Interplay of Structural Disorder and Short Binding Elements in the Cellular Chaperone Function of Plant Dehydrin ERD14

• DOI: 10.3390/cells9081856
• Publication Date: 2020-08-10T11:25:03Z
• Authors: Nikoletta Murvai; Lajos Kalmar; Bianka Szalaine A...; Beata Szabo; Agnes Tantos; Gyorgy Csikos; András Micsonai; József Kardos; Didier Vertommen; Phuong N. Nguyen; Nevena Hristozova; Andras Lang; Denes Kovacs; Laszlo Buday; Kyou-Hoon Han; Andras Perczel; Peter Tompa
• Keywords: 0301 basic medicine; cell protection; Proteome; QH3015 Molecular biology / molekuláris biológia; Arabidopsis; Article; 03 medical and health sciences; Protein Domains; Escherichia coli; chaperone; SB Plant culture / növénytermesztés; 0303 health sciences; Microbial Viability; QH3011 Biochemistry / biokémia; QH573-671; in-cell NMR; Arabidopsis Proteins; pre-structured motif; Intrinsically Disordered Proteins; intrinsic structural disorder; client protein; Microorganisms, Genetically-Modified; Cytology; Heat-Shock Response; Molecular Chaperones; Protein Binding

Details of the functional mechanisms of intrinsically disordered proteins (IDPs) in living cells is an area not frequently investigated. Here, we dissect the molecular mechanism of action of an IDP in cells by detailed structural analyses based on an in-cell nuclear magnetic resonance experiment. We show that the ID stress protein (IDSP) A. thaliana Early Response to Dehydration (ERD14) is capable of protecting E. coli cells under heat stress. The overexpression of ERD14 increases the viability of E. coli cells from 38.9% to 73.9% following heat stress (50 °C × 15 min). We also provide evidence that the protection is mainly achieved by protecting the proteome of the cells. In-cell NMR experiments performed in E. coli cells show that the protective activity is associated with a largely disordered structural state with conserved, short sequence motifs (K- and H-segments), which transiently sample helical conformations in vitro and engage in partner binding in vivo. Other regions of the protein, such as its S segment and its regions linking and flanking the binding motifs, remain unbound and disordered in the cell. Our data suggest that the cellular function of ERD14 is compatible with its residual structural disorder in vivo.