Environmental modulation of plant-pathogen interactions: Molecular mechanisms and evolution

Lead Research Organisation: John Innes Centre
Department Name: Cell and Develop Biology

Abstract

To meet the demands of an increasing global population there is an urgent need to double food production worldwide by 2050. Efforts towards achieving this goal are limited by decreased availability of agricultural land as well as the current scenario of climate change. Changing climate will hamper food production through unpredictable extreme weather conditions as well as by affecting plant growth and development and accelerating crop damage due to plant diseases and pests. Most of the crop plants are increasingly susceptible to diseases at higher temperatures. Climate change, especially increasing temperatures has resulted in the geographical range expansion of plant pathogens and pests. In addition, virulent pathogens with shorter latent periods are evolving faster worldwide. These pose a major challenge to sustained agricultural productivity, let alone increasing yield. This has increased our heavy reliance on agrochemicals. To ensure food security in the changing environmental conditions, there is an urgent need to develop crop plants with a durable and climate-resilient disease resistance to enhance productivity. Efforts are also required to have sustainable agricultural practices with reduced reliance on agrochemicals that accelerate environmental damage. Plants' ability to accelerate their defense system in response to non-pathogenic microbes and certain environmental conditions through priming for rapid aviation upon pathogen infection is promising. Yield losses due to increased diseases can be reduced to a great extent through crop improvement for climate-resilient disease resistance that is not sensitive to increasing temperatures and durable resistance though enhanced priming. Though known for more than nearly a century, environmental influence on disease resistance is not sufficiently well understood for potential applicability. The proposed research will aim to study these processes - temperature induced disease susceptibility and priming - in detail and understand the molecular basis through a series of molecular biology, genetics and biochemistry approaches. A major part of the work will be to understand the genetic basis and thereby understand the underlying molecular machinery. This will be achieved through unbiased forward genetic screens. To study the evolution of temperature induced disease susceptibility and priming, I will study the natural variation using the rich Arabidopsis genetic resources. Several accessions adapted to a wide range of geographic regions and environmental conditions will be screened to define their adaptive strategies to suit the specific environment. This multidisciplinary study will thus generate a wealth of information regarding the molecular aspects of environmental regulation of plant pathogen interactions. Knowledge gathered from these studies will serve as a novel platform for improving crop plants primarily oilseed rape to have climate-resilient durable resistance. These tools could be applicable to other major crops like other brassicas, rice, wheat, potato etc. that are directly under threat of severe diseases as a consequence of climate change. The study will thus enable us to enrich our fundamental understanding of disease resistance and strategies for local adaptation by plants with a direct practical application of crop improvement.

Technical Summary

The project is aimed to understand the molecular basis and adaptive evolution of environmental modulation of plant-pathogen interactions using Arabidopsis as the discovery platform and oilseed rape as the crop model. Research will concentrate on temperature induced defense breakdown and priming of plant defense responses. The recently discovered temperature sensing machinery involving variant histone H2A.Z and related chromatin machinery have been implicated in defense responses. Systematic analyses of chromatin dynamics will be done to dissect the role of chromatin especially H2A.Z in defense gene regulation. These will define the sequence of events that leads up to defense gene activation following pathogen perception. This would be followed up to understand how higher temperature or priming will alter the standard chromatin dynamics. This will establish possible chromatin signatures associated with these phenomena. Reporter based forward genetic screens will be performed to understand the genetic basis of defense breakdown at elevated temperature and priming. Arabidopsis natural accessions will be studied to understand the natural variability in temperature dependent disease susceptibility as well as priming, and to understand various adaptive strategies and evolution of these traits in the natural environment. The ultimate objective of the project is to contribute towards crop improvement. Paradigms established in Arabidopsis will be put to test in Brassica. TILLING will be employed to generate Brassica mutants o study the link between temperature and defense. Knowledge gathered from Arabidopsis will be used to screen Brassica germplasm to select valuable breeding materials and to develop strategies for crop improvement in Brassica. These strategies if successful, could be integrated to other Brassica species and potentially to other crop systems such as cereals through active collaborations.

Planned Impact

The project aims to understand the temperature-induced susceptibility to diseases and priming of disease resistance at the molecular level, with the ultimate objective of contributing towards crop improvement for developing climate-resilient disease resistance and durable resistance through enhanced priming. Apart from the direct scientific and academic impact, the project output is expected to have a wider socio-economic impact owing to its considerable relevance to agriculture, food security and ecology. The immediate beneficiaries of the project will be the wider scientific community of biologists especially plant and agricultural scientists. Research outcomes of the projects will be timely disseminated through publications in high impact journals, seminars and workshops to make the information available for the immediate beneficiary group. Collaborations with relevant groups will be sought to synergise activities and regular meetings will facilitate information flow. Outputs from the research will broaden our fundamental understanding of plant environment interactions and will therefore accelerate new synthesis. The projects outputs will have direct impact on farmers and will be of great interest as at its core the project is dealing directly with the real impact of climate change on agriculture and crop productivity. As it could better facilitate screening of the available germplasm for traits of interest to develop new breeding material, the study will directly reach out to plant breeders, whom I will seek to collaborate with intensively. Forums such as OREGIN (Oilseed Rape Genetic Improvement Network) offer platforms to interact with the stakeholders comprising of breeders, sponsors, scientists and farmers. Enhanced resistance, especially climate resilience of resistance is a highly desirable trait in agriculture. The project will elucidate the molecular basis for environmental modulation of plant defense, hence the impact of the project will be tremendous. Agricultural biotechnology companies will benefit from the results as it could provide a novel platform for crop improvement. Any results or findings of commercial potential will be judiciously exploited. Any developed technology will be made available appropriately through PBL who will file patents and manage licensing. Since the outcomes of the project will better facilitate impact assessment of climate change on crop production, biodiversity and ecosystem services, this will have a significant impact on a broad range of stakeholders including public and private sector business and trade and policy makers. To ensure impact of the project outcomes, the generated data will be made available to the ongoing crop simulation models at the RRes and elsewhere through collaborations. Climate change and environmental issues are of great interest to the general public as well. The project will thus attract considerable public attention. Through public engagement activities like popular science events and other appropriate forums, the findings and philosophy of the research will be publicised. Sustainable food production and climate change impact mitigation requires long-term, dedicated efforts in all related areas. In addition to the scientific impetus it will bring about, the project will add to these long-term goals through training of the research professionals - postdoctoral researchers and students as potential future leaders.

Publications

10 25 50
 
Description 1. Plant defense is strongly influenced by environmental factor, particularly temperature.

2. Temperature affects plant immunity at the level of signalling and molecular responses such as gene expression.

3. Thermosensory signalling directly influences plant defense responses.

4. An unbiased genetic screen has identified 'resilient' mutants that express robust defences at elevated temperatures that are otherwise inhibitory

5. We have identified novel thermosensory pathways that integrate seasonal signals to coordinate growth and defense.
Exploitation Route We have found that temperature-induced suppression of immunity is closely coordinated with thermosensory growth through the transcription factor PIF4. Modulating temperature responsive growth could alter thermal sensitivity of defense and lea to resilient resistance. Further, our work has established that thermosensory mechanisms are conserved between Arabidopsis and oilseed rape, allowing us to modify thermosensory signalling in crops to alter thermal sensitivity of defense. In summary, this project has established a research programme addressing an important fundamental biology question of great practical relevance. We have made several key discoveries that will help elucidate the complex interaction of plants with their environment, providing us with valuable insights. Most importantly, this research has provided us with a important leads and resources for further study to advance our understanding of the phenomenon and to exploit the same for crop improvement.
Sectors Agriculture, Food and Drink

 
Description By analysing the environmental modulation of plant pathogen interactions, we have discovered a molecular mechanism that coordinates growth and plant immunity at elevated temperatures. Based on our findings, we have developed a technology to develop climate resilient resistance in crops funded by Plant Biosciences Limited. The method is currently being evaluated in crops (e.g. Oils seed rape).
First Year Of Impact 2016
Sector Agriculture, Food and Drink
Impact Types Economic

 
Description H2020 MSCA Individual Fellowship
Amount € 404,387 (EUR)
Funding ID 656995 
Organisation European Commission 
Sector Public
Country European Union (EU)
Start 09/2015 
End 08/2017
 
Description D Lucyshyn 
Organisation University of Natural Resources and Life Sciences
Country Austria 
Sector Academic/University 
PI Contribution Collaborative research on low temperature mediated regulation of plant growth and development. Genetics and molecular biology experiments.
Collaborator Contribution Collaborative research on low temperature mediated regulation of plant growth and development. Genetics and molecular biology experiments.
Impact New collaboration. No reportable outcomes yet
Start Year 2015
 
Description Ive De Smet 
Organisation Flanders Institute for Biotechnology
Country Belgium 
Sector Charity/Non Profit 
PI Contribution Collaborative research on understanding the role of protein phosphorylation in plant temperature responses. Genetics, molecular biology related to temperature responses.
Collaborator Contribution Collaborative research on understanding the role of protein phosphorylation in plant temperature responses. Molecular biology and phosphor proteomics.
Impact No reportable outcomes yet. Ongoing collaboration.
Start Year 2015
 
Description Conflict of interests: How do plants sense and integrate environmental signals. 
Form Of Engagement Activity Participation in an activity, workshop or similar
Part Of Official Scheme? No
Geographic Reach International
Primary Audience Postgraduate students
Results and Impact Invited speaker at: Thermomorphogenesis 2016, (25 - 27 August 2016), Halle, Germany.
Year(s) Of Engagement Activity 2016
 
Description Conflict of interests: How do plants sense and integrate environmental signals? 
Form Of Engagement Activity A talk or presentation
Part Of Official Scheme? No
Geographic Reach International
Primary Audience Postgraduate students
Results and Impact Invited talk at BOKU, University of Natural Resources and Life Sciences, Vienna, Austria
April 2016
Year(s) Of Engagement Activity 2016
 
Description GARNet Youtube Interview 
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 Media (as a channel to the public)
Results and Impact GARNet youtube interview about two articles published in Current Biology and Cell reports
Year(s) Of Engagement Activity 2017
URL https://www.youtube.com/watch?v=L_--vJal50A
 
Description Garnet Youtube Interview 
Form Of Engagement Activity A broadcast e.g. TV/radio/film/podcast (other than news/press)
Part Of Official Scheme? No
Geographic Reach National
Primary Audience Media (as a channel to the public)
Results and Impact Garnet Youtube Interview about a published paper in Molecular Plant
Year(s) Of Engagement Activity 2016
URL https://www.youtube.com/watch?v=w5gk21sIE9I
 
Description Invited Talk 
Form Of Engagement Activity A talk or presentation
Part Of Official Scheme? No
Geographic Reach International
Primary Audience Professional Practitioners
Results and Impact Invited talk at VIB Ghent, Belgium. Talking about the research findings of the project.
Year(s) Of Engagement Activity 2016
 
Description Invited talk at University of Potsdam: Perception and integration of environmental signals in plants. 
Form Of Engagement Activity A talk or presentation
Part Of Official Scheme? No
Geographic Reach International
Primary Audience Postgraduate students
Results and Impact Invited Talk at Institute for Biochemistry and Biology, University of Potsdam, Germany.
Year(s) Of Engagement Activity 2016
 
Description Perception and integration of environmental signals in plants 
Form Of Engagement Activity Participation in an activity, workshop or similar
Part Of Official Scheme? No
Geographic Reach International
Primary Audience Postgraduate students
Results and Impact Invited talk at: Arabidopsis 2016: Emerging Challenges in Plant Biology, Mohali, India
March 2016
Year(s) Of Engagement Activity 2016
 
Description Putting it together: How do plants sense and integrate seasonal signals? 
Form Of Engagement Activity A talk or presentation
Part Of Official Scheme? No
Geographic Reach International
Primary Audience Professional Practitioners
Results and Impact Invited talk at: Institut de Biologie de l'École Normale Supérieure (IBENS), Paris, France. This has led to the establishment of a collaboration involving scientists from France and Spain.
Year(s) Of Engagement Activity 2017