Arabidopsis Heat Stress-Induced Proteins Are Enriched in Electrostatically Charged Amino Acids and Intrinsically Disordered Regions

[EN] Comparison of the proteins of thermophilic, mesophilic, and psychrophilic prokaryotes has revealed several features characteristic to proteins adapted to high temperatures, which increase their thermostability. These characteristics include a profusion of disulfide bonds, salt bridges, hydrogen bonds, and hydrophobic interactions, and a depletion in intrinsically disordered regions. It is unclear, however, whether such differences can also be observed in eukaryotic proteins or when comparing proteins that are adapted to temperatures that are more subtly different. When an organism is exposed to high temperatures, a subset of its proteins is overexpressed (heat-induced proteins), whereas others are either repressed (heat-repressed proteins) or remain unaffected. Here, we determine the expression levels of all genes in the eukaryotic model system Arabidopsis thaliana at 22 and 37 degrees C, and compare both the amino acid compositions and levels of intrinsic disorder of heat-induced and heat-repressed proteins. We show that, compared to heat-repressed proteins, heat-induced proteins are enriched in electrostatically charged amino acids and depleted in polar amino acids, mirroring thermophile proteins. However, in contrast with thermophile proteins, heat-induced proteins are enriched in intrinsically disordered regions, and depleted in hydrophobic amino acids. Our results indicate that temperature adaptation at the level of amino acid composition and intrinsic disorder can be observed not only in proteins of thermophilic organisms, but also in eukaryotic heat-induced proteins; the underlying adaptation pathways, however, are similar but not the same.
D.A.-P. and F.F. were supported by funds from the University of Nevada, Reno, and by pilot grants from Nevada INBRE (P20GM103440) and the Smooth Muscle Plasticity COBRE from the University of Nevada, Reno (5P30GM110767-04), both funded by the National Institute of General Medical Sciences (National Institutes of Health). M.X.R.-G. and M.A.F. were supported by grants from Science Foundation Ireland (12/IP/1637) and the Spanish Ministerio de Economia y Competitividad, Spain (MINECO-FEDER; BFU201236346 and BFU2015-66073-P) to MAF. MXRG was supported by a JAE DOC fellowship from the MINECO, Spain. F.V.-S. and M.A.P.-A. were supported by grant BIO2014-55946-P from MINECO-FEDER.