Interactions between crops, arbuscular mycorrhizal fungi and atmospheric CO2

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

Abstract

Since the post-war Green Revolution, agricultural productivity has increased dramatically in terms of crop yield and predictability. This has been dependent on the development and application of novel pesticides and nitrogen- and phosphorus-based fertilisers, coupled to advances in plant breeding and genetic technologies. Traditionally, the development of crop breeding programs has rarely considered the ability of crops to establish associations with mycorrhizal fungi (soil fungi that engage in a reciprocol exchange of nutrients for plant-fixed photosynthates in plant roots) as a main desirable trait.

As such, several studies have shown that the colonisation of roots by mycorrhiza varies significantly and continuously among cultivars in cereals. Even antagonistic breeding for such a character seems to occur in some cases, in which selection for increased disease resistance has led to varieties with reduced ability to form mycorrhizal associations. In addition, regular tillage of the soil disrupts mycorrhizal networks and reduces the extent of soil colonisation by mycorrhizal fungi. The intensive use of agrochemicals in agriculture has compounded this impaired mycorrhizal functioning, which further increases crop dependence on fungicide and fertilizer inputs to sustain yields in a positive feedback loop.

In the last 15 years key crop yields have plateaued. With an increasing human population, depletion of global rock-phosphorus and growing energy prices making fertiliser production unsustainable, Europe is now facing a food security crisis, further compounded by the environmental challenges presented by global climate change. This crisis requires new and innovative technologies developed from a variety of scientific disciplines, many of which already exist. In recent times there has been much interest in exploiting mycorrhizal associations for agronomic benefit such as enhanced access to existing soil P pools, enhanced disease resistance and drought tolerance. However, given the IPCC predictions for future increases in atmospheric CO2 concentrations, it is vital that we understand how these critically important symbioses will function under such a CO2-rich atmosphere.

Knowledge exchange (KE) between the academic research community and industry colleagues is essential to mitigate these challenges. By quantifying the functionality and efficiency of key European cereal crop-mycorrhiza interactions and their responses to atmospheric CO2 concentration, my research will address the critical and fundamental knowledge gaps in our understanding of crop-mycorrhizosphere interactions and the effects of future climate change on their interactions. Further, by working closely with my industrial partner, Dr Richard Summers (RAGT seeds), my research will bridge the divide between academic research and the agricultural industry, providing critical data and solutions to help mitigate the challenges posed by increasing atmospheric CO2 concentration on food security.

Technical Summary

Since the post-war Green Revolution, agricultural productivity has increased dramatically in terms of crop yield and predictability. This has been largely dependent on the development and application of novel pesticides and nitrogen- and phosphorus-based fertilisers, coupled to advances in plant breeding and genetic technologies.
In the last 15 years however, wheat yields have plateaued and this is replicated across many key crop species. With an ever- increasing human population and depletion of global rock- phosphorus and growing energy prices making fertiliser production unsustainable, Europe is now facing a food security crisis. Solving this crisis requires new and innovative technologies developed from a variety of scientific disciplines. Currently, the mechanisms we rely on to ensure security of our food supply remain unchanged with plant science research focussing on the symptoms, rather than the root causes of the problem.

Many key crop species have been shown to be able to form mutualistic symbioses with arbuscular mycorrhizal fungi (AMF) and this is leading to the development of novel approaches in crop breeding and agricultural practices, encouraging the formation of mycorrhizal associations and utilisation of previously plant-inaccessible phosphorus pools. My fundamental research on wild species has shown that the functional efficiency of the exchange of carbon-for nutrients is affected by atmospheric CO2 (a[CO2]). If similar responses to a[CO2] are to be expected in domestic crops as I have demonstrated in other plants, the benefits brought by changing agricultural practices with the development of mycorrhiza-friendly crops and rhizosphere-centric agricultural practises could be drastic. This represents a critical knowledge gap with immediate and urgent potential for translation.
My project will address this major gap in our knowledge of crop-mycorrhiza interactions and contribute directly to the development of new, efficient crops in the future.

Planned Impact

A key component of my fellowship project is the translation of my science into useable agri-solutions which will be achieved readily through collaboration with my industrial partner, RAGT Seeds.
In order to facilitate this process, and for other relevant plant science research at the University of Sheffield, I plan to develop an agri-tech 'innovation pipeline', generating awareness, opportunity and support for collaborations between scientists and industrial partners thereby promoting translational plant science. By developing a structured pipeline by which fundamental research is translated from lab bench to usable agri-solutions, my project will increase impact of BBSRC-funded science within Sheffield; providing the framework by which other faculties and universities can increase their own KE.

Objectives:
O1: Generate and maintain a user-searchable KE portal identifying the areas and themes of plant science research, key innovations in technology and their potential applications to agri-tech sector.
O2: Identify existing and potential industrial links and compile a list of the agri-tech "Grand challenges" to parameterise the 'innovation pipeline'.
O3: Use the 'innovation pipeline' to facilitate a step-change in the level of collaborative activity between plant scientists and industry end-users.
O4: Raise the profile of successful industrial applications of research at the University of Sheffield with the wider research and development community.

Publications

10 25 50
 
Description The most significant specific key findings relating to this award (so far) are:

* There is variation between modern spring wheat cultivars in terms of receptivity to and functionality of arbuscular mycorrhizal fungi. Our research showed that (cv. Cadenza) shows relatively good colonisation and Avalon is much less competent in forming associations with mycorrhizal fungi. We also showed variation in terms of mycorrhizal function (C-for-P) between these cultivars (Elliott et al., 2021, Plants, People, Planet).

* Mycorrhizal contributed to wheat P and N nutrition varies to a degree between cultivars of wheat and that, although total plant P and N are affected by rising atmospheric [CO2], this isn't a result of mycorrhizal contributions to plant nutrition. We also discovered that the contributions of modern wheat cultivars to mycorrhizal C were very low in comparison to other plants, again, this wasn't affected by increasing atmospheric [CO2] (Thirkell et al., 2019, Global Change Biology).

* Mycorrhizas contribute to barley nutrition in return for minimal C from the plant host. Mycorrhizal contributions to barley nutrition are not related to the C inputs from the plant host, and that they are insufficient to reduce nutrient dilution caused by increasing atmospheric [CO2] (Thirkell et al., 2020, Plants, People, Planet).

* In collaboration with industry partners ADAS, we screened a mapping population (Avalon x Cadenza) of wheat to investigate whether mycorrhizal responsiveness (i.e. wheat growth response, linked to P uptake) was a heritable trait that could be identified via QTL and potentially exploited to breed new wheat varieties that are more responsive to mycorrhizal colonisation that current modern cultivars. We found that there was significant variation across wheat lines ranging from a >50% reduction and up to >100% increase in growth in response to mycorrhizal colonisation. Interestingly, mycorrhization appeared to alleviate biomass-related shoot P dilution when compared to non-mycorrhizal plants. Our QTL analysis suggests that there is potential to breed for these positive responses with identification of several QTLs for these traits. These findings are in press with Food and Energy Security (Thirkell et al., 2022).

* Aphid herbivory (aphids redirect plant resources away from AMF, potentially affecting mycorrhizal benefits and are a major vector of disease in wheat, responsible for annual losses in cereal productivity of >£120M) had cultivar-specific effects on mycorrhizal function, reducing C allocation to mycorrhizal fungi with detrimental impacts on mycorrhizal-derived P and N. We hypothesised that increasing CO2 in the atmosphere would alleviate this effect by making C more available to the plant and hence the mycorrhizal fungi, however this was not the case (Charters et al. 2020, Current Biology).

Overall, this the results of this project can be considered from the translational/applied perspective in that they suggest there is a large amount of variation in the ability of modern UK cereals to form mycorrhizal associations with soil fungi with some cultivars forming associations much more readily than others. The ability to form these associations does not appear to be linked to the functionality of the symbiosis though, and this suggests that mycorrhizal function, rather than colonisation, should be a key target trait for plant breeders. Interestingly, rising atmospheric CO2 does not seem to impede the function of mycorrhizal associations in crops, although future work should aim to test this in combination with other critical climate change factors. This research has demonstrated that mycorrhizal responsiveness is associated with several QTLs across a wheat mapping population and thus there is feasible scope and potential to breed for mycorrhizal-function traits in modern cereals to reduce inputs of chemical-based fertilisers.

From a fundamental perspective, this project has opened some really exciting areas of future research. Our findings that mycorrhizal function does follow a simple linear relationship between carbon input to fungi vs nutrient supply to host, particularly when environmental or biotic perturbations are applied to the system, opposes widely-held dogma regarding mycorrhizal function.
Exploitation Route We have engaged with ADAS and a number of plant breeders to take this research forward and incorporate some of our findings in both current breeding programmes and for the future. In order to fully realise this however, we need to repeat the QTL screen and expand our dataset. To do this, we are currently working towards putting together a BBSRC IPA grant together with our industry partners. We are also starting to collaborate with Prof Giles Oldroyd (Cambridge Crop Science Centre) to investigate diverse mycorrhiza-forming fungi in barley and are hoping to apply for further funding to support that research and realise impact within the agritech community.

We are building on the more fundamental aspects of the research by investigating the importance of mycorrhizal networks in mono-cropping systems and assessing the relative contributions of individuals within the network, of the same genotype, of different genotype (cultivar) and of different species. We are overlaying this with environmental and biotic perturbations, for instance rising CO2, aphid herbivory or pathogens.
Sectors Agriculture, Food and Drink,Environment

 
Description Life In The Soil podcast - contributor to BiodivERsA-funded podcast about soil biodiversity, why it matters, and how we can protect it. (2021) https://rilliglab.org/podcast/ Sheffield DocFest Exchange: Beyond our own eyes - Wellcome Trust-funded commission to collaborate with Gregory Herbert, an artist working with film, sculpture and installation (https://gregoryherbert.co.uk), to produce a film inspired by my research into plant-fungal interactions, premiered at COP26 at Glasgow CCA, November 2021 BBC World Service - Science in Action, 22nd November 2019, Discussed findings and significance of Thirkell et al., 2019. https://www.bbc.co.uk/programmes/w3csym2q (from 9min 20s) Great Yorkshire Show 9-11th July 2019, Co-designed and ran an activity as part of the Generation Z section of the GYS's Discovery Zone for young adults looking at relationships between plants, soil and fungi. ITV News Calendar, 9th July 2019, discussed my research looking at how we can help crops get more nutrients out of the soil, without the need to add great quantities of fertilisers. Public lecture, Grow Wild, Univ. Leeds/Leeds Light Night (4-6.10.18) part of Kew's Grow Wild "More than a mushroom" event for Light Night (Leeds City Council) BBC Radio Wales: Good Morning Wales (12.09.18). Interview with Rachel Garside about release of Kew's State of the World's Fungi report (paid contribution) Public lecture, Eden Project, Cornwall (25.05.18). Part of opening festival for the Wellcome Trust-funded "Invisible Worlds" exhibition. Contribution to Postnote 601: Sustaining the Soil Microbiome (https://researchbriefings.parliament.uk/ResearchBriefing/Summary/POST-PN-0601)
Sector Agriculture, Food and Drink,Education,Environment
Impact Types Cultural,Societal,Policy & public services

 
Description Consolidator Grant. "MYCOREV - A Mycorrhizal Revolution: the role of diverse symbiotic fungi in modern terrestrial ecosystems"
Amount € 2,059,000 (EUR)
Funding ID 865225 
Organisation European Research Council (ERC) 
Sector Public
Country Belgium
Start 06/2020 
End 06/2025
 
Description Friend or foe; who wins in the competition for plant resources?
Amount £464,540 (GBP)
Funding ID RPG-2019-162 
Organisation The Leverhulme Trust 
Sector Charity/Non Profit
Country United Kingdom
Start 01/2020 
End 01/2023
 
Description How did the evolution of plants, microbial symbionts and terrestrial nutrient cycles change Earth's long-term climate?
Amount £617,796 (GBP)
Funding ID NE/S009663/1 
Organisation Natural Environment Research Council 
Sector Public
Country United Kingdom
Start 05/2019 
End 05/2022
 
Description LOCKED UP: The role of biotic and abiotic interactions in the stabilisation and persistence of soil organic carbon
Amount £611,642 (GBP)
Funding ID NE/S004963/1 
Organisation Natural Environment Research Council 
Sector Public
Country United Kingdom
Start 02/2019 
End 02/2023
 
Description Philip Leverhulme Prize 2017
Amount £100,000 (GBP)
Organisation The Leverhulme Trust 
Sector Charity/Non Profit
Country United Kingdom
Start 01/2018 
End 01/2021
 
Description Rank Prize Funds New Investigator Award
Amount £20,000 (GBP)
Organisation Rank Prize Funds 
Sector Charity/Non Profit
Country United Kingdom
Start 01/2017 
 
Description Standard grant
Amount £587,100 (GBP)
Funding ID NE/N00941X/1 
Organisation Natural Environment Research Council 
Sector Public
Country United Kingdom
Start 06/2016 
End 06/2019
 
Description White Rose PhD Studentship Training Network
Amount £65,000 (GBP)
Organisation White Rose University Consortium 
Sector Academic/University
Country United Kingdom
Start 10/2016 
End 09/2019
 
Title Soil binding assay 
Description Allows users to determine capacity of root exudates to bind soil, form aggregates etc. 
Type Of Material Biological samples 
Year Produced 2018 
Provided To Others? Yes  
Impact Publication: Akhtar J, Galloway AF, Nikolopoulos G, Field KJ, Knox JP. (2018) A quantitative method for the high throughput screening for the soil adhesion properties of plant and microbial polysaccharides and exudates. Plant and Soil 1-2: 57-65 doi: 10.1007/s11104-018-3670-1 
 
Description Collaboration with Neil Pavely and Mike Grimmer (ADAS) 
Organisation ADAS
Country United Kingdom 
Sector Private 
PI Contribution Wrote a successful N8 pump priming funding bid, developing an IPA grant
Collaborator Contribution QTL analysis of data obtained from screen of 100 wheat lines
Impact Awaiting results
Start Year 2018
 
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 interview: State of the World's Fungi response 
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 Wales interview (Good Morning Wales), response to publicaiton of Kew's State of the World's Fungi.
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 BBC World Service - Science in Action, 
Form Of Engagement Activity A press release, press conference or response to a media enquiry/interview
Part Of Official Scheme? No
Geographic Reach International
Primary Audience Public/other audiences
Results and Impact 22nd November 2019, Discussed findings and significance of Thirkell et al., 2019.
Year(s) Of Engagement Activity 2019
URL http://www.bbc.co.uk/programmes/w3csym2q
 
Description Faculty of Biological Sciences, Excellence with Impact event 
Form Of Engagement Activity Participation in an open day or visit at my research institution
Part Of Official Scheme? No
Geographic Reach Regional
Primary Audience Supporters
Results and Impact Presented my work on crops and mycorrhizas, produced a banner and manned a stand
Year(s) Of Engagement Activity 2016
 
Description Great Yorkshire Show 9-11th July 2019 
Form Of Engagement Activity Participation in an activity, workshop or similar
Part Of Official Scheme? No
Geographic Reach Regional
Primary Audience Schools
Results and Impact Co-designed and ran an activity as part of the Generation Z section of the GYS's Discovery Zone for young adults looking at relationships between plants, soil and fungi.
Year(s) Of Engagement Activity 2019
 
Description ITV News Calendar interview 
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 9th July 2019, discussed my research looking at how we can help crops get more nutrients out of the soil, without the need to add great quantities of fertilisers.
Year(s) Of Engagement Activity 2019
 
Description Observations on Being - scientific consultant for immersive, multisensory installation at Charterhouse Heritage Park, Coventry (June-August 2021) 
Form Of Engagement Activity Participation in an activity, workshop or similar
Part Of Official Scheme? No
Geographic Reach National
Primary Audience Public/other audiences
Results and Impact "Mapping the journey of breath from different scientific and cultural perspectives, this multisensory narrative of epic proportions uncovers the living worlds both beyond and within us, to reveal the deep and beautiful truths that lie just outside the limits of our perception. Inviting audiences to cross the threshold and follow an expansive journey through the invisible natural world, Observations on Being brings together a series of thought-provoking and immersive audiovisual art installations and soundscapes, which challenge our ideas of life and death and examine our symbiotic relationship with nature. The ambitious works will be located across the beautiful, tree-filled spaces and buildings of Charterhouse Heritage Park - Joseph Paxton's Grade I listed cemetery and its arboretum." https://yorkmediale.com/events/observations-on-being/
Year(s) Of Engagement Activity 2021
URL https://yorkmediale.com/events/observations-on-being/
 
Description Participation in podcast 
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 invited to participate in "Life in the Soil" podcast (https://rilliglab.org/podcast/). Life in the Soil is a collaboration between the Rillig Lab, at the Freie Universität Berlin - Institut für Biologie, and podcaster Anja Krieger. The podcast is funded through the BiodivERsA projekt Digging Deeper.
Year(s) Of Engagement Activity 2020,2021
URL https://rilliglab.org/podcast/
 
Description Public lecture for "More than a mushroom" event, Light Night, Leeds 
Form Of Engagement Activity A talk or presentation
Part Of Official Scheme? No
Geographic Reach Local
Primary Audience Public/other audiences
Results and Impact Public lecture on how fungi helped the Earth get green and future role in sustainability, invited as part of Kew's Grow Wild activities "More than a mushroom" event at University of Leeds for Leeds City Light Ninght (4-6.10.2018)
Year(s) Of Engagement Activity 2018
 
Description Public lecture on fungi at Eden Project 
Form Of Engagement Activity A talk or presentation
Part Of Official Scheme? No
Geographic Reach Local
Primary Audience Public/other audiences
Results and Impact Public lecture on significance of "invisible" fungi to general public, e.g. agriculture, evolution, climate
Year(s) Of Engagement Activity 2018
 
Description Sheffield DocFest Exchange: Beyond our own eyes 
Form Of Engagement Activity Participation in an activity, workshop or similar
Part Of Official Scheme? No
Geographic Reach International
Primary Audience Public/other audiences
Results and Impact Wellcome Trust-funded commission to collaborate with Gregory Herbert, an artist working with film, sculpture and installation (https://gregoryherbert.co.uk), to produce a film inspired by my research into plant-fungal interactions, premiered at COP26 at Glasgow CCA, November 2021
Year(s) Of Engagement Activity 2021
URL https://sheffdocfest.com/news/announcing-docfest-exchange-beyond-our-own-eyes-film-commissions