EARLY FLOWERING 3 (ELF3): a novel role in integrating environmental stimuli with root stem cell niche maintenance

Maintaining the stem cell niche (SCN) homeostasis in the root apical meristem (RAM) is essential for proper root growth and thus for the overall plant development. In Arabidopsis thaliana, a group of slowly dividing cells at the SCN center known as the quiescent center (QC) maintain the surrounding stem cells, including the distally located columella stem cells (CSCs) which give rise to the differentiated columella cells. Many actors, including the PLETHORA (PLT) family transcription factors, regulate the QC quiescence and CSC fate. However, little is known about the integration of external and/or internal cues into regulating SCN homeostasis. In this study, we report for the first time the interaction between PLT3 and a thermosensor and circadian clock related transcriptional regulator, EARLY FLOWERING 3 (ELF3), in the root SCN. We show that ELF3 is expressed in the root SCN, where it localizes, together with PLT3, to subcellular condensates and sustains the QC and CSC fate. We also demonstrate that ELF3 forms condensates in vitro and in vivo, in the cytoplasm, as well as in the nucleus, where it localizes with PLT3. Our studies also demonstrate that the interaction of ELF3 and PLT3 is driven by their intrinsically disordered prion-like domains (PrDs). Furthermore, transient expression in human epithelial cells (HEp-2) cells and in Nicotiana benthamiana shows that PHYTOCHROME INTERACTING FACTORS 3 and 4 (PIF3/4) function as nuclear shuttles for ELF3, recruiting it to nuclear condensates, where it colocalizes with PLT3, PIF3, and PIF4. Accordingly, we propose a model where the colocalization and interactions of ELF3, PLT3, PIF3, and PIF4 represent a dynamic mechanism to integrate environmental signals into SCN maintenance and cell fate decisions.