SHIFTING SYMBIOTIC SCENARIOS AT THE DAWN OF LAND PLANT-FUNGUS ASSOCIATIONS

Lead Research Organisation: University of Leeds
Department Name: Sch of Biology

Abstract

Plants colonised Earth's landmasses more than 475 Ma, drastically altering the development of the terrestrial biosphere, with far-reaching consequences for all subsequent terrestrial life. It is widely thought that symbiotic fungi facilitated early plant terrestrialisation by enhancing access to mineral nutrients in exchange for photosynthetically-fixed organic carbon. Our recent discoveries have brought into question the hitherto-assumed identity, biology and function of the fungal symbionts of the earliest diverging lineages of extant land plants. Our project addresses these fundamental knowledge gaps, including critical new questions arising from our previous research about the regulation and compatibility of plant-fungal associations. This project promises fascinating discoveries into the intertwined past, present and future of plants, microbes and soils.

More than 80% of plants today associate with soil-dwelling fungi called Glomeromycota, forming mutually beneficial partnerships known as arbuscular mycorrhizas (AM). These cooperative partnerships involve the transfer of plant sugars, produced through photosynthesis, to fungal partners in return for essential nutrients mined from minerals in the soil by the fungi. When the first rootless plants emerged from water onto dry land more the 475 million years ago, it is thought that cooperative fungi provided the nutrients that plants needed to grow on land. Recent research by members of the project team has shown that some of the most evolutionarily ancient plants on Earth, the liverworts, form partnerships with fungi that are probably more evolutionarily ancient than AM. These fungi are called Mucoromycotina. Our findings suggest that associations between liverworts and Mucoromycotina fungi may be ancestral to the mycorrhizal symbiosis, paving the way for the colonisation of the terrestrial environment by plants and the evolution of the intricate terrestrial ecosystems that we are familiar with today. It is equally possible that the earliest land plants actually associated with both Mucoromycotina and AM simultaneously, as some plants still do today. For more than 30 years there has been a focus on AM as the ancestral plant-fungal symbiosis but with our surprising recent discovery of an alternative globally widespread and ancient association, we have the unique opportunity and pressing need to understand a new biology with potentially myriad ramifications for life on Earth.

By using cutting-edge and novel methodologies from different fields of science, our research will generate crucial insights into the functioning and compatibility of cooperation between both groups of fungi with several major groups of land plants. Our experiments will be carried out under different atmospheric CO2 concentrations, reflecting the changing CO2 concentrations on Earth through evolutionary time, providing exciting new insights into the structure, function and evolution of modern plant-fungal symbioses.

Through a deeper mechanistic and evolutionary understanding of the interaction between CO2 and diverse soil fungi, our research expands into wider aspects of soil ecology, plant-soil processes, and may lead to more efficient conservation strategies (see Pathways to Impact document). Through examining the physiological responses of symbiosis through different groups of land plants, this research will aid understanding and prediction of responses of these systems to ongoing changes in atmospheric CO2 concentrations; important considerations within the NERC Climate System and Biodiversity strategies, and with major implications for food security and soil ecology. Looking further into the future, the techniques and hypotheses that we develop and test through this research are transferable to other economically-important symbioses within the plant kingdom, such as fungal diseases of crops and the use of mycorrhizas in crops for future sustainable agriculture.

Planned Impact

Our research proposal aims to address fundamental questions relating to the processes that control the functioning and specificity of mutually beneficial partnerships between land plants and their fungal partners. By examining the responses of plant-fungal symbiosis through key clades of land plants for which such data is currently non-existent, this project will aid understanding and prediction of responses of these systems to future changes in carbon dioxide concentration; important considerations within the NERC Climate System and Biodiversity strategies, and with potentially major implications for soil ecology and food security.

Appeal and benefit of research to wider communities:

1. Researchers and wider scientific audience
This proposal addresses a major gap in our current knowledge and understanding of mycorrhizal symbioses and the evolution of Earths ecosystems. This work will directly interest and benefit researchers in plant-fungal symbioses, evolutionary ecologists, biochemists and Earth system scientists, vegetation and plant-soil nutrient cycling modellers. The techniques and hypotheses that will be developed are potentially applicable to other economically-important plant symbioses, e.g. crop-mycorrhiza interactions in sustainable agriculture.

2. Conservation bodies, policy makers and lobby groups
At least 10% of the c. 1,000 UK bryophyte species are threated and 111 are listed on the UK Biodiversity Action Plan. In addition, the IUCN red list of threatened species currently includes 53 species of liverwort alone, many of which are symbiotic with fungi. Our research will be of direct interest to conservation biologists such as those involved in the Threatened Byrophyte Database (part of the British Bryological Society), and ecologists at related organisations including Scottish Natural Heritage (SNH). These target stakeholders are likely to benefit from gaining new insights into the functional nature of the diverse fungal symbionts in a range of under-studied plant taxa, allowing for a more targeted conservation approach and policies. Our research relates to major themes in conservation biology, such as invasive species and loss of biodiversity by addressing questions about the diversity and functioning of fungal symbionts and the role these interactions may play in interspecific competition in plant communities. Our proposal is particularly relevant to the snowbed vegetation monitoring work carried out by SNH. This work has been ongoing for the last nine years and focusses on the loss of specialist snowbed plants, many of which are bryophytes, from core snowbed sites in the Scottish highlands. Given that the environment beneath the snowbeds is enriched in CO2 and the soils are skeletal, our work is likely to help inform SNH conservation strategies by providing critical information about symbiotic fungal functioning and plant-fungal specificity in such habitats.

2. General public
By seeking to understand one of the most pivotally important symbiotic relationships on Earth that helped sculpt the complex and varied ecosystems of today, our research is of interest to the general public. Members of the project team have previously engaged with the public and students of school age through a number of outreach activities related to plant biology, plant evolution and Earth history such as Imperial Fringe, Science Uncovered, Nature Live, and World Fascination of Plants Day. Previous work by members of the project team has been covered by various media, including US Public Radio and national newspapers, showing the appetite and enthusiasm the general public has for our research

Publications

10 25 50
 
Description So far, we have discovered that Mucoromycotina symbioses are mutualistic with vascular plants, that they are much more widespread than previously thought - extending across the angiosperms. We have discovered these fungi play a far greater role in N nutrition than arbuscular mycorrhizal fungi.
Exploitation Route Further grant funding applications, conservation policy/strategies for endangered species (e.g. Lycopodiella inundata), translation into economically important species.
Sectors Agriculture, Food and Drink,Environment,Leisure Activities, including Sports, Recreation and Tourism,Other

 
Description Katie Field and Martin Bidartondo were featured in a Smith and Nasht documentary (The Kingdom: How fungi made the world) for broadcast in Canada, Australia, NZ, Sweden, France, Germany in April 2018 (http://www.smithandnasht.com/fungi/ - documentary available to download here: https://vimeo.com/ondemand/thekingdom).
Sector Creative Economy,Education,Leisure Activities, including Sports, Recreation and Tourism,Other
Impact Types Cultural,Societal,Policy & public services

 
Description Philip Leverhulme Prize 2017
Amount £100,000 (GBP)
Organisation The Leverhulme Trust 
Sector Academic/University
Country United Kingdom
Start 01/2018 
End 01/2021
 
Description Standard Grant
Amount £364,890 (GBP)
Funding ID NE/N002067/1 
Organisation Natural Environment Research Council 
Sector Public
Country United Kingdom
Start 03/2016 
End 02/2019
 
Description BBC Radio 4: The Today Programme (18.12.17) 
Form Of Engagement Activity A press release, press conference or response to a media enquiry/interview
Part Of Official Scheme? No
Geographic Reach National
Primary Audience Public/other audiences
Results and Impact BBC Radio 4: The Today Programme (18.12.17) Interview with John Humphrys regarding research paper publication (Mills et al., 2018).
Year(s) Of Engagement Activity 2018
 
Description BBC Radio Wales: Good Morning Wales (18.12.17) 
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 BBC Radio Wales: Good Morning Wales (18.12.17) Interview with Rachael Garside about research paper publication (Mills et al., 2018).
Year(s) Of Engagement Activity 2018
 
Description Kingdom of Fungi (release 2018) 
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 Public/other audiences
Results and Impact Kingdom of Fungi (release 2018) - Our research was featured in filming at UoL and Kew Gardens for forthcoming TV documentary The Kingdom of Fungi (Smith & Nascht - http://www.smithandnasht.com/fungi/)
Year(s) Of Engagement Activity 2018
URL http://www.smithandnasht.com/fungi/
 
Description PNAS Inner Workings article 
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 Our research on this project was featured in a PNAS Inner Workings article: Inner Workings: Special relationship between fungi and plants may have spurred changes to ancient climate (http://www.pnas.org/content/114/46/12089)
Year(s) Of Engagement Activity 2017
URL http://www.pnas.org/content/114/46/12089
 
Description UCL second year undergraduate lecture on the Origin and Evolution of plant-fungus associations 
Form Of Engagement Activity A talk or presentation
Part Of Official Scheme? No
Geographic Reach Local
Primary Audience Undergraduate students
Results and Impact Give a broad understanding of the importance of fungal-associations in land plants
Year(s) Of Engagement Activity 2017