Emerging Roles of Biomolecular Condensates and Phase Separation in Plant Stress Adaptation and Gene Regulation

Although plants are exposed to many environmental stressors (heat, drought, salinity, and pathogen), they survive by rapidly reprogramming their gene expression. Recent findings show that many regulatory mechanisms are maintained within liquid-liquid phase separation (LLPS) formed biomolecular condensates, instead of maintaining these mechanisms within membrane-bound organelles. LLPS has been shown to exist in plant cells; however, the integration of LLPS with functional stress adaptations and gene regulations is still unclear from the studies that have been published thus far. In this review, we discuss recent research that demonstrates how these biomolecular condensates act as dynamic regulatory centers by linking environmental stress perception to transcriptional and post-transcriptional regulation of genes in plants. We describe the biophysical principles that govern the occurrence of LLPS in a plant cellular environment and provide an overview of how both abiotic (e.g., drought, heat) and biotic (i.e., pathogens) stressors initiate the LLPS and remodel nuclear and cytosolic condensate structures. The focus of this work will be on the effects of stress-induced changes (both qualitatively and quantitatively) in the condensate composition and material properties on transcription factor activity (either as an activator or repressor) and the organization of chromatin, RNA stability, and selective translation. We will also discuss post-translational modifications (PTMs) that modulate condensate dynamics and allow for reversibility. Collectively, these findings suggest that LLPS likely contributes significantly to gene regulation and stress adaptation in plants, although the degree of mechanistic validation varies among different condensate systems.