Bilateral NSF/BIO-BBSRC: Modelling Light Control of Development

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

Abstract

Changes in the light environment, caused by encroaching vegetation or seasonal progression, can alter the course of development leading to a wide variety of plant architectures. This developmental "plasticity", is a defining characteristic of plants and a prerequisite for survival, allowing adaptation to an environment in flux. Adaptive responses to nearby vegetation are often crucial in the natural environment but costly in terms of yield in a field crop. Indeed, the ability to control crop architecture in dense canopy field conditions is a priority for plant breeders. Speaking to this need, the outputs from this project will generate novel targets and predictive tools that can be used to improve plant architecture in vegetation rich environments. The project aims to fill a knowledge gap: even though light constantly tunes plant development it is still unclear how this is executed at the cellular and molecular levels. A principal aim will be to establish how light signalling is coupled to development providing the first detailed understanding of how light drives plant growth plasticity.

Plants continue to grow and develop through their life cycle and so have to maintain an active stem cell pool. In the shoot, stem cells reside in the "meristem" which is located at the shoot apex. New organ (e.g. leaf) production is controlled by a suite of developmental genes that act at the shoot apex. Our earlier work and that of others showed that light controls the rate of leaf production, leaf size and morphology, suggesting light regulates meristem function. More recently we have uncovered molecular evidence that strongly reinforces this proposition. The research programme aims to delineate the molecular path from light activated signal transduction to organogenesis, providing the first account of how light directs development. To help resolve molecular connections, that may be intricate, we will employ an integrated modelling and experimental regime. This is possible as we have already developed light signalling model framework that can be extended to incorporate meristem genes. Model simulation of different pathway structures will allow us to predict new molecular connections that can be tested in the lab. This iterative process will facilitate and improve the accuracy of pathway assembly. The model will help us to determine how different light regimes alter pathway dynamics and development, providing a system level understanding of pathway behaviour. An important outcome will be the production of a developmental plasticity model with predictive capabilities: an invaluable resource for crop improvement programmes. Model development also represents an important step toward our future aim to construct a virtual plant.

Technical Summary

Through the plant lifecycle the phytochrome photoreceptors detect alterations in the light environment and propagate adaptive changes in plant architecture, yet it is unclear how this is executed at the molecular level. Our supporting data provide compelling evidence that light controls development via the Shoot Apical Meristem (SAM). HECTATE (HEC) transcription factors have recently been shown to control cell proliferation by regulating SAM genes. Our studies demonstrate that HECs operate through a Phytochrome Interaction Factor (PIF)-based mechanism, inferring a direct molecular link between PIFs and the SAM. This study will integrate experimental and theoretical approaches to: i) elucidate the molecular events through which light controls SAM function, ii) develop a new conceptual model for light signalling, and iii) provide technological advances in plant architecture manipulation for plant breeding. The project benefits from significant modelling and data storage/sharing resources offered by partner labs. An initial aim will be to extend our new light signalling model to incorporate HEC-PIF control of cell proliferation. Site directed expression, qRT-PCR and ChIP assays will establish whether PIFs operate externally or from within the SAM. The system will be characterised from the molecular to the whole plant level using methodologies including biochemical assays, time-resolved target gene expression and growth profiles. These data will be used for model parameterisation, while functional analysis will delineate the molecular links between HEC-PIF and the SAM. In silico testing of different circuit structures will aid the mapping of pathway connections and provide a means to understand the emergent properties of the network e.g. in different light conditions. The ultimate goal of the project will be to generate a molecular and systems level understanding of how light regulates organogenesis, providing a new paradigm for light signalling.

Planned Impact

Outputs from this project will include novel methods to control shoot morphology and the rate of development, traits strongly associated with crop yield. Uniquely the project will offer strategies to improve productivity in vegetation rich, field conditions. Our focus therefore aligns with a BBSRC's "Sustainable Intensification" priority to investigate methods that "produce more from the same or a smaller area of cultivated land". Project aims are likely to stimulate commercial interest, which will be pursued at an early stage to allow sufficient time to exploit and protect intellectual assets (see Pathways to Impact). This together with broad scope modelling workshops for the public, will maximise opportunities to deliver social and economic impact. Embedded in the BBSRC's Systems Approaches to the Biosciences" priority area, the project will stimulate conceptual thinking around systems modelling. A significant milestone will be the development of a robust modelling framework that predicts the impact of a changing light environment on plant development. Validated models will be made publically available through open-access University of Edinburgh and community databases. The modelling effort on project will comprise an important step toward the future aspiration to develop a digital organism.
This international partnership conforms to the BBSRC's overarching priority to encourage and support the movement of researchers between the UK and overseas (see Pathways to Impact). The US PDRA will train the UK RA in tissue-specific RNA extraction methods. In return, the US PDRA will receive tuition in methods to integrate data into models and in model simulation, through a planned sabbatical to Edinburgh. Our training exchange scheme will aid project cohesion, skill development, and assist the transfer of Systems Biology methodology to the US partner lab.

Publications

10 25 50
 
Description The phytochrome B (phyB) controlled shade avoidance response (SAR) is a pivotal adaptive growth strategy that is critical for plant survival. SAR induces dramatic metabolic and architectural changes in the growing plant, with notable modification of seedling and leaf morphology. While the early phyB signalling events have been studied in detail, very little is known of how phyB signalling is coupled to development. New knowledge has been generated as follows:

phyB regulates cell proliferation and the basic cellular machinery during leaf development. Our work has delineated the molecular mechanism through which phyB light receptor controls leaf blade cell division. New understanding also comes from the discovery that phyB plays a pivotal role in regulating basic cellular processes such as DNA replication, chromatin modification, ribosome biogenesis, translation and intracellular motility. These novel findings will stimulate new lines of investigation in the field. The study enabled training in specialist skills, including programming, software use and bioinformatics workflow operations, which have significantly increased our capabilities in the handling and interpretation of complex RNAseq timecourse data.

Dawn and photoperiodic sensing by PHYA. In collaboration with the Imaizumi lab (University of Washington, USA) we generated a new photoperiodic model that links PHYA to the circadian clock through the ELF3-PIF module (Seaton et al. PNAS 2018). Here, we demonstrate that diurnal control of PHYA transcription, combined with its unique photochemistry, make phyA a robust sensor of short photoperiods. The phyA-based "external coincidence" model provides sensitive detection of photoperiod length, and the morning-phased induction of seedling growth.

A novel molecular module that links PHYTOCHROME INTERACTING FACTOR (PIF) with developmental HECATE (HEC) Proteins. Molecular, genetic and biochemical approaches were used to uncover this previously unknown PIF-HEC mechanism that controls seedling photomorphogenesis.

New molecular processes through which the CONSTITUTIVE PHOTOMORPHOGENIC 1 - SUPPRESSOR OF PHYA (COP1-SPA) E3 ligase regulates the abundance of PIF proteins (Pham et al., Plant Journal, 2018; Pham et al., Development, 2018). Based on this work, a highlight article (http://dev.biologists.org/content/145/23/e2305) and author interview (http://dev.biologists.org/content/145/23/dev173518) were published in Development, 2018; 145 (23). Follow-on work demonstrated that SPA1 functions a serine/threonine kinase in phosphorylating PIF1 in response to light (Paik et al., Nature Communications, 2019).
Exploitation Route This is fundamental research that has opened new avenues of research for the scientific community. As the project was geared to understanding how the external light environment controls plant architecture, it is relevant to agriculture and particularly vertical farming, where plants experience dramatic spectral changes due to crowding.
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 Leverhulme Trust Research Grant
Amount £122,897 (GBP)
Funding ID RPG-2015-293 
Organisation The Leverhulme Trust 
Sector Charity/Non Profit
Country United Kingdom
Start 03/2016 
End 03/2018
 
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 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 Halliday-Imaizumi 
Organisation University of Washington
Country United States 
Sector Academic/University 
PI Contribution My lab contributed expertise in plant light signalling and modelling.
Collaborator Contribution The Imaizumi lab contributed expertise in photoperiodic flowering.
Impact Seaton DD, Smith RW, Song YH, MacGregor DR, Stewart K, Steel G, Foreman J, Penfield S, Imaizumi T, Millar AJ, Halliday KJ. Linked circadian outputs control elongation growth and flowering in response to photoperiod and temperature. Mol Syst Biol. 2015 11:776.
Start Year 2013
 
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 Author Interview 
Form Of Engagement Activity A press release, press conference or response to a media enquiry/interview
Part Of Official Scheme? No
Geographic Reach International
Primary Audience Professional Practitioners
Results and Impact Interview to Journal Development, based on scientific discoveries in (Pham et al., Development, 2018 Dec 3;145(23))
Year(s) Of Engagement Activity 2018
URL http://dev.biologists.org/content/145/23/dev173518
 
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 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 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 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 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 Press Release in Research Article 
Form Of Engagement Activity A press release, press conference or response to a media enquiry/interview
Part Of Official Scheme? No
Geographic Reach International
Primary Audience Media (as a channel to the public)
Results and Impact Press Release for Paik et al., Nature Communications, 2019, Sep 16;10(1):4216
Year(s) Of Engagement Activity 2019
URL https://cns.utexas.edu/news/discovery-gives-insight-into-how-seeds-germinate-in-response-to-light-1
 
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