Exploiting the immune system to tackle emerging filamentous diseases in tomato

Lead Research Organisation: University of Sheffield
Department Name: Animal and Plant Sciences

Abstract

The world's population is expected to increase by 1.6 billion in the next 40 years, which challenges humanity to increase food production by 70%. Despite current control measures, weeds, pests and pathogens claim up to 40% of our major crop yields after use of effective control. Filamentous pathogens (e.g. mildews, molds and late blight) are exceptionally problematic to control as their evolutionary capacity makes them highly proficient on overcoming the resistance offered by genes or chemical pesticides. In the past century, there has been an increasing number of virulent emerging pathogenic fungi. Agricultural systems are extremely vulnerable to emergence and epidemics of filamentous disease due to food mobility and climate change. Moreover, crop cultivation under controlled environment, even when it provides advantages in terms of increased production, it represents a clear disadvantage in controlling the spread of filamentous diseases. Current methods of control depend largely on the use of fungicides, which are under strict European regulation due to its toxicity to human health and the environment. Therefore, it is urgent to develop alternative strategies to control diseases.
Plants are equipped to defend themselves against harmful microbes through constitutive and inducible defence strategies. Alternatively, plants have evolved the capacity to prepare their immune system to respond faster and stronger against attackers. This so-called priming of defence can be triggered by a variety of signals that warn of an upcoming attack, including treatments with priming agents such as b-amino butyric acid (BABA). BABA has been shown to provide protection against a wide spectrum of filamentous diseases. The reason for this outstanding performance is due to its priming activity at different defence signalling pathways that are used by plants to fight diseases with different lifestyles. BABA has been shown to be effective in inducing resistance against a broad-spectrum of diseases in crops such as tomato. Filamentous pathogens are particularly problematic in this crop as they are responsible for yield loses pre- and post-harvest. Therefore, emerging filamentous diseases are a serious threat to the tomato market.
Tomato is a model plant for research in Solanaceae as its genome has been sequenced and crosses with their wild relatives allow the study of the genetics behind different processes. However, only one study in Arabidopsis has investigated genetic variation in the induced resistance response. This project will investigate genetic variation in induced resistance trigger by BABA in tomato with the overarching aim to identify advantageous traits which could potentially maximise the inducible resistance capacity of commercial varieties.
To achieve this aim, I will test BABA-induced resistance against the devastating pathogen Phytophthora infestans (late blight) in a Recombinant Inbred Line (RIL) population from the cross between a commercial tomato cultivar, and an accession of the wild relative. Induced resistance quantification will be done by using a sophisticated phenotyping scanner that can image and analyse different disease parameters in a high-throughput manner. The induced resistance traits (IR-traits) will be identified by sequencing of the significant quantitative trait loci (QTLs) and the molecular mechanisms behind the response will be investigated. The last part of the project will test the hypothesis that multi-directional resistance as a result of the IR-traits offers effective protection against newly identified strains of filamentous pathogens with a high risk of emergence, such as strains of late blight or Fusarium wilt (caused by the multi-host pathogen Fusarium oxysporum).
The results coming from this work will identify the genetic traits to exploit the tomato immune system for enhanced defence against a broad-spectrum of diseases, including emerging pathogens that can have a huge devastation potential.

Technical Summary

Agricultural systems are highly exposed to devastating attacks by emerging filamentous pathogens. Current methods of disease control depend on pesticides, increasingly regarded as unsuitable. Research that exploits the plant immune system against these biological threats provides a potential source for future disease control strategies. In addition to the innate immune system, plants have evolved the ability to adapt to hostile conditions by priming their defence mechanisms in response to hostile signals. Priming is triggered by signals that indicate an up-coming attack, including chemical priming agents such as b-amino butyric acid (BABA). BABA-induced resistance is an attractive concept for sustainable agriculture because it provides broad-spectrum resistance in a wide range of plant species, including tomato. The reason for its performance results from it priming multiple defence signalling pathways. Tomato is a host for pests and diseases that limit yield. Genetic variation in the induced resistance response has only been studied before in Arabidopsis. The overall aim of the project is to identify the induced-resistance traits (IR-traits) that maximise the induced resistance capacity of tomato to provide broad-spectrum protection against emerging filamentous diseases. I will use state-of-the-art facilities to quantitatively phenotype BABA-IR in a recombinant inbred line population against the devastating oomycete pathogen Phytophthora infestans. I will then identify and characterise the genetic and molecular mechanisms responsible for the IR-traits. Finally, I will test the hypothesis that multi-directional resistance provided by the IR-traits offers effective protection against new virulent strains of P. infestans and Fusarium oxysporum with highly emerging potential. This work will provide a revolutionary steps-ahead strategy against biological threats by exploiting the immune system to prepare for the fight against rapidly-evolved emerging pathogens.

Planned Impact

The project described in my proposal ultimately aims to find solutions to reduce the amount of pesticides in the tomato fields, thus enhancing the highly pursued agricultural sustainability. The main beneficiaries of my research are:

- Global agri-tech community:

Plant breeders. Due to their increasing unsuitability, the use of pesticides in agricultural fields has been highly legislated. In the next few years, practices need to dramatically change in order to implement new strategies that incur in lower costs for the health and environment. Upon project completion, plant breeders will benefit from having new tomato varieties available that enhance the capacity of plants to defend themselves better against emerging diseases.

Farmers. The proposed work develops technology to be implemented into Integrated Pest and Disease Management (IPM). The results will provide new strategies to reduce pesticides in greenhouse-grown tomatoes, therefore, farmers will be offered opportunities to change several agricultural practices that comply with new European regulation. The use of priming agents to boost the immune capacity of the plant will be implemented by the introduction of optimised treatments into the automatic irrigation system under greenhouse growth.

- Distributors and consumers: These two sectors will benefit from the development of new IPM strategies that will lower chemical pesticides residues and the risks of spreading emerging diseases.

- Policy makers. New cultivars and IPM strategies will ultimately provide solutions to secure food production in a sustainable manner. The use of pesticides that are under strict legislation. Therefore, the implications arising from the work described in this proposal will serve policy makers to identify and prioritise the new challenges in food security and safety.

- Global population. UK and global population directly benefit from this work as results will provide alternatives to the use of pesticides, increasingly looked down upon socially. Agriculture and food security is one of BBSRC's strategic priorities and my work will benefit from inspiring the next generations of scientists to pursue careers in plant science and agronomy, thus securing the UK intellectual investment in translational research to provide food security.
 
Description Brexit science and innovation Summit Submission
Geographic Reach National 
Policy Influence Type Contribution to a national consultation/review
URL https://sruk.org.uk/at-the-heart-of-the-brexit-debate/
 
Description Epigenetic control of long-lasting defence priming for the protection of fruit against postharvest diseases
Amount £18,593 (GBP)
Organisation Cranfield University 
Sector Academic/University
Country United Kingdom
Start 12/2021 
End 09/2022
 
Description Lamya Majid PhD iCASE studentship: Long-lasting defence priming for the protection of fruit against postharvest diseases
Amount £50,000 (GBP)
Organisation University of Warwick 
Sector Academic/University
Country United Kingdom
Start 09/2022 
End 09/2026
 
Description Midlands Integrative Biosciences training Partnership iCASE student
Amount £0 (GBP)
Organisation Midlands Integrative Biosciences Training Partnership 
Sector Academic/University
Country United Kingdom
Start 09/2019 
End 09/2023
 
Description New Investigator Award - Rank Prize Fund
Amount £20,000 (GBP)
Organisation Rank Prize Funds 
Sector Charity/Non Profit
Country United Kingdom
Start 03/2019 
End 03/2021
 
Description Organization of an International Research Symposium in Plant Pathology
Amount £1,000 (GBP)
Organisation Government of Spain 
Sector Public
Country Spain
Start 01/2019 
End 08/2019
 
Description Organization of an International Research Symposium in Plant Pathology
Amount £4,000 (GBP)
Organisation British Society of Plant Pathoogy 
Sector Learned Society
Country United Kingdom
Start 01/2019 
End 08/2019
 
Description PhD Studentship - Co-supervisor
Amount £30,000 (GBP)
Organisation University of Sheffield 
Department Grantham Centre for Sustainable Futures
Sector Academic/University
Country United Kingdom
Start 09/2017 
End 09/2021
 
Description Undergraduate Summer Bursary
Amount £2,100 (GBP)
Organisation The British Society of Plant Pathology 
Sector Charity/Non Profit
Country United Kingdom
Start 05/2017 
End 08/2017
 
Title Assessment of the effect of abscisic acid ABA in plant defence responses 
Description Machine learning model from the paper Stevens et al that has been made accessible in GitHub.: https://github.com/PlantPriming/ABAresistance 
Type Of Material Computer model/algorithm 
Year Produced 2023 
Provided To Others? Yes  
Impact We have demonstrated that the model improves its capacity to predict information when more data is fed into it and therefore we are encouraging researchers working in the topic to run the models inputting their data even when these have not been published. 
URL https://github.com/PlantPriming/ABAresistance
 
Description Collaboration with the Agri-tec company Enza Zaden 
Organisation Enza Zaden
Country United Kingdom 
Sector Private 
PI Contribution Enza Zaden initially supported my fellowship application and it has now come into the picture to provide a vehicle for application of my research findings. I have provided results obtained in a research setting that are extremely informative for them. I have supervised two postgraduate masters projects using genetic material provided by them
Collaborator Contribution My initial hypothesis in my fellowship has changed and now Enza are providing with the genetic material (tomato cultivars) that I need to test my newly formulated hypothesis. We have processed a Material Transfer Agreement for 8 tomato cultivars that show different levels of basal resistance to pathogens. They provided the hybrid lines and advice with the results obtained
Impact - Resistance and priming phenotypes in the panel of hybrid cultivars provided by them - Two masters thesis with the results that have been shared with Enza
Start Year 2018
 
Description Fusarium project 
Organisation University of Cordoba
Country Spain 
Sector Academic/University 
PI Contribution In 2017, I obtained a Marie Curie Fellowship to work with Prof. Antonio di Pietro at the University of Cordona (Spain). This fellowship is incompatible with the Future Leader Fellowship so I could not accept the grant. We however developed a collaboration that has continued for the last few months and we are going to carry out the project together through the supervision and training of students. I obtained funding for a summer student (summer 2017) that obtained some preliminary results. In 2018, I also obtained a New Investigator Award of the Rank Prize Fund. This grant supported this project as well and I hosted a PhD student from Antonio´s lab in my lab. In 2019, I will also visit the University of Cordoba for a 2-week visit to Antonio´s lab. In Autumn 2019, a student from Antonio Di Pietro's lab, Isabel Okeke, came to my lab for a 9-month research visit funded by the Rank Prize Fund. She could not complete her studentship and will come back at some point to finalise some experiments when the situation with the pandemic improves
Collaborator Contribution Antonio now has a master student working on the project and they are doing parts that I don't have the expertise for in the topic of fungal biology.
Impact This collaboration is multidisciplinary as I carry out all the plant biology whereas Antonio's group focuses in the biology of the fungus Fusarium oxysporum
Start Year 2017
 
Description H2020 Consortium 
Organisation James Hutton Institute
Country United Kingdom 
Sector Charity/Non Profit 
PI Contribution European Consortium that applied to the "Innovations in Plant Protection" call of H2020. I was part of 2 work packages and the Impact team of the proposal entitled " PRIMING THE PLANT'S SOCIAL NETWORK FOR SUSTAINABLE AND HEALTHY CROPS". The application went through the first round but it did not get funded.
Collaborator Contribution Preparation of the proposal that had 7 work packages, the impact section and the implementation section. The partners also visited the University of Sheffield in 2 occasions during the preparation of the proposal.
Impact Preparation of a research proposal. The consortium is multidisciplinary as 50% of the work packages and the research proposed in the application was carried out by members of the different institutions working in Social Sciences. Consumer perception and market readiness levels were deeply studied.
Start Year 2017
 
Description H2020 Consortium 
Organisation RWTH Aachen University
Country Germany 
Sector Academic/University 
PI Contribution European Consortium that applied to the "Innovations in Plant Protection" call of H2020. I was part of 2 work packages and the Impact team of the proposal entitled " PRIMING THE PLANT'S SOCIAL NETWORK FOR SUSTAINABLE AND HEALTHY CROPS". The application went through the first round but it did not get funded.
Collaborator Contribution Preparation of the proposal that had 7 work packages, the impact section and the implementation section. The partners also visited the University of Sheffield in 2 occasions during the preparation of the proposal.
Impact Preparation of a research proposal. The consortium is multidisciplinary as 50% of the work packages and the research proposed in the application was carried out by members of the different institutions working in Social Sciences. Consumer perception and market readiness levels were deeply studied.
Start Year 2017
 
Description H2020 Consortium 
Organisation Utrecht University
Country Netherlands 
Sector Academic/University 
PI Contribution European Consortium that applied to the "Innovations in Plant Protection" call of H2020. I was part of 2 work packages and the Impact team of the proposal entitled " PRIMING THE PLANT'S SOCIAL NETWORK FOR SUSTAINABLE AND HEALTHY CROPS". The application went through the first round but it did not get funded.
Collaborator Contribution Preparation of the proposal that had 7 work packages, the impact section and the implementation section. The partners also visited the University of Sheffield in 2 occasions during the preparation of the proposal.
Impact Preparation of a research proposal. The consortium is multidisciplinary as 50% of the work packages and the research proposed in the application was carried out by members of the different institutions working in Social Sciences. Consumer perception and market readiness levels were deeply studied.
Start Year 2017
 
Description H2020 Consortium 
Organisation Wageningen University & Research
Country Netherlands 
Sector Academic/University 
PI Contribution European Consortium that applied to the "Innovations in Plant Protection" call of H2020. I was part of 2 work packages and the Impact team of the proposal entitled " PRIMING THE PLANT'S SOCIAL NETWORK FOR SUSTAINABLE AND HEALTHY CROPS". The application went through the first round but it did not get funded.
Collaborator Contribution Preparation of the proposal that had 7 work packages, the impact section and the implementation section. The partners also visited the University of Sheffield in 2 occasions during the preparation of the proposal.
Impact Preparation of a research proposal. The consortium is multidisciplinary as 50% of the work packages and the research proposed in the application was carried out by members of the different institutions working in Social Sciences. Consumer perception and market readiness levels were deeply studied.
Start Year 2017
 
Description James Hutton / PhD Supervision 
Organisation James Hutton Institute
Country United Kingdom 
Sector Charity/Non Profit 
PI Contribution The collaboration works through the supervision of a PhD student. The project involved several techniques in the pathosystems that I am an expert in, both in tomato and in Arabidopsis. I have also performed several experiments that are going to be included in a publication currently under preparation.
Collaborator Contribution Obtained the funding and guide the project. Also first hand supervision.
Impact Publication Chitosan primes plant defence mechanisms against Botrytis cinerea, including expression of Avr9/Cf-9 rapidly elicited genes. De Vega D1§, Holden N1, Hedley P1, Luna E2* and Newton A1* (* indicates author for correspondence)
Start Year 2017
 
Description Penn State University 
Organisation Penn State University
Country United States 
Sector Academic/University 
PI Contribution I am carrying the experiments directly related to my fellowship. I moved institutions and make all efforts to obtain a new material transfer agreement.
Collaborator Contribution Prof. Majid Foolad has provided the genetic material for my experiments directed related to my fellowship. However, Prof Foolad never completed the task of sending me the RIL population needed for my experiments and has failed to sign the new MTA with the University of Birmingham.
Impact Identification of a Recombinant Inbred Line population which corresponds with objective 1 of my proposal.
Start Year 2017
 
Description Post-harvest biochemistry 
Organisation Jaume I University
Country Spain 
Sector Academic/University 
PI Contribution I have designed the project and performed preliminary experiments.
Collaborator Contribution Mass spectrometry analysis and provide experience in post-harvest biology
Impact Wilkinson et al., 2018
Start Year 2017
 
Description Post-harvest biochemistry 
Organisation University of Bordeaux
Country France 
Sector Academic/University 
PI Contribution I have designed the project and performed preliminary experiments.
Collaborator Contribution Mass spectrometry analysis and provide experience in post-harvest biology
Impact Wilkinson et al., 2018
Start Year 2017
 
Description Multilingualism event 
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 Over 120 languages are spoken in Sheffield, reflecting a diverse mix of communities that includes international students, long-established ethnic minority groups and more recently arrived refugees. Differences in language and culture can be a barrier that isolates these groups. It is known, that children are four times more likely to drop science as their career when they study in a second language. The event I organised in conjunction with the British Science Association and the Society of Spanish Researchers in the UK brought these different communities together to celebrate and learn about multilingualism, particularly the scientific theories behind it. This explored what happens in the brain as we learn and speak foreign languages; how children acquire languages so easily and the evidence that learning languages can prevent cognitive decline, such as in Alzheimer's disease.

The event was an immersive, interactive day of family-oriented activities at Weston Park Museum; a central and popular venue whose exhibits reflect Sheffield's cultural heritage. Crucially, our activities encouraged people from different language backgrounds to engage with one another, using science as a common medium and learning in the language that they understand better.

The activities included:

-Learning languages through science: simple family-friendly science experiments conducted in foreign languages to show how words/concepts can be acquired through practical application. I explained my work in Spanish.

-Presentations from guest researchers who study multilingualism, including social and cognitive consequences.

-Poster displays (including the evidence that being bilingual can combat Alzheimer's).

-Craft activities, with the chance for visitors to make a visual interpretation of what they have learnt.
Year(s) Of Engagement Activity 2018
URL https://www.facebook.com/pg/BSASheffield/photos/?tab=album&album_id=805320152990269
 
Description Personal Research website 
Form Of Engagement Activity Engagement focused website, blog or social media channel
Part Of Official Scheme? No
Geographic Reach International
Primary Audience Professional Practitioners
Results and Impact Personal research website where I describe my academic performance and also engage with industry, policy makers and the general audience.
I removed the "wordpress" from the URL and left it as lunas-research in order to focus it to my personal portfolio. As My group and results grow, I will include new sections in the website.
Year(s) Of Engagement Activity 2016,2017,2018
URL https://lunas-research.com/
 
Description Presentation "Mi Carrera Científica" 
Form Of Engagement Activity A talk or presentation
Part Of Official Scheme? No
Geographic Reach Local
Primary Audience Schools
Results and Impact I opened the Science Week at the Spanish School Vicente Cañada Blanch in London with a presentation about my work in Spanish. About 50 pupils from GCSC to the A Level years attended. My presentation went through my scientific career, how I got to work in a University in the UK and covered my work in exploiting the plant immune system to tackle filamentous diseases. I thoroughly enjoyed this activity and had a huge level of engagement from the students as they were presented with something that they did not know in the language that they understand better.
Year(s) Of Engagement Activity 2018
 
Description The Secret Life of Tomatoes at the Sheffield Food Festival 
Form Of Engagement Activity Participation in an activity, workshop or similar
Part Of Official Scheme? No
Geographic Reach Regional
Primary Audience Public/other audiences
Results and Impact Activity hosted at the Sheffield Food Festival on Sunday 28th May 2017. The title was "The Secret Life of Tomatoes" and it was organised by the British Science Association, in collaboration with other institutions, such as the Society of Spanish Researchers in the UK, The British Society for Plant pathology, The British Tomato Growers Association and The University of Sheffield.
The event was all based in the research and it was an outreach activity for the whole family: we had crafting, colouring, playdough, etc for the youngest, microscopes and a quiz for the older children and other activities targeted to parents, such as a tomato taster corner.
We had many freebies such as fluffy bugs, stickers (saying "plant Doctor") and tomato plants that were given away when completing the tomato quiz. The answers for the 10-question quiz where spread around the Sheffield Winter Gardens. This allow the public to engage in the different activities that we had lined up. The event was free and open to everyone.
The event also coincided with the British Tomato Week which served to bring the attention to the general public even more to crop research and innovation in crop biology. The general public also learnt considerably about the plant immune system.
Pictures of the event can be found here https://www.facebook.com/pg/BSASheffield/photos/?tab=album&album_id=660016174187335
And a blog post with how it went, written by one of the members of the working group can be found here http://scienceasadestiny.blogspot.co.uk/2017/05/ill-never-look-at-tomato-same-way-again.html
Year(s) Of Engagement Activity 2017
URL https://www.facebook.com/pg/BSASheffield/photos/?tab=album&album_id=660016174187335