Nuclear lamina phase separation orchestrates stress-induced transcriptional responses in plants

Abstract

The nuclear lamina (NL), a perinuclear protein meshwork formed by nucleoskeleton and inner nuclear membrane (INM) proteins, is crucial for chromatin organization at the nuclear periphery and gene expression regulation in eukaryotic cells. However, NL-dependent transcriptional regulation remains poorly understood in plants due to the absence of most canonical NL proteins found in animals. Here, we report that the plant INM protein PLANT NUCLEAR ENVELOPE TRANSMEMBRANE 2 (PNET2) interacts with membrane-bound NAC (NAM, ATAF1/2, and CUC2) transcription factors, NTLs, via intrinsic disorder regions and promotes liquid-liquid phase separation within the NL. This compartmentalization effectively sequesters NTLs and restricts their transcriptional activity. In the absence of PNET2, NTLs become deregulated, triggering spontaneous and broad-spectrum stress responses. Importantly, we found that stress stimuli, such as heat shock, disrupt PNET2-NTL phase separation, releasing NTLs for target gene binding and transcriptional activation. These findings demonstrate a phase separation-based regulatory mechanism within the NL that controls membrane-bound transcription factor activity in response to environmental cues.