A Cytoplasmic Osmosensing Mechanism Mediated by Molecular Crowding-Sensitive DCP5. DCP5：Decapping 5；DOSG：DCP5-enriched osmotic stress granule

Under the support of grants from the National Natural Science Foundation of China (Grant Numbers: 32261160572, 31870254), Professor Guo Hongwei's team at Southern University of Science and Technology has made progress in the field of plant osmotic stress sensing. Their research findings, titled "A cytoplasmic osmosensing mechanism mediated by molecular crowding-sensitive DCP5," were published in Science on November 1, 2024. The paper can be accessed at:http://doi.org/10.1126/science.adk9067.

Drought, flooding, extreme temperatures, and soil salinization can easily induce osmotic stress in sessile plants, severely affecting their growth and development, and causing significant losses to global crop yields. Understanding how plants sense osmotic stress holds important theoretical and practical significance, yet previous research has provided limited insights into the initial sensing mechanisms within plant cells. The research results from Professor Guo's team indicate that in isosmotic environments, the DCP5 (Decapping 5) protein is uniformly dispersed in the cytoplasm. When cells are exposed to hyperosmotic conditions, DCP5 responds to the molecular crowding caused by cell volume changes, undergoing liquid-liquid phase separation and forming condensates, thereby sensing the hyperosmotic stress. Further studies have confirmed that during the formation of these condensates, DCP5 co-enriches with RNA-binding proteins, translation initiation factors, and a large amount of mRNA, forming DCP5-enriched osmotic stress granules (DOSGs), which reprogram both the transcriptome and translatome, enabling immediate adaptation of plants to osmotic stress.

This study reveals that DCP5, as a multifunctional osmosensor, can instantly sense and adapt to osmotic stress through molecular crowding-sensitive phase separation and DOSG assembly pathways. Compared to the classic "receptor-signal transduction-gene expression regulation" pathway, the environmental sensing and adaptation mechanism mediated by phase-separated proteins and membraneless organelles does not require signaling molecules or signal transduction processes, thus enabling a more rapid response to environmental changes. This study provides important experimental evidence for the emerging view that protein phase separation serves as a general mechanism for cellular environmental sensing.