Phase separation in plants: New insights into cellular compartmentalization

Abstract

A fundamental challenge for cells is how to coordinate various biochemical reactions in space and time. To achieve spatiotemporal control, cells have developed organelles that are surrounded by lipid bilayer membranes. Further, membraneless compartmentalization, a process induced by dynamic physical association of biomolecules through phase transition offers another efficient mechanism for intracellular organization. While our understanding of phase separation was predominantly dependent on yeast and animal models, recent findings have provided compelling evidence for emerging roles of phase separation in plants. In this review, we first provide an overview of the current knowledge of phase separation, including its definition, biophysical principles, molecular features and regulatory mechanisms. Then we summarize plant-specific phase separation phenomena and describe their functions in plant biological processes in great detail. Moreover, we propose that phase separation is an evolutionarily conserved and efficient mechanism for cellular compartmentalization which allows for distinct metabolic processes and signaling pathways, and is especially beneficial for the sessile lifestyle of plants to quickly and efficiently respond to the changing environment.

The Receptor Kinase FER Mediates Phase Separation of Glycine-Rich RNA-Binding Protein 7 to Confer Temperature Resilience in Arabidopsis

“…The mechanism by which their LLPS-related biochemical behaviours are regulated and their relationships with stress or disease states are coming into focus. To date, only two plant RBP, FCA and MEL2 30, 50, 55, 56 , have been documented to display LLPS behaviours; these function in precursor mRNA polyadenylation in Arabidopsis 50 and that regulates the timing of meiotic transition in rice ( Oryza sativa ) 55 , respectively. LLPS of GRP7, reported here, provides a novel example of a plant RBP that mediates signal transduction in response to temperature stress.…”

Liquid-Liquid Phase Separation Phenomenon on Protein Sorting Within Chloroplasts

“…In humans, animals, plants, and many other organisms, LLPS participates in various biological processes, such as ribosome biogenesis, gene expression, RNA processing, heterochromatin formation, etc. (Zhang et al, 2020;Emenecker et al, 2021;Kim et al, 2021;Xu et al, 2021b). Disturbing the process of LLPS may lead to liquid condensates vanishing or transforming into other material states, which are associated with many human diseases, including infectious diseases, neurodegeneration, and cancer (Alberti et al, 2019).…”

Protein Targeting Into the Thylakoid Membrane Through Different Pathways

“…The nuclear-encoded thylakoid proteins with an N-terminal transit peptide (TP) are first imported into the stroma by the Toc/Tic (translocon at the outer/inner envelope membrane of chloroplasts) complexes, and then the TP is removed by the stromal processing peptidase, and the proteins are targeted into or across the thylakoid membranes through sophisticated targeting pathways ( Martin et al, 2002 ; Leister, 2003 ). To date, several independent pathways have been reported, of which the chloroplast signal recognition particle (cpSRP) pathway, the spontaneous insertion pathway and the recently discovered chloroplast Guided Entry of TA proteins (cpGET) pathway are responsible for inserting proteins into the thylakoid membrane ( Figure 1 ), while the chloroplast secretory (cpSec) and the chloroplast twin-arginine translocase (cpTat) pathways are needed for translocating proteins into the thylakoid lumen ( Schünemann, 2007 ; Ouyang et al, 2020 ; Anderson et al, 2021 ; Xu et al, 2021a , b ). In contrast, proteins encoded by the chloroplast genome are cotranslationally transported from the stroma to thylakoids ( Figure 1 ).…”