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Mechanisms and functions of photosynthetic entrainment of the Arabidopsis circadian clock

Reference	BB/M006212/1
Principal Investigator / Supervisor	Professor Alex Webb
Co-Investigators / Co-Supervisors	Professor Ian Henderson, Professor Julian Hibberd, Dr Philip Wigge
Institution	University of Cambridge
Department	Plant Sciences
Funding type	Research
Value (£)	416,244
Status	Completed
Type	Research Grant
Start date	01/10/2015
End date	30/09/2018
Duration	36 months

Abstract

We have identified a new pathway by which endogenous sugars produced by photosynthesis entrain the circadian clock of Arabidopsis. Our new finding provides opportunity for insight in to circadian regulation, sugar signalling and the maximisation of growth and minimisation of starvation. We will use a multidisciplinary approach to investigate why the circadian clock entrains to sugar signals, the advantages this confers and the molecular machinery responsible. Our research plan can be considered in three main parts 1. Determining the contribution of photosynthetic entrainment to circadian behaviour through studies in mutant backgrounds and in environmental regimes that manipulate photosynthetic and light signalling entrainment mechanisms. 2. Obtaining a theoretical understanding of whether photosynthetic entrainment enhances circadian performance, carbon metabolism or both, through mathematical analysis. We will perform analysis and simulation in a model of the inter-regulation of the circadian clock and carbon metabolism. The major predictions of these studies will be tested by experimental analyses of circadian rhythms, starvation and growth. 3. We will investigate the molecular basis of photosynthetic entrainment through studies of signalling and the regulation of the PRR7 promoter. We will identify if the entrainment of the circadian clock involves known sugar signalling pathways, transcriptional regulators and/or calcium signalling. Since we have previously determined that the PRR7 gene is critical for sensing of the sugars by the circadian clock, we will examine if sugar regulates PRR7 transcription through alterations in chromatin state. We will determine if photosynthetic entrainment of the circadian clock is cell autonomous or if sugars diffuse to couple circadian oscillators. This multidisciplinary study combines the strengths of researchers in the fields of circadian clocks, photosynthesis, mathematical modelling, chromatin and transcription.

Summary

The circadian clock is a 24 h timing device that controls daily rhythms of activity. In plants, the circadian clock regulates photosynthesis, growth and most aspects of metabolism and development to confer a competitive advantage. We have identified a new pathway in which the sugars made by photosynthesis, the defining metabolic pathway of plants, adjust the timing of the plant circadian clock to ensure that the rhythms of the plant are correctly matched to the local day/night cycle. This newly identified process defines a metabolic dawn. We wish now to understand the machinery by which the metabolic dawn occurs and understand why the circadian clock is adjusted by the sugars made by photosynthesis. We will perform experimental studies aimed at understanding the consequence for the circadian clock when the plant is prevented from responding to sugars produced by photosynthesis. We will find out if the daily cycle of sugars is sufficient alone to ensure correct timing of the circadian clock by perform experiments in conditions and mutant plants which prevent the normal light signalling pathways from operating. Using similar approaches to manipulate photosynthesis, we will study how well circadian rhythms are matched to the local day and night environment when photosynthesis is inhibited. This will inform about the contribution of photosynthetic entrainment to the functioning of the entire circadian clock. We will partner with researchers in Japan to create mathematical descriptions of the regulation of the circadian clock by sugars and the reverse process in which the circadian clock regulates the abundance of sugars. The mathematical analyses will determine if the response of the circadian clock to sugar is primarily to improve circadian clock performance or optimizes plant carbon usage. The predictions of the mathematical models will provide new avenues for experimental testing that would not be arrived at by intuition alone. We will perform experimental studies to investigate the machinery by which sugars regulate the circadian clock. We investigate whether the genes already known to be involved in other responses of plants to sugars are also involved in the regulation of the circadian clock. We will determine whether sugars regulate gene expression by causing chemical modifications of DNA-binding proteins. We will perform experiments to determine if the calcium ion and calcium-binding proteins are involved in the regulation of the circadian system by sugars. We will inhibit photosynthesis in specific cell-types to determine if sugar signals diffuse through the plant to regulate the circadian clock in neighbouring cells. To perform this work we have formed a team of researchers with skills in circadian rhythms, chemical modification of DNA-binding proteins, photosynthesis and mathematics.

Impact Summary

WHO WILL BENEFIT? (1) Academic scientists interested in circadian rhythms and the growth and carbon metabolism of plants (2) Industrial scientists interested in growth and carbon storage. (3) Research staff. (4) The general public. HOW WILL THEY BENEFIT? (1) Academic scientists will benefit because we aim to make conceptual advances in understanding the regulation of circadian clocks. Other theoretical and experimental research has the potential to unlock new directions in circadian biology and also in the study of the regulation of growth. We place emphasis in this research programme in gaining insight in to why the circadian system is regulated by sugars and the benefits this confers to the organism. We will ensure maximum impact by publishing our research in a timely manner. The applicants have a track record of publishing in high impact journals and widespread dissemination. (2) Industrial scientists will benefit because our work focuses on two of the major regulators of yield, the circadian clock and growth. Our focus on conceptual understanding of the relationship between carbon metabolism, growth and the circadian clock underpins applied research in the Agribusiness. We are transferring knowledge from our fundamental studies to our industrial partners e.g. Bayer CropScience (Webb) and Syngenta (Henderson). Monsanto reported that modest alterations in the dynamical behaviour of the circadian oscillator results in a 5% increase in soya bean yield under field conditions. (3) The PDRA will gain considerable benefit from being employed on the project. This will include training in circadian entrainment and sugar signalling. The practical training in molecular biology of gene regulation and physiology will place the PDRA in a good position for a further career in academia or the industry. The interface with theoretical biologists in Japan will provide the PDRA with broad scientific and cultural horizons. PDRAs from the Webb laboratory have had excellent careeradvancement. All BBSRC-funded PDRAs in the Webb laboratory have obtained publications in Science or Nature and eight former members of the Webb laboratory have obtained Faculty positions. (4) The general public will benefit from outreach activities at the Department of Plant Sciences, Cambridge. During Science Week numerous interactive and more formal displays on aspects of plant biology and research are presented and 2,000 - 5000 visit the Plant Sciences displays on 'Science Saturday' which will include dissemination of findings from this project. Webb has developed a website describing the function of the circadian clock and a road show that demonstrates how biological oscillators regulate complex behaviours in plants. This interactive display includes movies, interactive web pages and practical demonstrations using chocolates and string. We take every opportunity to publicise our findings, Dr Webb has appeared on Radio interviews (e.g. BBC Farming Today) and his recent findings have been summarised in media outlets as diverse as the Financial Times and Comedy Central's Colbert Report. It is hoped in the long term that the public will benefit from food security generated from the novel agricultural products that arise either directly or indirectly from our findings. Whilst recognising that in any field of study the translation rate from laboratory finding to industrial product is always low, we make every effort with our industrial partners (Bayer Cropscience) to translate our findings for public benefit.

Committee	Research Committee B (Plants, microbes, food & sustainability)
Research Topics	Plant Science
Research Priority	X – Research Priority information not available
Research Initiative	X - not in an Initiative
Funding Scheme	X – not Funded via a specific Funding Scheme

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