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Molecular basis of polyglutamine-modulated ELF3 phase change in Arabidopsis temperature response

Richard J. Lindsay, View ORCID ProfilePhilip A. Wigge, Sonya M. Hanson
doi: https://doi.org/10.1101/2023.03.15.532793
Richard J. Lindsay
1Center for Computational Biology and Center for Computational Mathematics, Flatiron Institute, Simons Foundation, 162 5th Ave, New York, NY 10010, USA
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Philip A. Wigge
2Leibniz-Institut für Gemüse- und Zierpflanzenbau, Großbeeren, Germany
3Institute of Biochemistry and Biology, University of Potsdam, Potsdam, Germany
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Sonya M. Hanson
1Center for Computational Biology and Center for Computational Mathematics, Flatiron Institute, Simons Foundation, 162 5th Ave, New York, NY 10010, USA
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  • For correspondence: shanson@flatironinstitute.org
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ABSTRACT

Temperature is a major environmental variable influencing the distribution and behavior of plants. Recent advances have led to the identification of a role for the circadian clock in sensing temperature in Arabidopsis thaliana. Elongation growth and flowering are accelerated at warmer temperatures, and these effects are mediated by the circadian clock gene EARLY FLOWERING 3 (ELF3). ELF3 exists with a tripartite protein complex called the Evening Complex (EC) that functions as a DNA transcription repressor targeting growth-related genes. ELF3, a large scaffold protein with disordered domains, binds to the transcription factor LUX ARRYTHMO (LUX) and ELF4 to form the EC. A crucial feature of ELF3 is that it acts as a highly sensitive thermosensor that responds directly and rapidly to small increases of temperature of about 5 ºC and is rapidly reversible. At temperatures of about 22 ºC and below, the EC is active, binding and repressing the promoters of multiple growth promoting genes, reducing their expression and cell elongation. At around 27 ºC and above ELF3 undergoes rapid and reversible phase change and protein condensate formation. This temperature-dependent activity causes EC occupancy on target genes to decrease at 27 ºC, allowing their increased expression. A C-terminal prion-like domain (PrD) is sufficient for ELF3 phase change and temperature responsiveness. The PrD region contains a polyglutamine (polyQ) repeat of variable length, the size of which has been found to modulate the thermal responsiveness as measured by hypocotyl (stem) elongation and condensate formation. How the PrD is able to respond to temperature is however poorly understood. To understand the underlying biophysical basis for ELF3 thermal responsiveness, we use a polymer chain growth approach to build large ensembles and characterize monomeric ELF3-PrD at a range of polyQ lengths and temperatures. We then explore temperature-dependent dynamics of wild-type ELF3-PrD, ELF3-PrD with the variable polyQ tract removed, and a mutant (F527A) using chain growth structures as initial conformations for replica exchange (REST2) simulations. In addition to different mechanisms of temperature sensing with and without the variable polyQ tract, we find increased solvent accessibility of expanded polyQ tracts, promotion of temperature-sensitive helices adjacent to polyQ tracts, and exposure of a cluster of aromatic residues at increased temperature, all three of which promote inter-protein interaction. These results suggest a set of potential design principles for the engineering of temperature dependent molecular interactions. This has considerable potential for biotechnological application in medicine and agriculture.

Competing Interest Statement

The authors have declared no competing interest.

Footnotes

  • https://github.com/flatironinstitute/ELF3

Copyright 
The copyright holder for this preprint is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under a CC-BY 4.0 International license.
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Posted March 16, 2023.
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Molecular basis of polyglutamine-modulated ELF3 phase change in Arabidopsis temperature response
Richard J. Lindsay, Philip A. Wigge, Sonya M. Hanson
bioRxiv 2023.03.15.532793; doi: https://doi.org/10.1101/2023.03.15.532793
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Molecular basis of polyglutamine-modulated ELF3 phase change in Arabidopsis temperature response
Richard J. Lindsay, Philip A. Wigge, Sonya M. Hanson
bioRxiv 2023.03.15.532793; doi: https://doi.org/10.1101/2023.03.15.532793

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