Structural transitions in the intrinsically disordered plant dehydration stress protein LEA7 upon drying are modulated by the presence of membranes

Dure, 1981, Developmental biochemistry of cottonseed embryogenesis and germination: changing messenger ribonucleic acid populations as shown by in vitro and in vivo protein synthesis, Biochemistry, 20, 4162, 10.1021/bi00517a033 Black, 1999, Water content, raffinose, and dehydrins in the induction of desiccation tolerance in immature wheat embryos, Plant Physiol., 120, 463, 10.1104/pp.120.2.463 Blackman, 1991, Maturation proteins associated with desiccation tolerance in soybean, Plant Physiol., 96, 868, 10.1104/pp.96.3.868 Hundertmark, 2008, LEA (Late Embryogenesis Abundant) proteins and their encoding genes in Arabidopsis thaliana, BMC Genomics, 9, 118, 10.1186/1471-2164-9-118 Battista, 2001, Inactivation of two homologues of proteins presumed to be involved in the desiccation tolerance of plants sensitizes Deinococcus radiodurans R1 to desiccation, Cryobiology, 43, 133, 10.1006/cryo.2001.2357 Browne, 2002, Plant desiccation gene found in a nematode, Nature, 416, 38, 10.1038/416038a Pouchkina-Stantcheva, 2007, Functional divergence of former alleles in an ancient asexual invertebrate, Science, 318, 268, 10.1126/science.1144363 Kikawada, 2006, Dehydration-induced expression of LEA proteins in an anhydrobiotic chironomid, Biochem. Biophys. Res. Comm., 348, 56, 10.1016/j.bbrc.2006.07.003 Close, 1993, An osmotic stress protein of cyanobacteria is immunologically related to plant dehydrins, Plant Physiol., 101, 773, 10.1104/pp.101.3.773 Bies-Etheve, 2008, Inventory, evolution and expression profiling diversity of the LEA (late embryogenesis abundant) protein gene family in Arabidopsis thaliana, Plant Mol. Biol., 67, 107, 10.1007/s11103-008-9304-x Dyson, 2005, Intrinsically unstructured proteins and their functions, Nat. Rev. Mol. Cell Biol., 6, 197, 10.1038/nrm1589 Tunnacliffe, 2010, LEA proteins: versatility of form and function, 91 Tunnacliffe, 2007, The continuing conundrum of LEA proteins, Naturwissenschaften, 94, 791, 10.1007/s00114-007-0254-y Battaglia, 2008, The enigmatic LEA proteins and other hydrophilins, Plant Physiol., 148, 6, 10.1104/pp.108.120725 Boucher, 2010, MtPM25 is an atypical hydrophobic late embryogenesis-abundant protein that dissociates cold and desiccation-aggregated proteins, Plant Cell Environ., 33, 418, 10.1111/j.1365-3040.2009.02093.x Chakrabortee, 2007, Hydrophilic protein associated with desiccation tolerance exhibits broad protein stabilization function, Proc. Natl Acad. Sci. U.S.A., 104, 18073, 10.1073/pnas.0706964104 Goyal, 2005, LEA proteins prevent protein aggregation due to water stress, Biochem. J., 388, 151, 10.1042/BJ20041931 Kovacs, 2008, Chaperone activity of ERD10 and ERD14, two disordered stress-related plant proteins, Plant Physiol., 147, 381, 10.1104/pp.108.118208 Boudet, 2006, Comparative analysis of the heat stable proteome of radicles of Medicago truncatula seeds during germination identifies late embryogenesis abundant proteins associated with desiccation tolerance, Plant Physiol., 140, 1418, 10.1104/pp.105.074039 Goyal, 2003, Transition from natively unfolded to folded state induced by desiccation in an anhydrobiotic nematode protein, J. Biol. Chem., 278, 12977, 10.1074/jbc.M212007200 Shih, 2004, Gene cloning and characterization of a soybean (Glycine max L.) LEA protein, GmPM16, Plant Mol. Biol., 56, 689, 10.1007/s11103-004-4680-3 Tolleter, 2007, Structure and function of a mitochondrial late embryogenesis abundant protein are revealed by desiccation, Plant Cell, 19, 1580, 10.1105/tpc.107.050104 Wolkers, 2001, Isolation and characterization of a D-7 LEA protein from pollen that stabilizes glasses in vitro, Biochim. Biophys. Acta, 1544, 196, 10.1016/S0167-4838(00)00220-X Thalhammer, 2010, Interaction of two intrinsically disordered plant stress proteins (COR15A and COR15B) with lipid membranes in the dry state, Biochim. Biophys. Acta, 1798, 1812, 10.1016/j.bbamem.2010.05.015 Tolleter, 2010, A mitochondrial late embryogenesis abundant protein stabilizes model membranes in the dry state, Biochim. Biophys. Acta, 1798, 1926, 10.1016/j.bbamem.2010.06.029 Bray, 1993, Molecular responses to water deficit, Plant Physiol., 103, 1035, 10.1104/pp.103.4.1035 Sakurai, 2005, RARGE: a large-scale database of RIKEN Arabidopsis resources ranging from transcriptome to phenome, Nucl. Acids Res., 33, D647, 10.1093/nar/gki014 Seki, 2002, Functional annotation of a full-length Arabidopsis cDNA collection, Science, 296, 141, 10.1126/science.1071006 Sreerama, 2000, Estimation of protein secondary structure from circular dichroism spectra: inclusion of denatured proteins with native proteins in the analysis, Anal. Biochem., 287, 243, 10.1006/abio.2000.4879 MacDonald, 1991, Small-volume extrusion apparatus for preparation of large, unilamellar vesicles, Biochim. Biophys. Acta, 1061, 297, 10.1016/0005-2736(91)90295-J Hincha, 2002, Specific effects of fructo- and gluco-oligosaccharides in the preservation of liposomes during drying, Glycobiology, 12, 103, 10.1093/glycob/12.2.103 Popova, 2003, Intermolecular interactions in dry and rehydrated pure and mixed bilayers of phosphatidylcholine and digalactosyldiacylglycerol: a Fourier-transform infrared spectroscopy study, Biophys. J., 85, 1682, 10.1016/S0006-3495(03)74598-6 Popova, 2007, Effects of cholesterol on dry bilayers: interactions between phosphatidylcholine unsaturation and glycolopid or free sugar, Biophys. J., 93, 1204, 10.1529/biophysj.107.108886 Crowe, 1997, Stabilization of dry membranes by mixtures of hydroxyethyl starch and glucose: the role of vitrification, Cryobiology, 35, 20, 10.1006/cryo.1997.2020 Geourjon, 1995, SOPMA: significant improvements in protein secondary structure prediction by consensus prediction from multiple alignments, Comput. Appl. Biosci., 11, 681 Guex, 1997, SWISS-MODEL and the Swiss-PdbViewer: an environment for comparative protein modeling, Electrophoresis, 18, 2714, 10.1002/elps.1150181505 Barth, 2007, Infrared spectroscopy of proteins, Biochim. Biophys. Acta, 1767, 1073, 10.1016/j.bbabio.2007.06.004 Byler, 1986, Examination of the secondary structure of proteins by deconvolved FTIR spectra, Biopolymers, 25, 469, 10.1002/bip.360250307 Arrondo, 1993, Quantitative studies of the structure of proteins in solution by Fourier-transform infrared spectroscopy, Progr. Biophys. Mol. Biol., 59, 26, 10.1016/0079-6107(93)90006-6 Susi, 1983, Protein structure by Fourier transform infrared spectroscopy: second derivative spectra, Biochem. Biophys. Res. Comm., 115, 391, 10.1016/0006-291X(83)91016-1 Susi, 1986, Resolution-enhanced Fourier transform infrared spectroscopy of enzymes, Meth. Enzymol., 130, 290, 10.1016/0076-6879(86)30015-6 Surewicz, 1988, New insight into protein structure from resolution-enhanced infrared spectra, Biochim. Biophys. Acta, 952, 115, 10.1016/0167-4838(88)90107-0 Krimm, 1980, Vibrational analysis of peptides, polypeptides, and proteins. V. Normal vibrations of β-turns, Biopolymers, 19, 1, 10.1002/bip.1980.360190102 Arrondo, 1999, Structure and dynamics of membrane proteins as studied by infrared spectroscopy, Prog. Biophys. Mol. Biol., 72, 367, 10.1016/S0079-6107(99)00007-3 Dong, 1998, Intermolecular β-sheet results from trifluoroethanol-induced nonnative α-helical structure in β-sheet predominant proteins: infrared and circular dichroism spectroscopic study, Arch. Biochem. Biophys., 355, 275, 10.1006/abbi.1998.0718 Frauenfelder, 2002, Hydration, slaving and protein function, Biophys. Chem., 98, 35, 10.1016/S0301-4622(02)00083-2 Mantsch, 1991, Phospholipid phase transitions in model and biological membranes as studied by infrared spectroscopy, Chem. Phys. Lipids, 57, 213, 10.1016/0009-3084(91)90077-O Wong, 1988, High-pressure infrared spectroscopic evidence of water binding sites in 1,2-diacyl phospholipids, Chem. Phys. Lipids, 46, 213, 10.1016/0009-3084(88)90024-2 Cacela, 2006, Low amounts of sucrose are sufficient to depress the phase transition temperature of dry phosphatidylcholine, but not for lyoprotection of liposomes, Biophys. J., 90, 2831, 10.1529/biophysj.105.074427 Koag, 2003, The binding of maize DHN1 to lipid vesicles. Gain of structure and lipid specificity, Plant Physiol., 131, 309, 10.1104/pp.011171 Koag, 2009, The K-segment of maize DHN1 mediates binding to anionic phospholipid vesicles and concomitant structural changes, Plant Physiol., 150, 1503, 10.1104/pp.109.136697 Rahman, 2010, Interactions of intrinsically disordered Thellungiella salsuginea dehydrins TsDHN-1 and TsDHN-2 with membranes—synergistic effects of lipid composition and temperature on secondary structure, Biochem. Cell Biol., 88, 791, 10.1139/O10-026 Mishra, 1994, Interactions ofsynthtic peptide analogs of the class A amphipathic helix with lipids, J. Biol. Chem., 289, 7185, 10.1016/S0021-9258(17)37266-6 Segrest, 1992, The amphipathic helix in the exchangeable apolipoproteins: a review of secondary structure and function, J. Lipid Res., 35, 141, 10.1016/S0022-2275(20)41536-6 Krishnan, 2008, Methyl group dynamics and the onset of anharmonicity in myoglobin, J. Phys. Chem. B, 112, 5522, 10.1021/jp076641z Roh, 2006, Influence of hydration on the dynamics of lysozyme, Biophys. J., 91, 2573, 10.1529/biophysj.106.082214 Tsai, 2000, Molecular dynamics of solid-state lysozyme as affected by glycerol and water: a neutron scattering study, Biophys. J., 79, 2728, 10.1016/S0006-3495(00)76511-8 Wharton, 2000, Infrared spectroscopy of enzyme reaction intermediates, Nat. Prod. Rep., 17, 447, 10.1039/b002066o