Tudor staphylococcal nuclease is a docking platform for stress granule components and is essential for SnRK1 activation in Arabidopsis
Emilio Gutiérrez-Beltrán, Pernilla H Elander, Kerstin Dalman, Guy W. Dayhoff, Panagiotis N. Moschou, Vladimir N. Uversky, José L. Crespo, Peter V. Bozhkov
Abstract
Tudor staphylococcal nuclease (TSN; also known as Tudor‐SN, p100, or SND1) is a multifunctional, evolutionarily conserved regulator of gene expression, exhibiting cytoprotective activity in animals and plants and oncogenic activity in mammals. During stress, TSN stably associates with stress granules (SGs), in a poorly understood process. Here, we show that in the model plant Arabidopsis thaliana, TSN is an intrinsically disordered protein (IDP) acting as a scaffold for a large pool of other IDPs, enriched for conserved stress granule components as well as novel or plant‐specific SG‐localized proteins. While approximately 30% of TSN interactors are recruited to stress granules de novo upon stress perception, 70% form a protein–protein interaction network present before the onset of stress. Finally, we demonstrate that TSN and stress granule formation promote heat‐induced activation of the evolutionarily conserved energy‐sensing SNF1‐related protein kinase 1 (SnRK1), the plant orthologue of mammalian AMP‐activated protein kinase (AMPK). Our results establish TSN as a docking platform for stress granule proteins, with an important role in stress signalling. Tudor staphylococcal nuclease (TSN) is an evolutionarily conserved component of stress granules (SGs). Here, TSN is found to serve both as a scaffold for previously uncharacterized components of plant stress granules, and as a positive regulator of SnRK1/AMPK signalling in Arabidopsis. Proteomic analysis of Arabidopsis stress granules identifies a role of intrinsically disordered Tudor staphylococcal nuclease (TSN) as docking platform for stress‐specific and stress‐independent components.