Prion-like domain in ELF3 acts as a thermosensor in the plant Arabidopsis

Today we have a “natural” as a topic for gene-environment interactions. And “prions” are mentioned again — just after an article about prions 2-3 days ago in these GEITP pages. Today the “environmental signal” is temperature (heat vs cold), and the “gene response to the environmental signal” (in the genome of the plant, Arabidopsis thaliana) involves a prion-like domain (PrD) in the thermosensor protein called ELF3, encoded by the EARLY FLOWERING-3 gene.

Unlike animals, plants cannot move (or, for humans, remove or add clothing) to escape harsh conditions. Consequently, plants must continuously monitor their environment and, when exposed to high temperatures, quickly adjust their expression of developmental- and growth-related genes. Authors [see attached article & editorial] describe a molecular process that appears to underlie this temperature responsiveness. Expression of developmental- and growth-related genes in animals and plants typically occurs in a rhythmic fashion over a 24-hour cycle. Such daily oscillations are controlled by a molecular loop of protein activity that provides what is termed “the circadian clock.” Clock-induced transcriptional changes enable plants to anticipate daily environmental changes.

In the tiny mustard plant A. thaliana, one component of the circadian clock is a protein assembly called the evening

complex, which is maximally active at dusk and represses expression of many genes important for plant development. The evening complex comprises the transcription-factor protein ELF3, a peptide known as ELF4 (a small α-helical protein), and a protein called LUX (a DNA-binding protein required to recruit the evening complex to transcriptional targets). Plants with mutations that disable the ELF gene tend to flower earlier than normal during development and grow longer embryonic stems (termed “hypocotyls”) — indicating that ELF3 has a key developmental role. ELF3 contains a polyglutamine (polyQ) repeat — embedded within a predicted prion domain (PrD). Authors [see attached article] discovered that the length of the polyQ repeat — correlates with thermal responsiveness.

Authors found that ELF3 proteins in plants from hotter climates — with no detectable PrD — are active at high temperatures, and lack thermal responsiveness. Temperature sensitivity of ELF3 is also modulated by ELF4 levels, indicating that ELF4 can stabilize the function of ELF3. In both Arabidopsis and a heterologous system, authors fused ELF3 with the intracellular marker, green fluorescent protein (GFP), and demonstrated that speckles are formed, within minutes, in response to higher temperatures — in a PrD-dependent manner. A purified peptide fragment — encompassing the ELF3 PrD — was found to reversibly form liquid droplets in response to increasing temperatures in cell culture, indicating that these properties reflect a direct biophysical response conferred by the PrD. This study shows that the ability of temperature to rapidly shift ELF3 between active and inactive states, via phase transition, represents a previously unknown thermosensory mechanism. 😊

DwN

Nature 10 Sept 2020; 585: 256-260 & editorial pp 191-192

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