Tracing the evolutionary emergence of the temperature sensing prion-like domain in EARLY FLOWERING 3 across the plant kingdom

Abstract

Plants have evolved to anticipate and adjust their growth and development in response to environmental changes. To mitigate the negative influence of global climate change on crop production, understanding the key regulators of plant performance is imperative.EARLY FLOWERING 3(ELF3) is such a regulator involved in the circadian clock and thermomorphogenesis.Arabidopsis thalianaELF3 contains a prion-like domain (PrD) that functions as a thermosensor, enabling its liquid-liquid phase separation at high ambient temperatures. To understand the conservation of this function across the plant kingdom, we traced the evolutionary emergence of ELF3 with a focus on the PrD, which confers liquid-liquid phase separation. We observed that the presence of the domain within ELF3, mainly contributed by the length of polyglutamine (polyQ) repeats, is largely restricted toBrassicales. This suggests that ELF3’s thermosensory function is a rather recent and secondary acquirement that was added to its main function. By analyzing 319 naturalArabidopsis thalianaaccessions, we detected a wide range of polyQ length variation in ELF3. However, polyQ length is only weakly associated with geographic origin, climate conditions, and classic temperature-responsive phenotypes. Consequently, we conclude that although the emergence of PrD is not likely to be a key driver of environmental adaptation, it adds an extra layer to ELF3’s role in thermomorphogenesis.