Population structure and natural selection in the Chalara ash dieback fungus, Hymenoscyphus pseudoalbidus

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

Abstract

Chalara ash dieback is a devastating disease of the European ash and has destroyed large numbers of trees in continental Europe and Scandinavia over the last 20 years. It is caused by a fungus, Hymenoscyphus pseudoalbidus, of which the asexual stage is Chalara fraxinea, hence the common name of the disease. It was first identified in the UK in 2012 and has since been found at hundreds of sites throughout Britain and Ireland. The fungus spreads by dispersal of the sexual spores by the wind and by imports of diseased trees.

Ash is a sexual species which reproduces by prolific seed production, so over the course of time, it is very likely that resistance to Chalara will evolve in the UK population by natural selection. An important challenge for forest scientists is to accelerate this process so that the ash population can recover more rapidly, ideally within a few decades. As the behaviour of introduced forest pathogens can be unpredictable, it is important to understand the evolutionary potential of the fungus.

This project will investigate the ecological genetics and evolutionary potential of H. pseudoalbidus, i.e. the way that genetic variation in the fungus is distributed in relation to the natural environment and its capacity to evolve in response to natural selection. We will obtain information about four key aspects of the population biology of the fungus which can be applied to breeding and management of commercial and natural ash populations.

First, we will investigate the distribution of vegetative compatibility (VC) groups in populations of H. pseudoalbidus in the UK. Many fungi use VC as a system of self/non-self recognition so that when genetically different individuals encounter each other, they form barriers between them which largely prevent each individual from invading the territory occupied by the other. Another important feature of VC barriers is that they inhibit fungi from transmitting doubled-stranded RNA viruses to each other. Study of the spatial distribution of VC groups and of the two mating types will allow us to assess the potential for dsRNA viruses to become established in the H. pseudoalbidus population and thus contribute to attenuating the Chalara epidemic.

Second, we will study the spatial distribution of genetic variation in H. pseudoalbidus, as determined by two types of DNA marker. As the fungus appears to be an ecologically obligate pathogen which depends entirely on its host to complete its life cycle, natural selection is most likely to takes place within host tissue. We will estimate levels of genetic diversity in local populations of H. pseudoalbidus and variation between populations. This will enable us to understand how diverse are the populations of the fungus which are dispersed by the wind and on imported trees. We will then investigate genetic diversity within trees at different stages of the life cycle. This will provide insights into the operation of natural selection on the fungus within its host.

Third, we will investigate variation in traits related to pathogenicity and the life-cycle of H. pseudoalbidus. This information is fundamental to understanding the way that natural selection can cause the fungus to evolve in the natural environment. It is also important for breeding resistant ash trees because if a higher level of pathogenicity involves a cost to the fungus in terms of its reproductive fitness, resistance should become established more widely in the population of ash trees.

Lastly, we will investigate the relationship of H. pseudoalbidus to a closely-related fungus, H. albidus, which has known in the UK since the 19th century and is not considered a harmful pathogen. In particular, our research will aim to understand why H. pseudoalbidus is a much more aggressive parasite than H. albidus and what potential there is for dsRNA viruses to be transferred from H. albidus to H. pseudoalbidus, possibly contributing to a decline in the epidemic of Chalara.

Technical Summary

This proposal is to research the ecological genetics and evolutionary potential of Hymenoscyphus pseudoalbidus (Hp), the ascomycete fungus which causes Chalara ash dieback (CAD) of the European ash (Fraxinus excelsior). This disease has destroyed large numbers of trees in continental Europe; it appeared in the UK in 2012 and has spread rapidly. The project will study four key aspects of Hp to provide a sound foundation for research on its population biology and disease management.

1. We will investigate the spatial distribution of vegetative compatibility (VC) groups in populations of Hp in the UK and will research the potential for dsRNA viruses to become established in Hp and thus attenuate the CAD epidemic.

2. We will study the spatial distribution of DNA marker variation in Hp, both within and between local populations and with developed lesions within trees. This will provide insights into the potential for natural selection to influence evolution of the fungus.

3. We will investigate variation in pathogenicity and life-cycle traits in Hp. This will provide insights into the potential for evolution of Hp by via natural selection, including responding to enhanced resistance in ash populations. Also, as coevolutionary theory makes the robust prediction that a higher cost of pathogenicity will lead to stronger selection for host resistance, studies of pathogen variation will allow predictions of the extent to which 'natural' resistance will become established in the ash population and how quickly this will happen.

4. We will investigate the genetic and ecological relationship between Hp and a closely related fungus, H. albidus (Ha), which is a non-pathogenic fungus indigenous to the UK. The research will compare pathogenicity traits in Ha and Hp and, through comparative study of their VC and mating sytems, will assess the potential for any dsRNA viruses to be transmitted between these fungal species.

Planned Impact

Knowledge about populations of Hymenoscyphus pseudoalbidus (Hp) will inform (1) breeding strategies for resistance to Chalara ash dieback (CAD) in commercial ash trees in the UK and elsewhere and (2) management of natural populations of Fraxinus excelsior, the European ash, to promote evolution of resistance to CAD. All four objectives of this project will contribute to this goal.

Diversity in vegetative compatibility (VC) groups (VCG) is an indicator of the likely success of control methods using hypovirulent Hp infected by dsRNA viruses pathogenic to the fungus. The diversity of VCG in ascomycetes is an important determinant of the rate of transmission of deleterious dsRNA. If VC diversity in Hp is low, both across the UK and in local populations, and if each genet in a developed lesion occupies a large volume of wood, it may be possible to consider using hypovirulent Hp to control CAD by transmitting the virus to other genets. This project will therefore provide information about the likely success of attempts to use hypovirulent strains of Hp to limit the severity of outbreaks of CAD.

The project will also provide information relevant to genetic and pathogenic variation in Hp and processes by which new genotypes are generated and dispersed. Such data on pathogen variation are essential in breeding for disease resistance. If new outbreaks are established by genetically diverse populations of Hp originating from sites where CAD is already established, it will be relatively easy to set up trials to select CAD-resistant ash because each trial will be exposed naturally to a wide range of pathogen genotypes. By contrast, if new outbreaks are established by small sub-samples of established populations, it will be necessary to establish many trial sites because data from any one site may not be typical of responses to Hp in general.

Data on fitness costs and trade-offs will indicate the likely success of resistance breeding and releasing resistant germplasm into the natural environment. An important feature of host-parasite coevolution is that variation in the host influences parasite evolution and vice-versa. Specifically, a higher cost of pathogenicity leads to a higher frequency of resistance in the host. If costs of pathogenicity are high, we can rely on natural selection to re-establish resistance to CAD in the wild population of F. excelsior because resistance genes will be reassorted within genomes of the host, which reproduces sexually and disperses prolific amounts of seed. By contrast, if costs are low, it may be necessary to devise other strategies for reviving the native ash population, such as introduction of resistant germplasm from East Asia.

Research on Hymenoscyphus albidus (Ha), a fungus indigenous to the UK which is closely related to Hp, is more speculative but may in the long term be richly rewarding. Ha may be a source of dsRNA viruses capable of mitigating the damage caused by Hp The potential for using Ha as a source of hypovirulence to control Hp requires not only knowledge of dsRNA in Ha but also of ecological and biological interactions between Ha and Hp.

The project will also contribute to the quality of life in the UK (BBSRC Strategic Priority for Lifelong Health and Wellbeing). A public health study (Donovan et al. 2013, Am. J. Preventative Medicine 44:139-145) showed that access to the natural environment, especially woodland, has great benefits in increasing opportunities for exercise and thus for cardiovascular and respiratory health. Indeed, FR has found that one of the main public concerns about CAD and other tree epidemics is the loss of access to woodland for recreation, a common theme in the value that the general public in the UK places on natural forests. As ash represents 13% of broadleaf tree cover in the UK, recovery from this destructive disease will benefit the public by restoring access to woodland and reducing the risk of injury from falling, diseased trees.
 
Title TheAshProject: A Lasting Legacy for the Ash Tree 
Description Artistic walks, talks and workshops 
Type Of Art Performance (Music, Dance, Drama, etc) 
Year Produced 2017 
Impact Producing a major new commission by internationally recognised artists Ackroyd & Harvey plus walks, talks and a programme of workshops, an online archive and a Kent wide plan for landscape restoration in the wake of ash dieback. 
URL http://www.theashproject.org.uk/
 
Description Not applicable at this time. Further details will be provided in a report to be submitted to the Tree Health and Plant Biosecurity Initiative by the end of March 2018.
Exploitation Route Not applicable at this time. Further details will be provided in a report to be submitted to the Tree Health and Plant Biosecurity Initiative by the end of March 2018.
Sectors Agriculture, Food and Drink,Communities and Social Services/Policy,Environment,Leisure Activities, including Sports, Recreation and Tourism,Transport

URL https://www.forestry.gov.uk/fr/infd-9kchzr
 
Description Not applicable at this time. Full details will be given in a report to be submitted to the THAPBI programme committee by the end of March 2018.
First Year Of Impact 2015
Sector Agriculture, Food and Drink,Communities and Social Services/Policy,Creative Economy,Environment,Leisure Activities, including Sports, Recreation and Tourism,Culture, Heritage, Museums and Collections,Transport
Impact Types Cultural,Societal,Economic,Policy & public services

 
Description Advice to House of Lords on plant biosecurity, especially trees: discussion with policy advisor to HoL Energy & Environment Select Committee regarding future biosecurity for UK woodlands and farming
Geographic Reach National 
Policy Influence Type Gave evidence to a government review
 
Description Advised DEFRA following a request for information following the potential threat from H. frxineus strains not yet present in Europe
Geographic Reach National 
Policy Influence Type Gave evidence to a government review
 
Description Discussions with Norfolk County Council on management of ash dieback and restoration of ash in Norfolk
Geographic Reach Local/Municipal/Regional 
Policy Influence Type Participation in a advisory committee
 
Description Engagement with Government: Advice to JNCC regarding deployment of resistant Ash trees
Geographic Reach National 
Policy Influence Type Gave evidence to a government review
Impact Dr Elizabeth Orton and Prof James Brown gave evidence based advice about how to proceed with developing a plan to deploy resistant ash.
 
Description Forest Pathology Group Presentation on ash dieback
Geographic Reach National 
Policy Influence Type Influenced training of practitioners or researchers
 
Description Hosted visit by Future Trees Trust and gave advice on current situation regarding testing for resistant ash trees in UK.
Geographic Reach National 
Policy Influence Type Influenced training of practitioners or researchers
 
Description Input to DEFRA review of research on ash
Geographic Reach National 
Policy Influence Type Participation in a national consultation
 
Description Meeting of Dr Joan Webber (Forest Research) with Rt Hon Michael Gove, Secretary of State for the Environment, Food and Rural Affairs.
Geographic Reach National 
Policy Influence Type Participation in a national consultation
 
Description Participated in DEFRA organised Ash Dieback Research Oversight Group (ADROG) meeting
Geographic Reach National 
Policy Influence Type Participation in a national consultation
 
Description Presentation and Discussion with Deputy Director for Animal and Plant Health Evidence and Analysis, DEFRA at JIC.
Geographic Reach National 
Policy Influence Type Participation in a national consultation
 
Description Presentation to Nicola Spence, DEFRA Chief Plant Health Officer on visit to JIC
Geographic Reach National 
Policy Influence Type Gave evidence to a government review
 
Description Seminar hosted by HRH Prince Charles on tree health & biosecurity, attended by Dr Joan Webber (Forest Research)
Geographic Reach National 
Policy Influence Type Membership of a guideline committee
Impact National consultation on tree health and biosecurity, including researchers, academics, NGOs, industry, etc hosted by HRH Prince Charles at Highgrove.
 
Description Student at Forest Research working on ash dieback, in collaboration with Woodland Trust and Network Rail
Amount £90,000 (GBP)
Organisation Department For Environment, Food And Rural Affairs (DEFRA) 
Sector Public
Country United Kingdom
Start 11/2017 
End 12/2020
 
Title JENNIFER collection of ash 
Description With East Malling Research, JIC established the JENNIFER collection of ash genotypes as a national resource for research in the UK. JENNIFER = John Innes / East Malling National Nursery for Integrated Fraxinus excelsior Research 
Type Of Material Database/Collection of data 
Year Produced 2018 
Provided To Others? Yes  
Impact Field trial of the JENNIFER collection planted at a site near Acle, Norfolk 
 
Description Collaboration of FR with BOKU, Austria 
Organisation University of Natural Resources and Applied Life Sciences
Country Austria 
Sector Academic/University 
PI Contribution Collaboration of Joan Webber & Clive Brasier, Forest Research, with Thomas Kiritsis, BOKU, Austria, on ecological genetics of Hymenoscyphus albidus.
Collaborator Contribution Information on breeding strategies of Hymenoscyphus albidus in Europe.
Impact Paper on ecological genetics and breeding systems of Hymenoscyphus albidus in Forest Ecology.
Start Year 2015
 
Description Collaboration on emerald ash borer 
Organisation East Malling Research
Country United Kingdom 
Sector Academic/University 
PI Contribution Identification of suitable Fraxinus excelsior accessions from the JENNIFER collection for emerald ash borer trials. Data analysis. Leading the publication.
Collaborator Contribution RBG Kew: Formation of collaboration and planning experiments. EMR: Provision of plant material for EAB experiments. OSU: Conduct of experiments and data analysis.
Impact Data on response of UK Fraxinus excelsior to emerald ash borer in controlled trials.
Start Year 2016
 
Description Collaboration on emerald ash borer 
Organisation Ohio State University
Country United States 
Sector Academic/University 
PI Contribution Identification of suitable Fraxinus excelsior accessions from the JENNIFER collection for emerald ash borer trials. Data analysis. Leading the publication.
Collaborator Contribution RBG Kew: Formation of collaboration and planning experiments. EMR: Provision of plant material for EAB experiments. OSU: Conduct of experiments and data analysis.
Impact Data on response of UK Fraxinus excelsior to emerald ash borer in controlled trials.
Start Year 2016
 
Description Collaboration on emerald ash borer 
Organisation Royal Botanic Gardens, Kew
Country United Kingdom 
Sector Charity/Non Profit 
PI Contribution Identification of suitable Fraxinus excelsior accessions from the JENNIFER collection for emerald ash borer trials. Data analysis. Leading the publication.
Collaborator Contribution RBG Kew: Formation of collaboration and planning experiments. EMR: Provision of plant material for EAB experiments. OSU: Conduct of experiments and data analysis.
Impact Data on response of UK Fraxinus excelsior to emerald ash borer in controlled trials.
Start Year 2016
 
Description Collaboration with NIBIO, Norway, to try to determine population structure of H. albidus in UK 
Organisation Norwegian Institute of Bioeconomy Research
PI Contribution Provided samples and post-doc to access sequencing technologies.
Collaborator Contribution Provided expertise and equipment to sequence samples
Impact Data are inconclusive
Start Year 2015
 
Description Establishment of JENNIFER population of ash genotypes 
Organisation East Malling Research
Country United Kingdom 
Sector Academic/University 
PI Contribution Production of replicated clones of 328 Fraxinus accessions in the JENNIFER collection, for future research on ash including ash dieback, resistance to herbivores and phenological traits.
Collaborator Contribution East Malling: Cloning the Fraxinus accessions by grafting. Norfolk CC and Forest Research: Provision of trial sites with deer fence for ash dieback trials.
Impact Planted field trial near Acle, Norfolk, January 2018.
Start Year 2015
 
Description Establishment of JENNIFER population of ash genotypes 
Organisation Forest Research
Country United Kingdom 
Sector Public 
PI Contribution Production of replicated clones of 328 Fraxinus accessions in the JENNIFER collection, for future research on ash including ash dieback, resistance to herbivores and phenological traits.
Collaborator Contribution East Malling: Cloning the Fraxinus accessions by grafting. Norfolk CC and Forest Research: Provision of trial sites with deer fence for ash dieback trials.
Impact Planted field trial near Acle, Norfolk, January 2018.
Start Year 2015
 
Description Establishment of JENNIFER population of ash genotypes 
Organisation Norfolk County Council
Country United Kingdom 
Sector Public 
PI Contribution Production of replicated clones of 328 Fraxinus accessions in the JENNIFER collection, for future research on ash including ash dieback, resistance to herbivores and phenological traits.
Collaborator Contribution East Malling: Cloning the Fraxinus accessions by grafting. Norfolk CC and Forest Research: Provision of trial sites with deer fence for ash dieback trials.
Impact Planted field trial near Acle, Norfolk, January 2018.
Start Year 2015
 
Description JENNIFER collaboration with Warwick and E.Malling 
Organisation East Malling Research
Country United Kingdom 
Sector Academic/University 
PI Contribution Led collaboration to develop research proposal on the influence of secondary metabolites in European ash (Fraxinus excelsior) on possible trade-offs between resistances to ash dieback and to herbivores.
Collaborator Contribution Contributed to research proposal on the influence of secondary metabolites in European ash (Fraxinus excelsior) on possible trade-offs between resistances to ash dieback and to herbivores.
Impact Response-mode grant proposal submitted to BBSRC. Multi-disciplinary: pathology, entomology, genetics, population genetics, ecology, forestry, analytical chemistry, plant molecular biology.
Start Year 2017
 
Description JENNIFER collaboration with Warwick and E.Malling 
Organisation University of Warwick
Country United Kingdom 
Sector Academic/University 
PI Contribution Led collaboration to develop research proposal on the influence of secondary metabolites in European ash (Fraxinus excelsior) on possible trade-offs between resistances to ash dieback and to herbivores.
Collaborator Contribution Contributed to research proposal on the influence of secondary metabolites in European ash (Fraxinus excelsior) on possible trade-offs between resistances to ash dieback and to herbivores.
Impact Response-mode grant proposal submitted to BBSRC. Multi-disciplinary: pathology, entomology, genetics, population genetics, ecology, forestry, analytical chemistry, plant molecular biology.
Start Year 2017
 
Description JIC/FR collaboration on Chalara ash dieback 
Organisation Forest Research
Country United Kingdom 
Sector Public 
PI Contribution Research on pathology, molecular markers, population genetics and natural selection in Chalara ash dieback.
Collaborator Contribution Research on pathology, population genetics and forest management in relation to Chalara ash dieback.
Impact Papers in peer-reviewed journals: published and in press. Advice to Forestry Commission and DEFRA. Public awareness activities. Advice to forestry industry. Disciplines: plant pathology (particularly forest pathology), population genetics, forestry.
Start Year 2014
 
Description Review of ash resources in UK and impact of dieback 
Organisation Earth Trust
Country United Kingdom 
Sector Charity/Non Profit 
PI Contribution Review of ash genetics resources and impact of dieback in the UK.
Collaborator Contribution Review of ash genetics resources and impact of dieback in the UK.
Impact Book chapter by Clark & Webber.
Start Year 2015
 
Description Advice by Dr Joan Webber (Forest Research) to Forestry Commission on tree management related to ash dieback 
Form Of Engagement Activity A formal working group, expert panel or dialogue
Part Of Official Scheme? No
Geographic Reach National
Primary Audience Industry/Business
Results and Impact Advice by Dr Joan Webber (Forest Research) to Forestry Commission on management of trees related to falling boughs and whole trees caused by ash dieback.
Year(s) Of Engagement Activity 2018
 
Description Advisor, Nornex 
Form Of Engagement Activity A formal working group, expert panel or dialogue
Part Of Official Scheme? No
Geographic Reach International
Primary Audience Professional Practitioners
Results and Impact Prof James Brown was one of the two advisors to the Nornex project on ash dieback, contributing knowledge about population genetics and plant breeding.
Year(s) Of Engagement Activity 2013,2014,2015,2016
 
Description Appearance by Dr Joan Webber (Forest Research) on Countryfile Winter Diaries, BBC1 
Form Of Engagement Activity A broadcast e.g. TV/radio/film/podcast (other than news/press)
Part Of Official Scheme? No
Geographic Reach International
Primary Audience Media (as a channel to the public)
Results and Impact Interviewed for BBC1 TV Countryfile Winter Diaries about tree diseases, including ash dieback.
Year(s) Of Engagement Activity 2018
 
Description Article on ash dieback in the John Innes Centre 'Advances' magazine. 
Form Of Engagement Activity A magazine, newsletter or online publication
Part Of Official Scheme? No
Geographic Reach International
Primary Audience Public/other audiences
Results and Impact Article on ash dieback written for the print and online publication Advances by the JIC to report on the work happening on the project.
Year(s) Of Engagement Activity 2017
 
Description Article on on the Ash dieback project featured in NERC's magazizne Planet Earth 
Form Of Engagement Activity A magazine, newsletter or online publication
Part Of Official Scheme? No
Geographic Reach International
Primary Audience Public/other audiences
Results and Impact An article was written for NERC's magazine to show what was currently being funded and the work we intended to do.
Year(s) Of Engagement Activity 2014
 
Description Attended and presented a poster at the international conference 'Genetics of Tree-Parasite Interactions' in Orleans, France 
Form Of Engagement Activity A talk or presentation
Part Of Official Scheme? No
Geographic Reach International
Primary Audience Other audiences
Results and Impact We presented our ongoing work to a international community of delegates as well as meeting local landowners to discuss impacts of tree diseases.
Year(s) Of Engagement Activity 2015
 
Description Dr Joan Webber (Forest Research) regularly updated FR ash dieback project pages. 
Form Of Engagement Activity Engagement focused website, blog or social media channel
Part Of Official Scheme? No
Geographic Reach International
Primary Audience Public/other audiences
Results and Impact Regular updates of Forest Research web pages on ash dieback with information relevant to the general public, industry, policy-makers and others.
Year(s) Of Engagement Activity 2014,2015,2016,2017,2018
 
Description Dr Joan Webber, Forest Research: professional advice to student at National School of Forestry & University of Cumbria 
Form Of Engagement Activity A formal working group, expert panel or dialogue
Part Of Official Scheme? No
Geographic Reach National
Primary Audience Postgraduate students
Results and Impact Advice to an undergraduate student at the University of Cumbria and National School of Forestry relating to his thesis on, 'The effect of Chalara dieback and rainfall on tree-ring increment in European ash (Fraxinus excelsior)'.
Year(s) Of Engagement Activity 2015,2016,2017
 
Description Dr Joan Webber, Forest Research: visit by Chinese forest pathologists 
Form Of Engagement Activity A talk or presentation
Part Of Official Scheme? No
Geographic Reach International
Primary Audience Professional Practitioners
Results and Impact Study visit by Chinese scientists to Forest Research, including Dr Joan Webber, to learn about current research on ash dieback.
Year(s) Of Engagement Activity 2015
 
Description Hosted a visit of representatives from The Woodland Trust,Tree Council, Norfolk and Suffolk County Councils 
Form Of Engagement Activity Participation in an open day or visit at my research institution
Part Of Official Scheme? No
Geographic Reach National
Primary Audience Professional Practitioners
Results and Impact Stakeholders with an interest in woodlands and the environment visited the institute to discuss the impact of ash dieback on land management practice and understand implications for the disease in the short and longer term. They left with a better understanding of the disease and raised many questions about future research areas,
Year(s) Of Engagement Activity 2017
 
Description Meeting with Natural England, about ash dieback 
Form Of Engagement Activity Participation in an open day or visit at my research institution
Part Of Official Scheme? No
Geographic Reach National
Primary Audience Policymakers/politicians
Results and Impact Prof James Brown updated science advisor to Natural England on current situation of ash dieback, prospects for recovery and future threats to woodland
Year(s) Of Engagement Activity 2017
 
Description On camera interview with BBC local news and press release published by local newspaper. 
Form Of Engagement Activity A press release, press conference or response to a media enquiry/interview
Part Of Official Scheme? No
Geographic Reach Regional
Primary Audience Public/other audiences
Results and Impact Interview and press release on our recently published paper on ash dieback attracted interest form local news outlets and led to questions from public.
Year(s) Of Engagement Activity 2017
 
Description Presentation to British Society for Plant Pathology Annual Meeting about the project and findings regarding population structure 
Form Of Engagement Activity A talk or presentation
Part Of Official Scheme? No
Geographic Reach International
Primary Audience Other audiences
Results and Impact Presented the current findings of out work on populations structure of the pathogen in the UK to researchers including postgraduate students. This sparked discussion afterwards.
Year(s) Of Engagement Activity 2016