14 ERA-CAPS PHYTOCAL: Phytochrome Control of Resource Allocation and Growth in Arabidopsis and in Brassicaceae crops

Lead Research Organisation: University of Edinburgh
Department Name: Sch of Biological Sciences

Abstract

For plants, light is a signal that carries information about the environment, and a source of energy for photosynthesis. PHYTOCAL focuses on the interaction between phytochrome signalling and photosynthesis, and seeks to understand fundamental processes that make carbon (C) and nitrogen (N) resources available for plant growth. These unexplored connections underlie plasticity, which contributes significantly to yield variability in the field. Phytochrome photochemistry is exquisitely tuned to detect spectral changes indicative of nearby vegetation. This light-activated surveillance mechanism initiates changes in plant architecture, biomass formation and the timing of reproduction: traits that are strongly linked to crop yield. These changes in growth strategy require corresponding adjustments in resource deployment, yet we have no understanding of how this is accomplished.
PHYTOCAL builds on new research from the partner labs showing that cross talk between phytochrome and carbon signalling is central to C resource use efficiency and resource conservation. A principal aim will be to determine the role of phytochrome in C resource management. PHYTOCAL will also delineate the genetic basis and impact of shading-induced N re-allocation in canopies. This trait strongly impacts on N use efficiency and stand photosynthesis, and in many crops is closely linked to yield.
PHYTOCAL will conduct a systematic study across scales, delivering mechanistic information about signal integration, time-resolved transcriptome and metabolite profiles, and quantitative information about biomass accumulation, defined as the flux of carbon to protein and cell wall components, and growth dynamics. The experimental findings will be integrated into models to test hypotheses and to gain understanding at a system level. An aim will be to build models that predict the dual action of phytochrome and photosynthesis on resource management and biomass production. PHYTOCAL will run parallel work programmes in the reference species, Arabidopsis and the closely related crop Brassica rapa. The rapid life cycle and larger resource pool of the reference species will enable us to accelerate knowledge acquisition. B. rapa brings the advantage of larger size, and allows new insights to be directly applied to a food crop.

Technical Summary

PHYTOCAL builds on new research from the partner labs showing that cross talk between phytochrome and carbon signalling is central to C resource use efficiency and resource conservation. It will test the following hypotheses: (i) phytochrome plays an influential role in coupling C resources to growth; (ii) phytochrome and photosynthesis signals cooperate to conserve night time C reserves, preventing starvation and growth arrest; and (iii) phytochrome and photosynthesis interact at dawn to delay the activation of energy costly processes until the light intensity is high enough to drive photosynthesis. PHYTOCAL will also delineate the impact and genetic basis of shading-induced N re-allocation in canopies. This trait strongly impacts on N use efficiency, and yield in many crops.
PHYTOCAL will conduct a systematic study across scales, delivering mechanistic information about signal integration, time-resolved transcriptome and metabolite profiles, and quantitative information about biomass accumulation, defined as the flux of carbon to protein and cell wall components, and growth dynamics. The experimental findings will be integrated into models to test hypotheses and to gain understanding at a system level. PHYTOCAL benefits from prior investment in modelling from partner labs: (i) a Phytochrome Signalling Model that regulates growth; and (ii) a modular Framework Model where environmental inputs (incl. light) control resource production and allocation to leaves and growth. These models will be amalgamated to produce models that predict the dual action of phytochrome and photosynthesis on resource management and biomass production.
PHYTOCAL will work in the reference species, Arabidopsis and the closely related crop Brassica rapa. The rapid life cycle and larger resource pool of the reference species will to enable us to accelerate knowledge acquisition. B. rapa brings the advantage of larger size, and allows new insights to be directly applied to a food crop.

Planned Impact

Confronted by the competing pressures of a rapidly-increasing human population, decreasing available arable land, and a climate in flux, there has perhaps never been a time where increasing crop yields has been more urgent for the global economy and the environment. This project is squarely focused on the connection between C metabolism and allocation and growth, a link that has been largely overlooked in previous efforts for yield improvement. Moreover, global increases in CO2 levels will have highly variable impacts on plants, depending on their genetics and their environment, and FACE experiments point to the allocation of C for growth and N use efficiency as a feature that will limit plant productivity in these future conditions. The data and models proposed as major milestones for this project may aid in planning for plants in both agricultural and natural settings. Seen in terms of the main focus areas of ERA-CAPS 2014, thus PHYTOCAL will provide basic insights into adaptation to a changing climate and plant responses to biotic/abiotic stress, and will establish a pipeline to accelerate the transfer of findings from a model system to a crop plant grown in the countries of all three partners, thus contributing to food security. Existing connections to biotechnology companies by the partners will be leveraged to facilitate technology transfer and new product development.

Publications

10 25 50
 
Description For plants, light is a signal that carries information about the environment, and a source of energy for photosynthesis. The PHYTOCAL project explored how light signalling and photosynthesis are coordinated to achieve carbon resource management and growth over the varied light conditions that plant experience everyday.

PHYTOCAL researchers have shown that the phytochrome light receptors control carbon resource allocation to leaves, and metabolic flux to stress metabolites, sugars and starch, a major carbon reserve in plants. Light irradiance levels, and particularly photoperiod length governs the proportion of carbon that is stored as starch. The photoperiodic mechanism, which comprises light receptor and circadian clock interactions, ensures sufficient starch is synthesised during short photoperiods to prevent starvation during long (winter) nights. In natural dawns, where light intensity rises gradually, clock rephrasing prevents carbon starvation around dawn, before photosynthesis is initiated. We have shown phytochrome is a potent modulator of the genome-wide carbon starvation response. Here phytochrome operates in concert with the clock to antagonise starvation-mediated gene expression. ELF3 (EARLY FLOWERING 3), the circadian clock evening complex component, is known to transcriptionally regulate light controlled PIF (PHYTOCHROME INTERACTING FACTOR) genes. We have learned that that ELF3 and PIFs, are regulated by the plants internal carbon status, they control the morning phase-rise in reducing sugars, the allocation to starch. The ELF3-PIF module therefore fulfils an important role in coupling carbon resource availability to growth.

The project has validated B. rapa as a crop model with a conserved phytochrome-carbon network. This work showed that elevated CO2 has a dramatic impact on B. rapa growth and resource allocation, and that BrphyB is a centrally positioned regulator of these CO2-elicited responses. We exploited the upright stature of B. rapa to document the dynamic transcriptome-level changes that occur in canopy leaves that have been occluded from light. Our data showed that occlusion strongly induced genes involved in autophagy, catabolism and leaf senescence, and supressed genes involved in photosynthesis, metabolism and translation. These findings indicate that leaf masking, which occurs frequently in nature, drives a shift from carbon fixation and nutrient acquisition toward redistribution of cellular resources. We established that BrphyB signalling contributes to this reprogramming by regulating processes including translation, peptide and cellular biosynthesis. Further, BrphyB action is important for photosynthetic machinery recovery when covered leaves are re-exposed to light. PrphyB therefore contributes to dynamic carbon-resource allocation during and after canopy leaf shading.

Model-based analysis has generated new conceptual insights into how the light and clock pathways control metabolism and growth. For instance, we established that the sizeable impact of phytochrome action on final plant biomass is determined solely at the seedling stage. This work points to the critical role of phytochrome during seedling establishment, and setting the initial pace of biomass accumulation. We have generated a new photoperiodic model that links PHYA to the circadian clock through the carbon responsive ELF3-PIF module. This phyA-based "external coincidence" model provides sensitive detection of photoperiod length, and the induction of (secondary metabolite) flavonoid pathway gene expression, specifically in short days.
Exploitation Route Our findings provide a basic strategy to maximise plant/crop biomass and to improve resilience to abiotic stresses.
Sectors Agriculture, Food and Drink

 
Description Plant Health Centre
Geographic Reach National 
Policy Influence Type Participation in a advisory committee
Impact Advice to government on Ash die back, disease transmission from imported plants. Capabilities to respond rapidly to urgent situations that arise from plant/habitat contamination or disease threats.
URL https://www2.gov.scot/planthealth
 
Description Scottish Consortium for Rural Research - SCRR
Geographic Reach National 
Policy Influence Type Participation in a advisory committee
Impact SCRR provides information and advice to Scottish policy makers that work closely with government.
URL http://www.scrr.ac.uk/
 
Description Plant Health Centre
Amount £12,000 (GBP)
Organisation Government of Scotland 
Sector Public
Country United Kingdom
Start  
 
Description eBase: Evidence-Base; growing the Big Grant Club
Amount £582,054 (GBP)
Funding ID EP/S012087/1 
Organisation Engineering and Physical Sciences Research Council (EPSRC) 
Sector Public
Country United Kingdom
Start 12/2018 
End 11/2020
 
Title 13C labelling to measure protein turnover 
Description Refined 13CO2 labelling and mass spectrometric analysis was used to measure the rates of protein synthesis and degradation (Ishihara et al Plant Journal 2017 Aug;91(3):416-429) 
Type Of Material Technology assay or reagent 
Year Produced 2017 
Provided To Others? Yes  
Impact Improved method for measuring carbon flux to proteins in biologically-relevant conditions 
 
Title Enzymatic metabolite assays 
Description Quantifying metabolite abundance by enzymatic assays - developed by project members (Mengin et al, Plant Cell Environ. 2017 Nov;40(11):2608-2627) 
Type Of Material Technology assay or reagent 
Year Produced 2017 
Provided To Others? Yes  
Impact Simplified assays for measurement of selected indicator metabolites 
 
Title Supporting data for "A photometric stereo-based 3D imaging system using computer vision and deep learning for tracking plant growth" 
Description Tracking and predicting the growth performance of plants in different environments is critical for future crop development, which is under dual pressure from population expansion and global climate change. Automated approaches for image capture and analysis have allowed for substantial increases in the throughput of quantitative growth trait measurements compared to manual assessments. Recent work has focused on adopting computer vision and machine learning approaches to improve the accuracy of automated plant phenotyping. Here we present PS-Plant, a low-cost and portable 3D plant phenotyping platform based on an imaging technique novel to plant phenotyping called photometric stereo (PS). We calibrated PS-Plant to track the model plant Arabidopsis thaliana throughout the day-night (diel) cycle and investigated growth architecture under a variety of conditions to illustrate the dramatic effect of the environment on plant phenotype. We developed bespoke computer vision algorithms and assessed available deep neural network architectures to automate the segmentation of rosettes and individual leaves, and extract basic and more advanced traits from PS-derived data, including the tracking of 3D plant growth and diel leaf hyponastic movement. Furthermore, we have produced the first PS data set, which includes 221 manually annotated Arabidopsis rosettes that were used for training and data analysis (1768 images in total). PS-Plant is a powerful new phenotyping tool for plant research that provides robust data at high temporal and spatial resolutions. The system is well-suited for small and large-scale research and will help to accelerate bridging of the phenotype-to-genotype gap. 
Type Of Material Database/Collection of data 
Year Produced 2019 
Provided To Others? Yes  
 
Description Photoperiod model 
Organisation University of Washington
Department Department of Biochemistry
Country United States 
Sector Academic/University 
PI Contribution Building on our earlier joint publication (Seaton et al., Mol Syst Biol. 2015 Jan 19;11(1):776), we have continued to expand our understanding of photoperiodic mechanisms. We have contributed data, plus expertise in light signalling and modelling.
Collaborator Contribution The Imaizumi lab have contributed data and expertise on the circadian oscillator.
Impact An earlier collaboration led to the publication of Seaton et al., Mol Syst Biol. 2015 Jan 19;11(1):776. This more recent collaboration has culminated in a manuscript that we are in the final stages of preparation.
Start Year 2015
 
Description Plant Health Centre 
Organisation Biomathematics and Statistics Scotland (BioSS)
Country United Kingdom 
Sector Public 
PI Contribution Advice and guidance on environmental/abiotic impacts on plant growth and health.
Collaborator Contribution Work cross-disciplinary to solve problems relating to Scottish plant health. Pool expertise and provide advice to policy makers.
Impact ongoing - advice to government on Ash die back, disease transmission from imported plants. Disciplines- plant breeding, disease specialists, mathematical modellers, social scientists
Start Year 2018
 
Description Plant Health Centre 
Organisation Forest Research
Country United Kingdom 
Sector Public 
PI Contribution Advice and guidance on environmental/abiotic impacts on plant growth and health.
Collaborator Contribution Work cross-disciplinary to solve problems relating to Scottish plant health. Pool expertise and provide advice to policy makers.
Impact ongoing - advice to government on Ash die back, disease transmission from imported plants. Disciplines- plant breeding, disease specialists, mathematical modellers, social scientists
Start Year 2018
 
Description Plant Health Centre 
Organisation James Hutton Institute
Country United Kingdom 
Sector Charity/Non Profit 
PI Contribution Advice and guidance on environmental/abiotic impacts on plant growth and health.
Collaborator Contribution Work cross-disciplinary to solve problems relating to Scottish plant health. Pool expertise and provide advice to policy makers.
Impact ongoing - advice to government on Ash die back, disease transmission from imported plants. Disciplines- plant breeding, disease specialists, mathematical modellers, social scientists
Start Year 2018
 
Description Plant Health Centre 
Organisation Royal Botanic Garden Edinburgh (RBGE)
Country United Kingdom 
Sector Charity/Non Profit 
PI Contribution Advice and guidance on environmental/abiotic impacts on plant growth and health.
Collaborator Contribution Work cross-disciplinary to solve problems relating to Scottish plant health. Pool expertise and provide advice to policy makers.
Impact ongoing - advice to government on Ash die back, disease transmission from imported plants. Disciplines- plant breeding, disease specialists, mathematical modellers, social scientists
Start Year 2018
 
Description Plant Health Centre 
Organisation Science and Advice for Scottish Agriculture
Country United Kingdom 
Sector Public 
PI Contribution Advice and guidance on environmental/abiotic impacts on plant growth and health.
Collaborator Contribution Work cross-disciplinary to solve problems relating to Scottish plant health. Pool expertise and provide advice to policy makers.
Impact ongoing - advice to government on Ash die back, disease transmission from imported plants. Disciplines- plant breeding, disease specialists, mathematical modellers, social scientists
Start Year 2018
 
Description Plant Health Centre 
Organisation Scotland's Rural College
Country United Kingdom 
Sector Academic/University 
PI Contribution Advice and guidance on environmental/abiotic impacts on plant growth and health.
Collaborator Contribution Work cross-disciplinary to solve problems relating to Scottish plant health. Pool expertise and provide advice to policy makers.
Impact ongoing - advice to government on Ash die back, disease transmission from imported plants. Disciplines- plant breeding, disease specialists, mathematical modellers, social scientists
Start Year 2018
 
Description Plant Health Centre 
Organisation University of Strathclyde
Country United Kingdom 
Sector Academic/University 
PI Contribution Advice and guidance on environmental/abiotic impacts on plant growth and health.
Collaborator Contribution Work cross-disciplinary to solve problems relating to Scottish plant health. Pool expertise and provide advice to policy makers.
Impact ongoing - advice to government on Ash die back, disease transmission from imported plants. Disciplines- plant breeding, disease specialists, mathematical modellers, social scientists
Start Year 2018
 
Description Toledo-Ortiz Collaboration 
Organisation Lancaster University
Department Department of Physics
Country United Kingdom 
Sector Academic/University 
PI Contribution We sought and were awarded funding from the Leverhulme Trust to support this joint venture
Collaborator Contribution new research findings and expertise
Impact We are preparing a research manuscript that describes our joint findings
Start Year 2015
 
Description Cold Spring Harbor Asia Conference (S. Korea), Plant Cell & Developmental Biology 
Form Of Engagement Activity A talk or presentation
Part Of Official Scheme? No
Geographic Reach International
Primary Audience Professional Practitioners
Results and Impact Platform presentation disseminating research findings
Year(s) Of Engagement Activity 2019
URL https://meetings.cshl.edu/CSHAsia/
 
Description ERA-CAPs Award holders meeting 
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 Sharing project aims and objectives with the other ERA-CAPs awardees and the funding agencies.
Year(s) Of Engagement Activity 2015
 
Description Edinburgh Plant Science Network- Meeting series 
Form Of Engagement Activity A formal working group, expert panel or dialogue
Part Of Official Scheme? No
Geographic Reach Local
Primary Audience Other audiences
Results and Impact I am Director of Edinburgh Plant Science (EPS), a body that aims to bring plant scientists and social together to participate in strategic research. EPS is committed to delivering fundamental and translational research, education and outreach to ensure that new discoveries bring benefits for human health, society and the environment.

Edinburgh Plant Science assembles over 600 plant scientists and social scientists that collectively provide wide-ranging expertise and capability in food security, environmental sustainability and related policy. Since the launch in June 2015 EPS activities have brought in >£2M in joint grant funding.
Year(s) Of Engagement Activity 2015,2016,2017
URL http://www.edinburghplantscience.com/
 
Description Equate Scotland - Gender Equality Event, Playfair Library Old College University of Edinburgh 
Form Of Engagement Activity A talk or presentation
Part Of Official Scheme? No
Geographic Reach Regional
Primary Audience Other audiences
Results and Impact Equate Scotland event to discuss gender equality in the workplace. Broad audience- academics, students, general public.
Year(s) Of Engagement Activity 2017
URL http://www.equatescotland.org.uk/
 
Description GCRF Impact Accelerator Award meeting, Niarobi 
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 GCRF-inspired meeting in Nairobi, 2017 to build collaborations based on translating our research findings to crops. The meeting focuses on how we can utilise genetic / imaging / surveillance and modelling methods to improve crop yield in arid or changeable environments in sub-Saharan Africa.
Year(s) Of Engagement Activity 2017
 
Description ISPP Conference, Japan, 2018 
Form Of Engagement Activity A talk or presentation
Part Of Official Scheme? No
Geographic Reach International
Primary Audience Professional Practitioners
Results and Impact Presented Research findings at the International Symposium of Plant Photobiology, Shimane, Japan, 14-19 January 2018
Year(s) Of Engagement Activity 2018
 
Description International Symposium on Plant Photoiology 
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 Schools
Results and Impact Participation in project with local art-school students from Barcelona. Scientists were interviewed by students about their journey as a scientists and boundaries they had experienced.
Year(s) Of Engagement Activity 2019
URL https://www.youtube.com/watch?v=OKMu0ws2vKY&list=PLbGP88SHZ9vylz-6z56owDjoIrL2lZFo9
 
Description International Symposium on Plant Photoiology 
Form Of Engagement Activity A talk or presentation
Part Of Official Scheme? No
Geographic Reach International
Primary Audience Professional Practitioners
Results and Impact Plenary Talk. Presentation of research findings to academic audience. Panel discussion inviting input from audience.
Year(s) Of Engagement Activity 2019
URL https://www.ispphotobiology2019.com/
 
Description Phytocal Project Workshop Golm 
Form Of Engagement Activity Participation in an activity, workshop or similar
Part Of Official Scheme? No
Geographic Reach International
Primary Audience Study participants or study members
Results and Impact Join Phytocal project workshop (June 2017) hosted by Professor Mark Stitt at Max Planck Institute of Molecular Plant Physiology, Golm
Year(s) Of Engagement Activity 2017
 
Description Plant Biology Conference Halle, Germany 
Form Of Engagement Activity A talk or presentation
Part Of Official Scheme? No
Geographic Reach International
Primary Audience Professional Practitioners
Results and Impact Research presented at the Thermomorphogenesis Conference, Halle, Germany, 25-27 August 2016.
Year(s) Of Engagement Activity 2016
 
Description Royal Society London- Parent Carer Scientist Launch 
Form Of Engagement Activity Participation in an activity, workshop or similar
Part Of Official Scheme? No
Geographic Reach National
Primary Audience Study participants or study members
Results and Impact The Royal Society Parent-Carer-Scientist Launch aimed to raise awareness that science drives huge benefits from a diverse workforce. The event, was attended by scientists, their families and friends. It celebrated the best UK science, while highlighting the challenges that many scientists have in managing other matters such as disability and/or caring responsibilities. Several of the attendees were interviewed by the BBC and other press outlets.
Year(s) Of Engagement Activity 2016
URL https://royalsociety.org/topics-policy/diversity-in-science/parent-carer-scientist/
 
Description SIGNAT Conference Chile 
Form Of Engagement Activity A talk or presentation
Part Of Official Scheme? No
Geographic Reach International
Primary Audience Professional Practitioners
Results and Impact Present research findings at International SIGNAT Conference, Santiago, Chile, 30th November - 2nd December 2017.
Year(s) Of Engagement Activity 2017
 
Description Scientific Conference - Barcelona, Spain 
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 Talk delivered on project findings and future directions. The talk stimulated discussion on several novel lines of research that we are pursuing on project. The aim was to open dialogue around our new hypotheses and new ways of thinking in the scientific field of plant light signalling.
Year(s) Of Engagement Activity 2016
 
Description Scientific Conference - Gelveston, Texas USA 
Form Of Engagement Activity A talk or presentation
Part Of Official Scheme? No
Geographic Reach International
Primary Audience Other audiences
Results and Impact Scientific conference where project findings were presented to an audience that mainly comprised scientists in the field
Year(s) Of Engagement Activity 2016
URL https://www.grc.org/programs.aspx?id=14420
 
Description Scientific Conference - Halle, Germany 
Form Of Engagement Activity A talk or presentation
Part Of Official Scheme? No
Geographic Reach International
Primary Audience Other audiences
Results and Impact Talk delivered on using mathematical modelling approaches to understand complex signalling pathway behaviour. The talk stimulated discussion on the utility of modelling methods in testing hypotheses and predicting pathway and whole plant responses. In this conference the focus was on the influence of temperature on plant signalling, metabolism and development.
Year(s) Of Engagement Activity 2016
 
Description Scientific workshop - Dundee, UK 
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 Local Plant Science meeting. Plant scientists from around Scotland delivered talks with a view to sharing ideas and initiating new collaborations.
Year(s) Of Engagement Activity 2016
 
Description Utrecht Summer School 
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 Delivered seminar and ran workshop in the Utrecht summer school. Main audience: postgraduate students
Year(s) Of Engagement Activity 2019
URL https://www.utrechtsummerschool.nl/
 
Description XII Chilean Plant Biology Conference, Chile 
Form Of Engagement Activity A talk or presentation
Part Of Official Scheme? No
Geographic Reach International
Primary Audience Professional Practitioners
Results and Impact Research findings presented at the XII Chilean Plant Biology Conference (Chilean Society of Plant Biologists), Villarrica, Chile, December 4-7, 2017.
Year(s) Of Engagement Activity 2017
 
Description Young Researchers Symposium on Plant Photobiology 
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 Plenary presentation and workshop lead. Audience: early career scientists, incl. postdocs, PhD students, some undergraduates.
Year(s) Of Engagement Activity 2020
URL http://www.bio.uni-freiburg.de/YRSPP2020