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The role of circadian oscillators in temperature responses of wheat

Reference	BB/W001209/1
Principal Investigator / Supervisor	Professor Alex Webb
Co-Investigators / Co-Supervisors	Professor Ian Henderson, Dr James Locke
Institution	University of Cambridge
Department	Plant Sciences
Funding type	Research
Value (£)	784,154
Status	Current
Type	Research Grant
Start date	01/02/2022
End date	31/01/2025
Duration	36 months

Abstract

Temperature effects on crops are important considerations for breeding. In Arabidopsis, temperature responses are modulated by the circadian clock, partly by EARLY FLOWERING (ELF3). ELF3 is co-expressed at dawn with LUX and ELF4 to form an evening complex (EC) of proteins in the clock. LUX DNA-binding activity is regulated by ELF3 and ELF4 binding. ELF3 function depends on temperature-dependent condensation because of poly Q and prion-like protein domains. Wheat ELF3 is unlikely to form an EC because it is expressed at dawn, unlike LUX which is expressed at dusk and ELF4 is absent. Also, wheat ELF3 might not be temperature-dependent because it lacks poly Q and prion-like domains. We will answer the question of how does the clock function in wheat and what is the consequence for temperature responses by making a mathematical model derived from time series RNAseq. Experiments performed in wheat ELF3 mutants will determine if ELF3 contributes to regulation of gene expression. Temperature regulation of the clock will be incorporated into the model based on data describing temperature regulation of transcript abundance. Modelling experimental data, including phase response curves in mutant lines, will describe the mechanistic basis of temperature entrainment of the wheat clock. Complementation in Arabidopsis mutants and imaging studies will determine if wheat ELF3 has temperature-dependent functions and condensation. We will discover if an EC is likely to form in wheat using FRET. Knowledge from the mathematical models will be used to inform experiments in wheat mutants to investigate the circadian regulation of temperature stress responses. We will model the circadian regulation of thermosensitive growth in wheat to understand how the clock contributes to growth. Our combined theoretical and experimental work will describe the function of a wheat gene regulatory network in growth and temperature responses which will inform breeders in trait selection.

Summary

Due to climate change we need to understand the basic biology of temperature responses of crop plants. The Webb lab contributed to the discovery that one regulator of temperature responses is the circadian clock, which controls the timing of events in plants. We have found differences between the circadian clocks in the model plant Arabidopsis and wheat, the UK's major crop. The differences are in a protein called EARLY FLOWERING 3 (ELF3), which might affect the circadian clock and temperature responses. In Arabidopsis, ELF3 binds LUX ARRHYTHMO (LUX), a DNA binding protein that regulates genes. ELF3-LUX are also bound by ELF4 to form an evening complex of proteins to regulate the circadian clock and temperature responses due to temperature-sensitive prion-like domains in ELF3. At higher temperatures ELF3 condensates and cannot bind LUX. We have found wheat ELF3 is unlikely to bind LUX because they are made at different times, LUX at dusk and ELF3 at dawn. Wheat ELF3 might not contribute to temperature sensing because it lacks temperature-sensitive domains. These differences mean that it is not possible to transfer knowledge from Arabidopsis to wheat to predict how the circadian clock functions, nor how wheat growth is regulated by temperature. We will describe the structure of the wheat circadian clock and how it contributes to temperature responses to provide information about gene function for breeders to identify targets for improved wheat in a changing climate. To understand the wheat circadian clock, we will make a mathematical model based on the timing of gene activity. We will model temperature effects on the circadian clock from data describing the abundance clock components at different temperatures. A full understanding of the effect of temperature on the wheat circadian clock will be achieved by testing the predictions of the mathematical models of the wheat circadian clock by experimentation. If we find deviation between the models and the data, the model will be refined to incorporate new information. The refined model will be used to design experiments that inform how temperature cycles set the timing of the circadian clock in wheat. We will perform a number of experiments to understand if wheat ELF3 has similar or different function to Arabidopsis: we will measure gene activity in wheat plants with and without functional ELF3 to discover whether ELF3 regulates gene expression as it does in Arabidopsis, and if similar genes are regulated; we will discover if wheat ELF3 protein can fulfill the functions of the Arabidopsis protein in Arabidopsis lacking functional ELF3; we will determine if wheat ELF3 forms a protein complex with LUX and discover if wheat ELF3 protein function and solubility are affected by temperature. Webb contributed to the discovery that responses to cold stress depends on the time of the day due to the circadian clock. We will investigate if that is also the case in wheat to determine if circadian clock genes might be useful targets for breeding tolerance to the extreme stresses expected in the changed environment. Lastly, we will attempt understanding how much the wheat circadian clock contributes to thermosensitive growth by connecting our mathematical model of the circadian clock with the daily growth of wheat. We have put together a multi-skilled team of experts in circadian rhythms, mathematical modelling and analysis of genomes to achieve an understanding of the mechanisms that occur during temperature resetting of the clock and temperature regulation of wheat growth. We will share the mathematical models and data in open formats to allow those working on other aspects of wheat biology to use the information and incorporate the models into larger models of wheat growth. The goal is to provide basic biological understanding that can be used to develop improved wheat varieties.

Committee	Research Committee B (Plants, microbes, food & sustainability)
Research Topics	Crop Science, Plant Science, Systems Biology
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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