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PIKOBODIES: Made-to-order plant disease resistance genes using receptor-nanobody fusions

Lead Research Organisation: University of East Anglia
Department Name: Sainsbury Laboratory

Abstract

PIKOBODIES is a daring project that aims to revolutionize the way we protect plants from diseases. Unlike animals, plants do not have an adaptive immune system, instead, they rely on innate receptors to detect and fend off harmful invaders. Until now, our efforts to enhance this natural defense system have had limited success, with new types of diseases often managing to overcome our engineered solutions.

However, with PIKOBODIES, we are set to change the game. We've discovered that we can use these innate plant receptors and combine them with VHH nanobodies - these are tiny but powerful parts of the antibodies found in animals like camels. This innovative fusion can activate the plant's defense mechanisms when specific disease-causing organisms are present, and can effectively make the plant resistant to the disease.

What's truly exciting about this project is that nanobodies can be designed to recognize almost any kind of molecule. This means that we can potentially engineer plant defenses against a broad spectrum of diseases, pests, and any other threats that manage to get inside plant cells.

Through this project, we'll delve deeper into understanding how Pikobodies work, and how we can improve their design and deployment. We're essentially aiming to give plants a sort of 'vaccination' system, which can adapt to different threats much like the immune systems of mammals.

By pioneering this new technology, PIKOBODIES could offer an effective and versatile way to safeguard our precious plant life from disease. This isn't just a step forward for bioengineering - it's a giant leap for protecting our global food supply.
 
Description Cell biology of NLR immune receptors 
Organisation Imperial College London
Country United Kingdom 
Sector Academic/University 
PI Contribution To understand the sub cellular localisation of NLR immune receptors both in their resting and activated states. Ibrahim, T., Yuen, E.L.H., Wang, H.Y., King, F.J., Toghani, A., Kourelis, J., Vuolo, C., Adamkova, V., Castel, B., Jones, J.D.G., Wu, C.-H., Kamoun, S. and Bozkurt, T.O. 2024. A helper NLR targets organellar membranes to trigger immunity. bioRxiv, doi: https://doi.org/10.1101/2024.09.19.613839. Madhuprakash, J., Toghani, A., Contreras, M.P., Posbeyikian, A., Richardson, J., Kourelis, J., Bozkurt, T.O., Webster, M.W., and Kamoun, S. 2024. A disease resistance protein triggers oligomerization of its NLR helper into a hexameric resistosome to mediate innate immunity. Science Advances, 10:eadr2594. Selvaraj, M., Toghani, A., Pai, H., Sugihara, Y., Kourelis, J., Yuen, E.L.H., Ibrahim, T., Zhao, H., Xie, R., Maqbool, A., De la Concepcion, J.C., Banfield, M.J., Derevnina, L., Petre, B., Lawson, D.M., Bozkurt, T.O., Wu, C.-H. Kamoun, S., and Contreras, M.P. 2024. Activation of plant immunity through conversion of a helper NLR homodimer into a resistosome. PLOS Biology, 22:e3002868.
Collaborator Contribution Our partner is an expert in plant cell biology (a real cell biologist) and has contributed to imaging NLR immune receptors.
Impact Punctate plasma membrane localisation of activated NLR proteins Organellar localisation of helper NLR proteins Perihaustorial localisation of helper NLR proteins
Start Year 2021
 
Description Collaboration with Prof. Ryohei Terauchi 
Organisation University of Kyoto
Country Japan 
Sector Academic/University 
PI Contribution Retooling rice immunity for resistance against rice blast disease The collaborator Prof. Kamoun is a world-renowned scientist in the field of plant-microbe interactions. Short visits of young Japanese scientists to Prof. Kamoun's laboratory to carry out collaborative studies will greatly enhance their career development by exposure to The Sainsbury Lab research environment and learning the cutting edge scientific researches implemented in the Kamoun Lab. Among the benefits, the visiting scientists will enhance their presentation skills by joining weekly lab meetings and journal clubs and present his/her own work. Overall, these activities will help foster the next generation scientists of Japan and enable them to build lasting connection with UK science. Development of durable blast disease resistant rice cultivars by engineering of NLRs and S-genes will greatly benefit Japanese rice production by ensuring high productivity and reducing the use of fungicide.
Collaborator Contribution Prof. Terauchi is a leading figure in rice research and has developed methods for genomics-based isolation of rice genes, e.g. MutMap. In addition, he is a leader in blast fungus having cloned and studied both rice immune receptors, such as Pik-1, and matching fungus effectors. Thus, UK team would greatly benefit from the collaboration not only from an intellectual perspective but also from the practical aspects of technology transfer, method development and exchange of biomaterial. Visits to Japan would be extremely productive as they will tap into years of expertise and knowledge about the rice blast system. Some of the proposed work, such as S-gene cloning by using rice inbred lines, would essentially be impossible in the UK as rice cannot be grown outdoors. Although the primary goal of this collaboration is on rice blast, this fungal disease has emerged as a significant problem on wheat and is a potential threat to Europe. This collaboration will help the Kamoun Lab transition to blast diseases, which has started in 2016 following the Bangladeshi wheat blast outbreak. Interactions with the Japanese collaborators would also ensure the success of the recently funded Advanced Investigator ERC award to Kamoun, which focuses on blast diseases.
Impact 33 publications per PubMed (March 2021) https://pubmed.ncbi.nlm.nih.gov/?term=kamoun%20AND%20terauchi&sort=date?=yes
 
Description Collaboration with Prof. Suomeng Dong 
Organisation Nanjing Agricultural University
Country China 
Sector Academic/University 
PI Contribution Transcriptome specialization following host-jumps in the Irish potato famine pathogen lineage The collaborator Prof. Kamoun is a world leading scientist in the field of plant-microbe interactions. Short visits of young Chinese scientists to Prof. Kamoun's group at The Sainsbury Lab to carry out collaboration will greatly enhance their career development by exposure to an outstanding research environment and cutting edge scientific research. Among the benefits, the visiting scientists will enhance their communication and presentation skills by joining weekly lab meetings and presenting their own work. Overall, these activities will help foster the next generation scientists of China and enable them to build lasting connections with UK science. More specifically, Chinese research community will access high-quality and large-scale PacBio sequencing of potato late blight genomes. The CRISPR/Cas9 tool that modified in this project will be shared with the wider Chinese Phytopathology community. Also, the open source aspects of the project would serve as an exemplar for the wider community. China is the biggest potato producer in the world yet late blight remains the number disease and problem of the Chinese potato crop. This project would ultimately provide useful information for engineering
Collaborator Contribution Nanjing Agricultural University (NAU) is the center of excellence for oomycete (Phytophthora) research in China. After joining NAU in 2014, Prof. Suomeng Dong has quickly developed into one of the most energetic new wave scientists in this field, having studied several aspects of Phytophthora gene regulation, such as discovering m6A DNA methylation and alternative splicing pathways. He received prestigious awards such as Chinese National Science Fund for Excellent Young investigator and National Thousand Youth Talents Plan. Thus, the UK team would greatly benefit from the collaboration not only from an intellectual perspective but also from the practical aspects of technology transfer, method development and exchange of biomaterial. Visits to China would be extremely productive as they will tap into years of experience with Phytophthora, notably CRISPR/Cas gene editing. The collaboration would not only benefit the Kamoun Lab but also other groups at TSL that have an interest in P. infestans, e.g. the groups of Jonathan Jones and Wenbo Ma. This project will also strengthen links between the Norwich and China, given Centre of Excellence for Plant and Microbial Science (CEPAMS)-a budding partnership between the Norwich based John Innes Centre and the Chinese Academy of Sciences (CAS).
Impact 11 joint publications per PubMed (March 2021) https://pubmed.ncbi.nlm.nih.gov/?term=kamoun+AND+dong
Start Year 2012
 
Description Collaboration with Prof. Tofazzal Islam 
Organisation Bangabandhu Sheikh Mujibur Rahman Agricultural University
Country Bangladesh 
Sector Academic/University 
PI Contribution Exchange of materials/expertise.
Collaborator Contribution Exchange of materials/expertise. Professor Islam's group is working on genomic and postgenomic analyses of wheat blast fungus, which recently emerged as a devastating pathogen of wheat in Bangladesh. He is leading a dream project titled "Mining biogold from Bangladesh"where they identified more than 600 plant probiotics potential for using as biofertilizer and biopesticides. Another important focus of Prof. Islam's group is to analyze the genomes of a number of plant probiotic bacteria potential for biocontrol of major phytopathogens and biofertilization of rice and wheat. In collaboration with Prof. Sophien Kamoun, Prof. Islam is dedicated to the promotion of open science and open data sharing (e.g., open wheat blast www.wheatblast.net) which they think very critical for rapidly addressing the emerging plant diseases.
Impact #OpenWheatBlast http://openwheatblast.net https://twitter.com/search?q=%23OpenWheatBlast&src=typd Win, J., Chanclud, E., Reyes-Avila, C.S., Langner, T., Islam, T., and Kamoun, S. 2019. Nanopore sequencing of genomic DNA from Magnaporthe oryzae isolates from different hosts. Zenodo, http://doi.org/10.5281/zenodo.2564950. Valent, B., Farman, M., Tosa, Y., Begerow, D., Fournier, E., Gladieux, P., Islam, M.T., Kamoun, S., Kemler, M., Kohn, L.M.8., Lebrun, M.H., Stajich, J.E., Talbot, N.J., Terauchi, R., Tharreau, D., Zhang, N. 2019. Pyricularia graminis-tritici is not the correct species name for the wheat blast fungus: response to Ceresini et al. (MPP 20:2). Molecular Plant Pathology, 20:173-179. Gupta, D.R., Reyes Avila, C., Win, J., Soanes, D.M., Ryder, L.S., Croll, D., Bhattacharjee, P., Hossain, S., Mahmud, N.U., Mehebub, S., Surovy, M.Z., Rahman, M., Talbot, N.J., Kamoun, S., and Islam, T. 2018. Cautionary notes on use of the MoT3 diagnostic assay for Magnaporthe oryzae Wheat and rice blast isolates. Phytopathology, in press. Islam, T., Croll, D., Gladieux, P., Soanes, D., Persoons, A., Bhattacharjee, P., Hossain, S., Gupta, D., Rahman, Md.M., Mahboob, M.G., Cook, N., Salam, M., Surovy, M.Z., Bueno Sancho, V., Maciel, J.N., Nani, A., Castroagudin, V., de Assis Reges, J.T., Ceresini, P., Ravel, S., Kellner, R., Fournier, E., Tharreau, D., Lebrun, M.-H., McDonald, B., Stitt, T., Swan, D., Talbot, N., Saunders, D., Win, J., and Kamoun, S. 2016. Emergence of wheat blast in Bangladesh was caused by a South American lineage of Magnaporthe oryzae. BMC Biology, 14:84.
Start Year 2016
 
Description Evolutionary mechanisms that equip wild potato with disease resistance against the notorious late blight pathogen (Phytophthora infestans) 
Organisation Wageningen University & Research
Country Netherlands 
Sector Academic/University 
PI Contribution Recognising the disease To defend itself the first thing the plant has to do is detect the pathogen. "The plant has receptors for this, a kind of antennas. These bind tiny pieces of Phytophthora protein, which is the signal that something is wrong. This is when the defense responses kick in. So it is very important that the plant can actually detect the disease and has the right receptors in place to activate its defences", says Vleeshouwers. These receptors are located either inside or on the surface of the cell. Receptors inside the cell are encoded by specific R genes (R stands for resistance), and potato breeders take advantage of these. They develop resistant varieties by selecting for these R genes. However, the problem is that the pathogen manages to break through that resistance, time and again. "Much less is known about the receptors on the outside, on the cell surface, the Pattern Recognition Receptors (PRRs). These receptors drive more general immune responses," Vleeshouwers says. Plant breeders are currently focusing their attention on R genes, but there is still a gap to be filled in the fundamental understanding of PRRs before the potential applications and benefits of less specific defensive responses can be explored in breeding robust disease resistance. To this end, Wageningen University & Research is cooperating with the University of Tübingen (Germany) and The Sainsbury Laboratory in Norwich (UK) to study the evolution and diversification of PRRs in potato.
Collaborator Contribution PERU Vleeshouwers explains, "We have been studying a specific type of PRR receptor called PERU. It binds a special piece of Phytophthora protein, Pep-13, which triggers the potato plant to recognise the disease. It was generally assumed that PRR receptors hardly change over time (a well-known example is the very stable receptor that recognises bacteria flagella). But we found that PERU actually exhibits dynamic evolution, and changes much faster than the more well-known PRR receptors. This is a totally new insight." According to co-research leader Thorsten Nürnberger of the Centre for Plant Molecular Biology (ZMBP) at the University of Tübingen, the research results show that the evolution of immune receptors on the cell surface of plants is much more complex than we previously thought.
Impact Sustainable cultivation This insight into this type of receptors (with more to follow) paves the way for the sustainable potato of the future. This sustainable crop could have R genes encoding for specific receptors within the cells, plus enhanced general defensive responses using PRRs on the cell surface. "Before today, breeders focused on R genes. However, the resistance they offer is constantly being thwarted. By studying how wild potato species survive in an environment where they are constantly assailed by diseases, we can discover what mechanisms they use, and then introduce these mechanisms in our own potato varieties," Vleeshouwers concludes.
Start Year 2022
 
Description Wheat Disease Early Warning Advisory System (Wheat DEWAS) 
Organisation International Centre for Maize and Wheat Improvement (CIMMYT)
Country Mexico 
Sector Charity/Non Profit 
PI Contribution CIMMYT has launched the Wheat Disease Early Warning Advisory System (Wheat DEWAS), funded through a $7.3 million grant from the Bill & Melinda Gates Foundation and the United Kingdom's Foreign, Commonwealth & Development Office, to enhance crop resilience to wheat diseases. Wheat DEWAS is designed to help safeguard wheat productivity and advance sustainable agricultural practices in collaboration with international partners, including researchers at the John Innes Centre, The Sainsbury Laboratory and GetGenome.
Collaborator Contribution Led by David Hodson from CIMMYT and Maricelis Acevedo from Cornell University, this ambitious project brings together a global team of experts. Professor Sophien Kamoun is particularly delighted to expand collaboration with CIMMYT and African scientists, developing and expanding the cutting-edge platforms for genomic surveillance of wheat pathogen. Open science and international collaborations were at the core of the successful tracing and identification of wheat blast clones after the devastating wheat disease spread to two other continents. By creating the website Open Wheat Blast, the rapid sharing of data was facilitated between researchers, which proved crucial for tracking wheat blast pathogens and ensured that all contributions were appropriately credited. This resulting publication was recently highlighted as an exemplary way of working with the Global South in an article calling for more collaborative authorship practices. GetGenome, a charitable initiative that aims to provide equitable access to genomic technologies, was inspired by these principles and is designed to enable open science and data sharing with contributions properly credited from the start.
Impact The combination of rapid identification of emerging variants together with pathotyping to assess the variants' potential to impact wheat production will inform the generation of a list of Variants of Concern. This valuable data will be shared with project partners and contribute to the deployment of effective disease management strategies.
Start Year 2023
 
Description SchoBozKa Annual Retreat 
Form Of Engagement Activity Participation in an activity, workshop or similar
Part Of Official Scheme? No
Geographic Reach Regional
Primary Audience Postgraduate students
Results and Impact The event is an annual retreat of the following labs to enable interactions between the team members and explore research avenues. This also includes a career development activity. The groups involved are Sebastian Schornack @dromius | Tolga Bozkurt @Tolga_Bzkrt | Lida Derevnina @lderevnina | Phil Carella @Phil_Carella | Jiorgos Kourelis @JiorgosKourelis
Year(s) Of Engagement Activity 2023,2024,2025
URL https://kamounlab.tumblr.com/post/776102920337915904/its-that-time-of-year-schobozka-running-strong
 
Description TSL Symposium - Plant resistance to pathogens in the face of climate change 
Form Of Engagement Activity Participation in an activity, workshop or similar
Part Of Official Scheme? No
Geographic Reach International
Primary Audience Other audiences
Results and Impact The symposium held on November 4th, 2024, in Norwich. This event marks the launch of the strategic partnership between The Sainsbury Laboratory and the Khalifa Center for Genetic Engineering and Biotechnology. Our collaboration aims to advance climate-resilient plant immunity research by uniting our expertise in plant-pathogen interactions specific to desert and dryland plants.
Year(s) Of Engagement Activity 2024
URL https://kamounlab.medium.com/opening-remarks-tsl-symposium-plant-resistance-to-pathogens-in-the-face...