Tudor staphylococcal nuclease is a docking platform for stress granule components and is essential for SnRK1 activation in Arabidopsis

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.

TDRD5 Is Required for Spermatogenesis and Oogenesis in Locusta migratoria

“…Tudor proteins are members of a royal superfamily that also contains the Chromo, MBT, PWWP, and plant Agenet domain proteins [ 28 , 29 ]. Since the first Tudor protein discovered in D. melanogaster [ 30 ], these proteins are also found in mouse, human, zebrafish, yeast, and plants [ 31 , 32 , 33 , 34 , 35 , 36 , 37 , 38 , 39 , 40 , 41 ]. Tudor proteins bind to proteins with methylated arginine or lysine residues and take part in cellular processes, such as DNA methylation, RNA metabolism, transcription regulation, DNA damage detection and repair, the P-element-induced wimpy testis (PIWI)-interacting RNA (piRNA) pathway, and the maintenance of genomic stability [ 32 , 42 ].…”

The “Proxitome” of Arabidopsis Processing Bodies Reveals a Condensate-Membrane Interface Instructing Actin-Driven Directional Growth

“…1c), which may lead to increases in their size and number and likely to a change in composition 5 . HS also enhances RNA decapping through the increased association of the mRNA decapping complex DCP1–DCP2 with polysomes 19 . We observed that HS does not significantly affect biotinylation levels of DCP1-TurboID-HF (Supplementary Fig.…”

The TSN1 Binding Protein RH31 Is a Component of Stress Granules and Participates in Regulation of Salt-Stress Tolerance in Arabidopsis

“…TSN is also involved in regulating transcription ( Paukku et al, 2003 ; Yang et al, 2014 ), pre-mRNA splicing ( Yang et al, 2007 ), mRNA stabilization ( Paukku et al, 2008 ), RNA silencing ( Caudy et al, 2003 ), and cleaving hyperedited double-stranded RNA ( Scadden, 2005 ) in animals. Most relevant to the present study, TSN is established with an important role in stress signaling as a docking platform for stress granule proteins and is necessary for assembly and/or function of SGs ( Gao et al, 2015 ; Gutierrez-Beltran et al, 2021 ).…”

“…Meanwhile, TSN functions in mRNA catabolism and links the formation of SGs and processing bodies (PBs)-cytoplasmic RNA granules which are believed to be sites of mRNA degradation ( Arribere et al, 2011 ; Gutierrez-Beltran et al, 2015 ). In the latest study, TSN is established with an important role in stress signaling as a docking platform for stress granule proteins ( Gutierrez-Beltran et al, 2021 ). Therefore, TSN is important for plant development and stress tolerance.…”