagement Activity A talk or presentation
Part Of Official Scheme? No
Geographic Reach National
Primary Audience Industry/Business
Results and Impact A presentation on the status of wheat stem rust in the UK that led to further discussion with industry.
Year(s) Of Engagement Activity 2021
 
Description University of Arkansas - invited talk 
Form Of Engagement Activity A talk or presentation
Part Of Official Scheme? No
Geographic Reach International
Primary Audience Professional Practitioners
Results and Impact An invited talk to share my groups research activities.
Year(s) Of Engagement Activity 2020
 
Description University of Florida - invited speaker 
Form Of Engagement Activity A talk or presentation
Part Of Official Scheme? No
Geographic Reach International
Primary Audience Professional Practitioners
Results and Impact An invited talk to share my groups research.
Year(s) Of Engagement Activity 2020