Exploiting the immune system to tackle emerging filamentous diseases in tomato

Lead Research Organisation: University of Birmingham
Department Name: Sch of Biosciences

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 - We have identified tomato genes that play an important role in resistance against filamentous diseases.
- We have identified that resistance phenotypes can be durable and reach the fruit stage as well as tomato plants. We know that this long-lasting resistance is also broad-spectrum
- We also have identified that young plants are more able to acquire immunity than mature plants and we are looking into the epigenetic mechanisms behind this
- We have identified certain key characteristics of tomato plants that determine the role of a plant hormone in defence
Exploitation Route - Data base on changes in DNA methylation in tomato plants and fruit that will be shared with the research community
- Meta-analysis on the role of ABA in defence responses
Sectors Agriculture, Food and Drink

 
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 10/2022 
End 09/2026
 
Description MIBTP studentship
Amount £30,000 (GBP)
Organisation University of Warwick 
Sector Academic/University
Country United Kingdom
Start 10/2022 
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 10/2019 
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 04/2019 
End 03/2021
 
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 David Baulcombe, Cambridge University, UK 
Organisation University of Cambridge
Country United Kingdom 
Sector Academic/University 
PI Contribution We have performed experiments with tomato transgenic lines to test the resistance of those genotypes to different pathogens
Collaborator Contribution Provided the genetic material to do the experiments
Impact - Results on the resistance phenotypes of different tomato genotypes against plant pathogens - Potential publication in the future
Start Year 2020
 
Description Collaboration with Dr Leach and Newcastle University 
Organisation University of Newcastle
Country Australia 
Sector Academic/University 
PI Contribution In 2019 we started a new project in the potato crop and resistance to P. infestans. This collaboration takes results from my fellowship in the tomato crop further as it evaluates the impact of highly virulent strains of P. infestans in different genetically different varieties of potato. We continue with this project and I co-supervised a PhD student in my lab, where we have the facilities to do the experiments with P. infestans (under an APHA licence). This student has now finished her degree and left the university. Dr Leach and myself have succesfully secured another MIBTP student (Jack Bosanquet) that has already started. In addition, together with the University of Newcastle we have applied for further funding in the form of a BBSRC Responsive Mode Project currently under revision.
Collaborator Contribution They have provided the plantations in the farm and the potato varieties. They have the expertise in the genetics of those lines whereas I have the experience in pathology
Impact - Analysis of resistance phenotypes of 25 varieties of potato - Identification of varieties that are more susceptible and more resistant for future metabolome and transcriptome analysis
Start Year 2019
 
Description Collaboration with Iain Johnston, Bergen University 
Organisation University of Bergen
Country Norway 
Sector Academic/University 
PI Contribution During the lockdown, I developed a collaboration with iain Johnston top do a meta-analysis on the role of the plant hormone ABA in resistance against plant pathogens. One of my PhD students allocated 4 months into this meta analysis and we have now published the results: Stevens et al 2023
Collaborator Contribution Assisted with the data analysis with his background in computational biology
Impact - Research publication on the role of ABA in plant defence. We aim to submit it to the journal Plant Quantitative Biology in the first semester of 2021
Start Year 2020
 
Description Collaboration with Iain Johnston, Bergen University 
Organisation University of Bergen
Country Norway 
Sector Academic/University 
PI Contribution During the lockdown, I developed a collaboration with iain Johnston top do a meta-analysis on the role of the plant hormone ABA in resistance against plant pathogens. One of my PhD students allocated 4 months into this meta analysis and we have now published the results: Stevens et al 2023
Collaborator Contribution Assisted with the data analysis with his background in computational biology
Impact - Research publication on the role of ABA in plant defence. We aim to submit it to the journal Plant Quantitative Biology in the first semester of 2021
Start Year 2020
 
Description Collaboration with the Agri-Tech Saturn Bioponics 
Organisation Saturn Bioponics Ltd
Country United Kingdom 
Sector Private 
PI Contribution I have started a collaboration with the hydroponics company Saturn Bioponics in order to continue my research in hydroponically-grown crops and to serve as the vehicle for commercialization of my results in hydroponic systems. I will provide the intellectual input and my published results in postharvest induced resistance against fungal diseases. I supervise an iCASE PhD student as main academic supervisor and also visited the Saturn facilities to replicate commercial conditions within the glasshouses of the University of Birmingham
Collaborator Contribution Saturn Bioponics have supported an iCASE studentship that has been funded and an student has been allocated. The iCASE project, through the MIBTP scheme, will receive support through facilities (greenhouse and hydroponic systems), bio-stimulants and commercial varieties of tomato and strawberry. They have also provided and installed, free of charge, a hydroponic system to do the experiments with strawberry plants in a similar setting than they do in their commercial polytunnel
Impact - Funding of an iCASE PhD Studentship through the MIBTP scheme
Start Year 2018
 
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 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 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 University of Porto - Research project and PhD supervision of Chiara Murena 
Organisation University of Porto
Country Portugal 
Sector Academic/University 
PI Contribution I supported a project internationally for the University of Porto to translate priming from tomato to strawberry. The project also has a PhD student that I co-supervise
Collaborator Contribution The project started in January 2022 and we have already had a kick-off meeting in Porto to set up the objectives of the project. Several projects meetings have taken place and the student will be visiting the University of Birmingham for a 6 month secondment from May 2023.
Impact Still no outputs
Start Year 2022
 
Description "Things I Should Know" workshop on my fellowship 
Form Of Engagement Activity A talk or presentation
Part Of Official Scheme? No
Geographic Reach National
Primary Audience Postgraduate students
Results and Impact About 30 postgraduate students and staff from the institute Rothamsted Research attended a workshop on my experience with my BBSRC future leader fellowship
Year(s) Of Engagement Activity 2021
 
Description BBSRC-EPSRC Workshop on Advanced Horticulture 
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 I was invited to attend the BBSRC-EPSRC Workshop on Advanced Horticulture that was held in Birmingham on the 25th February 2020.
I contributed with a presentation and debates with industry
Year(s) Of Engagement Activity 2020
 
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 Science in the pub presentation 
Form Of Engagement Activity A talk or presentation
Part Of Official Scheme? No
Geographic Reach International
Primary Audience Postgraduate students
Results and Impact I was invited to give a presentation about my career in the UK so far to a group of international PG students and ECR. The presentation was in a pub in the town centre of Birmingham and gathered about 30 people. I went through the different stages of my career in this country, from obtaining my PhD to securing a permanent position in a top university.
I also explained part of the science that I do.
The event was organised by the Society of Spanish Researchers in the UK
Year(s) Of Engagement Activity 2019
URL https://sruk.org.uk/events/i-was-only-meant-to-work-here-for-6-months-my-11-year-career-in-the-uk/
 
Description Visit from Multinational company Enza Zaden 
Form Of Engagement Activity A formal working group, expert panel or dialogue
Part Of Official Scheme? No
Geographic Reach International
Primary Audience Industry/Business
Results and Impact I hosted a visit to the University of Birmingham of the company Enza Zaden. Three employers of the company visited my lab and we discussed our ongoing collaboration and future steps of the project. Our ongoing collaboration has the potential to impact food producers and consumers as we are working with a panel of commercial tomato varieties on their capacity to express induced resistance
Year(s) Of Engagement Activity 2019
 
Description Workshop about my BBSRC fellowship 
Form Of Engagement Activity Participation in an activity, workshop or similar
Part Of Official Scheme? No
Geographic Reach National
Primary Audience Other audiences
Results and Impact I was invited to run a workshop at Rothamsted Research. The workshop, that lasted 2 hours and targeted ECR in the institute, was to explain the different stages in the application for a fellowship and what having a fellowship had meant to me. I also had the opportunity to talk about the research that I am doing in the fellowship as this is a centre for plant science research
Year(s) Of Engagement Activity 2020