The continuing conundrum of the LEA proteins

Naturwissenschaften

Volumn 94, Issue 10, 2007, Pages 791-812

  Tunnacliffe, Alan ^a   Wise, Michael J ^b  

^a UNIVERSITY OF CAMBRIDGE   (United Kingdom)

^b UNIVERSITY OF WESTERN AUSTRALIA   (Australia)

Author keywords

Anhydrobiosis; Cold stress; Desiccation tolerance; Drought stress; Water stress

Indexed keywords

LATE EMBRYOGENESIS ABUNDANT PROTEIN; PROTEIN; UNCLASSIFIED DRUG;

ANTIOXIDANT; DESICCATION; DROUGHT STRESS; EMBRYONIC DEVELOPMENT; MEMBRANE; PROTEIN; SEED; TEMPERATURE EFFECT; WATER STRESS;

ABIOTIC STRESS; AMINO ACID SEQUENCE; BACTERIUM; BIOCHEMISTRY; COLD STRESS; DATA ANALYSIS; DEHYDRATION; EUKARYOTE; GENOME ANALYSIS; HUMAN; HYDROPHILICITY; IN VITRO STUDY; INVERTEBRATE; MOLECULAR BIOLOGY; NONHUMAN; PHYLOGENY; PLANT SEED; PROKARYOTE; PROTEIN ANALYSIS; PROTEIN EXPRESSION; PROTEIN FAMILY; PROTEIN FOLDING; PROTEIN FUNCTION; PROTEIN MOTIF; PROTEIN STABILITY; PROTEIN STRUCTURE; REVIEW; SEQUENCE HOMOLOGY; STRESS; WATER STRESS;

INVERTEBRATA;

EID: 34548460796     PISSN: 00281042     EISSN: None     Source Type: Journal    
DOI: 10.1007/s00114-007-0254-y     Document Type: Review

References (177)

1. Alban C, Job D, Douce R (2000) Biotin metabolism in plants. Annu Rev Plant Physiol Plant Mol Biol 51:17-47
2. Alpert P (2005) The limits and frontiers of desiccation-tolerant life. Integr Comp Biol 45:685-695
3. Alsheikh MK, Heyen BJ, Randall SK (2003) Ion binding properties of the dehydrin ERD14 are dependent upon phosphorylation. J Biol Chem 278:40882-40889
4. Alsheikh MK, Svensson JT, Randall SK (2005) Phosphorylation regulated ion-binding is a property shared by the acidic subclass dehydrins. Plant Cell Environ 28:1114-1122
5. Artus NN, Uemura M, Steponkus PL, Gilmour SJ, Lin C, Thomashow MF (1996) Constitutive expression of the cold-regulated Arabidopsis thaliana COR15a gene affects both chloroplast and protoplast freezing tolerance. Proc Natl Acad Sci USA 93:13404-13409
6. Asai GN (1943) A study of frost injury and frost resistance in garden roses. Ph.D. Thesis. Cornell University
7. Asghar R, Fenton RD, DeMason DA, Close TJ (1994) Nuclear and cytoplasmic localization of maize embryo and aleurone dehydrin. Protoplasma 177:87-94
8. Babu RC, Zhang J, Blum A, Ho T-HD, Wu R, Nguyen HT (2004) HVA1, a LEA gene from barley confers dehydration tolerance in transgenic rice (Oryza sativa) via cell membrane protection. Plant Sci 166:855-862
9. Baker J, Steele C, Dure L III (1988) Sequence and characterization of 6 Lea proteins and their genes from cotton. Plant Mol Biol 11:277-291
10. Bartels D (2005) Desiccation tolerance studied in the resurrection plant Craterostigma plantagineum. Integr Comp Biol 45:696-701
11. Bateman A, Coin L, Durbin R, Finn RD, Hollich V, Griffiths-Jones S, Khanna A, Marshall M, Moxon S, Sonnhammer EL et al (2004) The Pfam protein families database. Nucleic Acids Res 32(Database issue):D138-D141
12. Battista JR, Park MJ, McLemore AE (2001) Inactivation of two homologues of proteins presumed to be involved in the desiccation tolerance of plants sensitizes Deinococcus radiodurans R1 to desiccation. Cryobiology 43:133-139
13. Berjak P (2006) Unifying perspectives of some mechanisms basic to desiccation tolerance across life forms. Seed Sci Res 16:1-15
14. Bies N, Aspart L, Carles C, Gallois P, Delseny M (1998) Accumulation and degradation of Em proteins in Arabidopsis thaliana: evidence for post-transcriptional controls. J Exp Bot 49:1925-1933
15. Blackman SA, Obendorf RL, Leopold AC (1995) Desiccation tolerance in developing soybean seeds-the role of stress proteins. Physiol Plant 93:630-638
16. Bochicchio B, Tamburro AM (2002) Polyproline II structure in proteins: identification by chiroptical spectroscopies, stability, and functions. Chirality 14:782-792
17. Bokor M, Csizmók V, Kovács D, Bánki P, Friedrich P, Tompa P, Tompa K (2005) NMR relaxation studies on the hydrate layer of intrinsically unstructured proteins. Biophys J 88:2030-2037
18. Boudet J, Buitink J, Hoekstra FA, Rogniaux H, Larré C, Satour P, Leprince O (2006) Comparative analysis of the heat stable proteome of radicles of Medicago trunculata seeds during germination identifies late embryogenesis abundant proteins associated with desiccation tolerance. Plant Physiol 140:1418-1436
19. Bravo LA, Gallardo J, Navarrete A, Olave N, Martínez J, Alberdi J, Close TJ, Corcuera LJ (2003) Cryoprotective activity of a cold-induced dehydrin purified from barley. Physiol Plant 118:262-269
20. Bray EA (1993) Molecular responses to water deficit. Plant Physiol 103:1035-1040
21. Bray EA (1994) Alterations in gene expression in response to water deficit. In: Basra AS (ed) Stress-induced gene expression in plants. Harwood Academic, Newark, NJ, pp 1-23
22. Bray EA (2000) Responses to abiotic stresses. In: Buchanan RB, Gruissem W, Jones RL (eds) Biochemistry and molecular biology of plants. The American Society of Plant Physiologists, Rockville, MD, pp 1158-1203
23. Brini F, Fanin M, Lumbreras V, Irar S, Pagès M, Masmoudi K (2007) Functional characterization of DHN-5, a dehydrin showing a differential phosphorylation pattern in two Tunisian durum wheat (Triticum durum Desf.) varieties with marked differences in salt and drought tolerance. Plant Sci 172:20-28
24. Browne JA, Tunnacliffe A, Burnell AM (2002) Plant desiccation gene found in a nematode. Nature 416:38
25. Browne JA, Dolan KM, Tyson T, Goyal K, Tunnacliffe A, Burnell AM (2004) Dehydration-specific induction of hydrophilic protein genes in the anhydrobiotic nematode Aphelenchus avenae. Eukaryot Cell 3:966-975
26. Burke MJ (1986) The vitreous state and survival of anhydrous biological systems. In: Leopold AC (ed) Membranes, metabolism and dry organisms. Cornell University Press, New York, pp 358-364
27. Campos F, Zamudio F, Covarrubias AA (2006) Two different late embryogenesis abundant proteins from Arabidopsis thaliana contain specific domains that inhibit Escherichia coli growth. Biochem Biophys Res Comm 342:406-413
28. Carles C, Bies-Etheve N, Aspart L, Léon-Kloosterziel KM, Koorneef M, Echeverria M, Delseny M (2002) Regulation of Arabidopsis thaliana Em genes: role of ABI5. Plant J 30:373-383
29. Ceccardi TL, Meyer NC, Close TJ (1994) Purification of a maize dehydrin. Protein Expr Purif 5:266-269
30. Cheng Z, Targolli J, Huang X, Wu R (2002) Wheat LEA genes, PMA80 and PMA1959, enhance dehydration tolerance of transgenic rice (Oryza sativa L.). Mol Breed 10:71-82
31. Clayton DF, George JM (1999) Synucleins in synaptic plasticity and neurodegenerative disorders. J Neurosci Res 58:120-129
32. Close TJ (1996) Dehydrins: emergence of a biochemical role of a family of plant dehydration proteins. Physiol Plant 97:795-803
33. Close TJ (1997) Dehydrins: a commonalty in the response of plants to dehydration and low temperature. Physiol Plant 100:291-296
34. Close TJ, Kortt AA, Chandler PM (1989) A cDNA-based comparison of dehydration-induced proteins (dehydrins) in barley and corn. Plant Mol Biol 13:95-108
35. Crowe JH, Oliver AE, Hoekstra FA, Crowe LM (1997) Stabilization of dry membranes by mixtures of hydroxyethyl starch and glucose: the role of vitrification. Cryobiology 3:20-30
36. Crowe JH, Carpenter JF, Crowe LM (1998) The role of vitrification in anhydrobiosis. Annu Rev Physiol 60:73-103
37. Cuming AC (1999) LEA proteins. In: Shewry PR, Casey R (eds) Seed proteins. Kluwer, Dordrecht, The Netherlands, pp 753-780
38. Danyluk J, Houde M, Rassart E, Sarhan F (1994) Differential expression of a gene encoding an acidic dehydrin in chilling sensitive and freezing tolerant gramineae species. FEBS Lett 344:20-24
39. Danyluk J, Perron A, Houde M, Limin A, Fowler B, Benhamou N, Sarhan F (1998) Accumulation of an acidic dehydrin in the vicinity of the plasma membrane during cold acclimation of wheat. Plant Cell 10:623-638
40. Dunker AK, Lawson JD, Brown CJ, Williams RM, Romero P, Oh JS, Oldfield CJ, Campen AM, Ratliff CM, Hipps KW, Ausio J, Nissen MS, Reeves R, Kang C, Kissinger CR, Bailey RW, Griswold MD, Chiu W, Garner EC, Obradovic Z (2001) Intrinsically disordered protein. J Mol Graphics Model 19:26-59
41. Dure L III (1993) Structural motifs in Lea proteins. In: Close TJ, Bray EA (eds) Plant responses to cellular dehydration during environmental stress. The American Society of Plant Physiologists, Rockville, MD, pp 91-103
42. Dure L III, Greenway SC, Galau GA (1981) Developmental biochemistry of cottonseed embryogenesis and germination: changing messenger ribonucleic acid populations as shown by in vitro and in vivo protein synthesis. Biochemistry 20:4162-4168
43. Dure L III, Crouch M, Harada J, Ho T-HD, Mundy J, Quatrano R, Thomas T, Sung ZR (1989) Common amino acid sequence domains among the LEA proteins of higher plants. Plant Mol Biol 12:475-486
44. Dyson HJ, Wright PE (2002) Coupling of folding and binding for unstructured proteins. Curr Opin Struct Biol 12:54-60
45. Edgar RC (2004) MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res 32:1792-1797
46. Egerton-Warburton LM, Balsamo RA, Close TJ (1997) Temporal accumulation and ultrastructural localization of dehydrins in Zea mays L. Physiol Plant 101:545-555
47. Eisenberg D (1984) Three-dimensional structure of membrane and surface proteins. Ann Rev Biochem 53:595-623
48. Ellis RJ (2004) From chloroplasts to chaperones: how one thing led to another. Photosynth Res 80:333-343
49. Ellis RJ, Vandervies SM (1991) Molecular chaperones. Annu Rev Biochem 60:321-347
50. Eom J, Baker WR, Kintanar A, Wurtele ES (1996) The embryo-specific EMB-1 protein of Daucus carota is flexible and unstructured in solution. Plant Sci 115:17-24
51. Felsenstein J (2004) PHYLIP (Phylogeny Inference Package) version 3.6. Distributed by the author. Department of Genome Sciences, University of Washington, Seattle
52. Felsenstein J, Churchill GA (1996) A hidden Markov model approach to variation among sites in rate of evolution. Mol Biol Evol 13:93-104
53. Figueras M, Pujal J, Saleh A, Savé R, Pagès M, Goday R (2004) Maize Rab17 overexpression in Arabidopsis plants promotes osmotic stress tolerance. Ann Appl Biol 144:251-257
54. Finch-Savage WE, Pramanik SK, Bewley JD (1994) The expression of dehydrin proteins in desiccation-sensitive (recalcitrant) seeds of temperate trees. Planta 193:478-485
55. Franz G, Hatzopoulos P, Jones TJ, Krauss, M, Sung ZR (1989) Molecular and genetic analysis of an embryonic gene, DC 8, from Daucus carota L. Mol Gen Genet 218:143-151
56. Gal TZ, Glazer I, Koltai H (2003) Differential gene expression during desiccation stress in the insect killing nematode Steinernema feltiae IS-6. J Parasitol 89:761-766
57. Gal TZ, Glazer I, Koltai H (2004) An LEA group 3 family member is involved in survival of C. elegans during exposure to stress. FEBS Lett 577:21-26
58. Galau GA, Dure L III (1981) Developmental biochemistry of cottonseed embryogenesis and germination: changing messenger ribonucleic acid populations as shown by reciprocal heterologous complementary deoxyribonucleic acid-messenger ribonucleic acid hybridization. Biochemistry 20:4169-4178
59. Galau GA, Hughes DW, Dure L III (1986) Abscisic acid induction of cloned cotton late embryogenesis-abundant (Lea) mRNAs. Plant Mol Biol 7:155-170
60. Galau GA, Wang HY-C, Hughes DW (1993) Cotton Lea5 and Lea14 encode atypical late embryogenesis-abundant proteins. Plant Physiol 101:695-696
61. Garay-Arroyo A, Colmenero-Flores JM, Garciarrubio A, Covarrubias AA (2000) Highly hydrophilic proteins in prokaryotes and eukaryotes are common during conditions of water deficit. J Biol Chem 275:5668-5674
62. Gerstein M (1998) How representative are the known structures of the proteins in a complete genome? A comprehensive structural census. Fold Des 3:497-512
63. Gething MJ, Sambrook J (1992) Protein folding in the cell. Nature 355:33-45
64. Goday A, Jensen AB, Cullanez-Macia FA, Alba MM, Figueras M, Serratosa J, Torrent M, Pages M (1994) The maize abscisic-acid responsive protein Rab17 is located in the nucleus and interacts with nuclear localization signals. Plant Cell 6:351-360
65. Godoy JA, Lunar R, Torres-Schumann S, Moreno J, Rodrigo RM, Pintor-Toro JA (1994) Expression, tissue distribution and subcellular localization of dehydrin TAS14 in salt-stressed tomato plants. Plant Mol Biol 26:1921-1934
66. Goyal K, Tisi L, Basran A, Browne J, Burnell A, Zurdo J, Tunnacliffe A (2003) Transition from natively unfolded to folded state induced by desiccation in an anhydrobiotic nematode protein. J Biol Chem 278:12977-12984
67. Goyal K, Walton LJ, Tunnacliffe A (2005a) LEA proteins prevent protein aggregation due to water stress. Biochem J 388:151-157
68. Goyal K, Pinelli C, Maslen SL, Rastogi RK, Stephens E, Tunnacliffe A (2005b) Dehydration-regulated processing of late embryogenesis abundant protein in a desiccation-tolerant nematode. FEBS Lett 579:4093-4098
69. Grelet J, Benamar A, Teyssier E, Avelange-Macherel M-H, Grunwald D, Macherel D (2005) Identification in pea seed mitochondria of a late-embryogenesis abundant protein able to protect enzymes from drying. Plant Physiol 137:157-167
70. Grossoehme NE, Akilesh S, Guerinot ML, Wilcox DE (2006) Metal-binding thermodynamics of the histidine-rich sequence from the metal-transporter protein ITR1 of Arabidopsis thaliana. Inorg Chem 45:8500-8508
71. Hand SC, Jones D, Menze MW, Witt TL (2006) Life without water: expression of plant LEA genes by an anhydrobiotic arthropod. J Exp Zool 305A:1-5
72. Hara M, Terashima S, Kuboi T (2001) Characterization and cryoprotective activity of cold-responsive dehydrin from Citrus unshiu. J Plant Physiol 158:1333-1339
73. Hara M, Terashima S, Fukaya T, Kuboi T (2003) Enhancement of cold tolerance and inhibition of lipid peroxidation by citrus dehydrin in transgenic tobacco. Planta 217:290-298
74. Hara M, Fujinaga M, Kuboi T (2004) Radical scavenging activity and oxidative modification of citrus dehydrin. Plant Physiol Biochem 42:657-662
75. Hara M, Fujinaga M, Kuboi T (2005) Metal binding by citrus dehydrin with histidine-rich domains. J Exp Bot 56:2695-2703
76. Heazlewood JL, Tonti-Filippini J, Verboom RR, Millar AH (2005) Combining experimental and predicted datasets for determination of subcellular location of proteins in Arabidopsis. Plant Physiol 29:598-609
77. Herzer S, Kinealy K, Asbury R, Beckett P, Eriksson K, Moore P (2003) Purification of native dehydrin from Glycine max cv., Pisum sativum, and Rosmarinum officinalis by affinity chromatography. Protein Expr Purif 28:232-240
78. Heyen BJ, Alsheikh MK, Smith EA, Torvik CF, Seals DF, Randall SK (2002) The calcium-binding activity of a vacuole-associated, dehydrin-like protein is regulated by phosphorylation. Plant Physiol 130:675-687
79. Hoekstra FA, Golovina EA, Buitink J (2001) Mechanisms of plant desiccation tolerance. Trends Plant Sci 6:431-438
80. Holm L, Sander C (1998) Removing near-neighbour redundancy from large protein sequence collections. Bioinformatics 14:423-429
81. Hong B, Barg R, Ho T-HD (1992) Developmental and organ-specific expression of an ABA- and stress-induced protein in barley. Plant Mol Biol 18:663-674
82. Honjoh K-I, Oda Y, Takata R, Miyamoto T, Hatano S (1999) Introduction of the hiC6 gene, which encodes a homologue of a late embryogenesis abundant (LEA) protein, enhances freezing tolerance of yeast. J Plant Physiol 155:509-512
83. Honjoh K-I, Matsumoto H, Shimizu H, Ooyama K, Tanaka K, Oda Y, Takata R, Joh T, Suga K, Miyamoto T, Iio M, Hatano S (2000) Cryoprotective activities of Group 3 late embryogenesis abundant proteins from Chlorella vulgaris C-27. Biosci Biotechnol Biochem 64:1656-1663
84. Houde M, Daniel C, Lachapelle M, Allard F, Laliberté S, Sarhan F (1995) Immunolocalization of freezing-tolerance-associated proteins in the cytoplasm and nucleoplasm of wheat crown tissues. Plant J 8:583-593
85. Houde M, Dallaire S, N'Dong D, Sarhan F (2004) Overexpression of the acidic dehydrin WCOR410 improves freezing tolerance in transgenic strawberry leaves. Plant Biotech J 2:381-387
86. Hsing YC, Chen ZY, Shih MD, Hsieh JS, Chow TY (1995) Unusual sequences of group 3 LEA mRNA inducible by maturation or drying in soybean seeds. Plant Mol Biol 29:863-868
87. Hughes DW, Galau GA (1989) Temporally modular gene expression during cotyledon development. Genes Dev 3:358-369
88. Hundertmark M, Hincha DK (2007) LEA (late embryogenesis abundant) proteins and their encoding genes in Arabidopsis thaliana. Plant Physiol (in press)
89. Illing N, Denby KJ, Collett H, Shen A, Farrant JM (2005) The signature of seeds in resurrection plants: a molecular and physiological comparison of desiccation tolerance in seeds and vegetative tissues. Integr Comp Biol 45:771-787
90. Imai R, Chang L, Ohta A, Bray EA, Takagi M (1996) A lea-class gene of tomato confers salt and freezing tolerance when expressed in Saccharomyces cerevisiae. Gene 170:243-248
91. Irar S, Oliveira E, Pagès M, Goday A (2006) Towards the identification of late-embryogenic-abundant phosphoproteome in Arabidopsis by 2-DE and MS. Proteomics 6:S175-S185
92. Ismail AM, Hall AE, Close TJ (1997) Chilling tolerance during emergence of cowpea associated with a dehydrin and slow electrolyte leakage. Crop Sci 37:1270-1277
93. Ismail AM, Hall AE, Close TJ (1999a) Allelic variation of a dehydrin gene cosegregates with chilling tolerance during seedling emergence. Proc Natl Acad Sci USA 96:13566-13570
94. Ismail AM, Hall AE, Close TJ (1999b) Purification and partial characterization of a dehydrin involved in chilling tolerance during seedling emergence of cowpea. Plant Physiol 120:237-244
95. Iturbe-Ormaetxe I, Escuredo PR, Arrese-Igor C, Becana M (1998) Oxidative damage in pea plants exposed to water deficit or paraquat. Plant Physiol 116:173-181
96. Iturriaga G, Schneider K, Salamini F, Bartels D (1992) Expression of desiccation-related proteins from the resurrection plant Craterostigma plantagineum in transgenic tobacco. Plant Mol Biol 20:555-558
97. Jao CC, Der-Sarkissian A, Chen J, Langen R (2004) Structure of membrane-bound α-synuclein studied by site-directed spin labeling. Proc Natl Acad Sci USA 101:8331-8336
98. Jensen AB, Goday A, Figueras M, Jessop AC, Pagès M (1998) Phosphorylation mediates the nuclear targeting of the maize Rab17 protein. Plant J 13:691-697
99. Kazuoka T, Oeda K (1994) Purification and characterization of COR85-oligomeric complex from cold-acclimated spinach. Plant Cell Physiol 35:601-611
100. Kikawada T, Nakahara Y, Kanamori Y, Iwata KI, Watanabe M, McGee B, Tunnacliffe A, Okuda T (2006) Dehydration-induced expression of LEA proteins in an anhydrobiotic chironomid. Biochem Biophys Res Commun 348:56-61
101. Koag M-C, Fenton RD, Wilkens S, Close TJ (2003) The binding of maize DHN1 to lipid vesicles. Gain of structure and lipid specificity. Plant Physiol 131:309-316
102. Krogh A, Larsson B, von Heijne G, Sonnhammer ELL (2001) Predicting transmembrane protein topology with a hidden Markov model: application to complete genomes. J Mol Biol 305:567-580
103. Krüger C, Berkowitz O, Stephan UW, Hell R (2002) A metal-binding member of the late embryogenesis abundant protein family transports iron in the phloem of Ricinus communis L. J Biol Chem 277:25062-25069
104. Kyte J, Doolittle RF (1982) A simple method for displaying the hydropathic character of a protein. J Mol Biol 157:105-132
105. Lan Y, Cai D, Zheng YZ (2005) Expression in Escherichia coli of three different soybean late embryogenesis abundant (LEA) genes to investigate enhanced stress tolerance. J Int Plant Biol 47:613-621
106. Lång V (1993) The role of ABA and ABA-induced gene expression in cold acclimation of Arabidopsis thaliana. Ph.D. Thesis, Swedish University of Agricultural Sciences, Uppsala, Sweden
107. Levitt J, Scarth GW (1936) Frost hardening studies with living cells. I. Osmotic and bound water changes in relation to frost resistance and the seasonal cycle. II. Permeability in relation to frost resistance and the seasonal cycle. Can J Res C 14:267-305
108. Lin C, Thomashow MF (1992a) A cold-regulated Arabidopsis gene encodes a polypeptide having potent cryoprotective activity. Biochem Biophys Res Commun 183:1103-1108
109. Lin C, Thomashow MF (1992b) DNA sequence analysis of a complementary DNA for cold-regulated Arabidopsis gene cor15 and characterization of the COR15 polypeptide. Plant Physiol 99:519-525
110. Lindquist S (1986) The heat-shock response. Annu Rev Biochem 55:1151-1191
111. Lisse T, Bartels D, Kalbitzer HR, Jaenicke R (1996) The recombinant dehydrin-like desiccation stress protein from the resurrection plant Craterostigma plantagineum displays no defined three-dimensional structure in its native state. Biol Chem 377:555-561
112. Liu Y, Zheng Y (2005) PM2, a group 3 LEA protein from soybean, and its 22-mer repeating region confer salt tolerance in Escherichia coli. Biochem Biophys Res Commun 331:325-332
113. Manfre AJ, Lanni LM, Marcotte WR Jr (2006) The Arabidopsis Group 1 late embryogenesis abundant protein ATEM6 is required for normal seed development. Plant Physiol 140:140-149
114. Marttila S, Tenhola T, Mikkonen A (1996) A barley (Hordeum vulgare L) LEA3 protein, HVA1, is abundant in protein storage vacuoles. Planta 199:602-611
115. McCubbin WD, Kay CM, Lane BG (1985) Hydrodynamic and optical properties of the wheat germ Em protein. Can J Biochem Cell Biol 63:803-811
116. McGee BM (2006) Hydrophilic proteins in the anhydrobiosis of bdelloid rotifers. Ph.D. Thesis. University of Cambridge
117. Mishra VK, Palgunachari MN, Segrest JP, Anantharamaiah GM (1994) Interactions of synthetic peptide analogs of the class A amphipathic helix with lipids. J Biol Chem 269:7185-7191
118. Momma M, Kaneko S, Haraguchi K, Matsukura U (2003) Peptide mapping and assessment of cryoprotective activity of 26/27-kDa dehydrin from soybean seeds. Biosci Biotechnol Biochem 67:1832-1835
119. Mouillon J-M, Gustafsson P, Harryson P (2006) Structural investigation of disordered stress proteins. Comparison of full-length dehydrins with isolated peptides of their conserved segments. Plant Physiol 141:638-650
120. Mukhopadhyay R, Kumar S, Hoh JH (2004) Molecular mechanisms for organizing the neuronal cytoskeleton. BioEssays 26:1017-1025
121. Mundy J, Chua N-H (1988) Abscisic acid and water-stress induce the expression of a novel rice gene. EMBO J 7:2279-2286
122. Nair R, Rost B (2004) LOCnet and LOCtarget: Sub-cellular localization for structural genomics targets. Nucleic Acids Res 32(Database issue):W517-W521
123. Napper DH (1983) Polymeric stabilization of colloidal dispersions. Academic, London
124. NDong C, Danyluk J, Wilson KE, Pocock T, Huner NPA, Sarhan F (2002) Cold-regulated cereal chloroplast late embryogenesis abundant-like proteins. Molecular characterization and functional analyses. Plant Physiol 129:1368-1381
125. Nylander M, Svensson J, Palva ET, Welin BV (2001) Stress-induced accumulation and tissue-specific localization of dehydrins in Arabidopsis thaliana. Plant Mol Biol 45:263-279
126. Oliver MJ, Dowd SE, Zaragoza J, Mauget SA, Payton PR (2004) The rehydration transcriptome of the desiccation-tolerant bryophyte Tortula ruralis: transcript classification and analysis. BMC Genomics 5:89
127. Park B-J, Liu ZC, Kanno A, Kameya T (2005) Genetic improvement of Chinese cabbage for salt and drought tolerance by constitutive expression of a B. napus LEA gene. Plant Sci 169:553-558
128. Pelah D, Cohen E (2005) Cellular response of Chlorella zofingiensis to exogenous selenium. Plant Growth Regul 45:225-232
129. Prilusky J, Felder CE, Zeev-Ben-Mordehai T, Rydberg EH, Man O, Beckmann JS, Silman I, Sussman JL (2005) FoldIndex: a simple tool to predict whether a given protein sequence is intrinsically unfolded. Bioinformatics 21:3435-3438
130. Puhakainen T, Hess MW, Mäkelä P, Svensson J, Heino P, Palva ET (2004) Overexpression of multiple dehydrin genes enhances tolerance to freezing stress in Arabidopsis. Plant Mol Biol 54:743-753
131. Puupponen-Pimia R, Saloheimo M, Vasara T, Ra R, Gaugecz J, Kurten U, Knowles JK, Keranen S, Kauppinen V (1993) Characterization of a birch (Betula pendula Roth.) embryogenic gene, BP8. Plant Mol Biol 23:423-428
132. Reyes JL, Rodrigo M-J, Colmenero-Flores JM, Gil J-V, Garay-Arroyo A, Campos F, Salamini F, Bartels D, Covarrubias AA (2005) Hydrophilins from distant organisms can protect enzymatic activities from water limitation effects in vitro. Plant Cell Environ 28:709-718
133. Riera M, Figueras M, López C, Goday A, Pagès M (2004) Protein kinase CK2 modulates developmental functions of the abscisic acid responsive protein Rab17 from maize. Proc Natl Acad Sci USA 101:9879-9884
134. Rinne PLH, Kaikuranta PLM, van der Plas LHW, van der Schoot C (1999) Dehydrins in cold-acclimated apices of birch (Betula pubescens Ehrh.): production, localization and potential role in rescuing enzyme function during dehydration. Planta 209:377-388
135. Roberts JK, DeSimone NA, Lingle WL, Dure L III (1993) Cellular concentrations and uniformity of cell-type accumulation of two Lea proteins in cotton embryos. Plant Cell 5:769-780
136. Rodrigo MJ, Bockel C, Blervacq AS, Bartels D (2004) The novel gene CpEdi-9 from the resurrection plant C. plantagineum encodes a hydrophilic protein and is expressed in mature seeds as well as in response to dehydration in leaf phloem tissues. Planta 219:579-589
137. Rohila JS, Jain RK, Wu R (2002) Genetic improvement of Basmati rice for salt and drought tolerance by regulated expression of a barley Hva1 cDNA. Plant Sci 163:525-532
138. Röhrig H, Schmidt J, Colby T, Brautigam A, Hufnagel P, Bartels D (2006) Desiccation of the resurrection plant Craterostigma plantagineum induces dynamic changes in protein phosphorylation. Plant Cell Environ 29:1606-1619
139. Russouw PS, Farrant J, Brandt W, Maeder D, Lindsey GG (1995) Isolation and characterization of a heat-soluble protein from pea (Pisum sativum) embryos. Seed Sci Res 5:137-144
140. Russouw PS, Farrant J, Brandt W, Lindsey GG (1997) The most prevalent protein in a heat-treated extract of pea (Pisum sativum) embryos is an LEA group 1 protein; its conformation is not affected by exposure to high temperature. Seed Sci Res 7:117-123
141. Saavedra L, Svensson J, Carballo V, Izmendi D, Welin B, Vidal S (2006) A dehydrin gene in Physcomitrella patens is required for salt and osmotic stress tolerance. Plant J 45:237-249
142. Sales K, Brandt W, Rumbak E, Lindsey G (2000) The LEA-like protein HSP12 in Saccharomyces cerevisiae has a plasma membrane location and protects membranes against desiccation and ethanol-induced stress. Biochim Biophys Acta 1463:267-278
143. Sanchez-Ballesta MT, Rodrigo MJ, Lafuente MT, Granell A, Zacarias L (2004) Dehydrin from Citrus, which confers in vitro dehydration and freezing protection activity, is constitutive and highly expressed in the flavedo of fruit but responsive to cold and water stress in leaves. J Agric Food Chem 52:1950-1957
144. Scheef ED, Fink JL (2003) Fundamentals of protein structure. In: Bourne PE, Weissig H (eds) Structural bioinformatics. Wiley-Liss, Hoboken NJ pp 15-39
145. Shih M-D, Lin S-C, Hsieh J-S, Tsou C-H, Chow T-Y, Lin T-P, Hsing Y-IC (2004) Gene cloning and characterization of a soybean (Glycine max L.) LEA protein, GmPM16. Plant Mol Biol 56:689-703
146. Siminovitch D, Briggs DR (1953) Studies on the chemistry of the living bark of the black locust tree in relation to frost hardiness. IV. Effects of ringing on translocation, protein synthesis and development of hardiness. Plant Physiol 28:177-200
147. Singh S, Cornilescu CC, Tyler RC, Cornilescu G, Tonelli M, Lee MS, Markley JL (2005) Solution structure of a late embryogenesis abundant protein (LEA14) from Arabidopsis thaliana, a cellular stress-related protein. Protein Sci 14:2601-2609
148. Sivamani E, Bahieldin A, Wraith JM, Al-Niemi T, Dyer WE, Ho T-HD, Qu R (2000) Improved biomass productivity and water use efficiency under water deficit conditions in transgenic wheat constitutively expressing the barley HVA1 gene. Plant Sci 155:1-9
149. Small I, Peeters N, Legeai F, Lurin C (2004) Predotar: A tool for rapidly screening proteomes for N-terminal targeting sequences. Proteomics 4:1581-1590
150. Soulages JL, Kim K, Walters C, Cushman JC (2002) Temperature-induced extended helix/random coil transitions in a group 1 late embryogenesis-abundant protein from soybean. Plant Physiol 128:822-832
151. Soulages JL, Kim K, Arrese EL, Walters C, Cushman JC (2003) Conformation of a Group 2 late embryogenesis abundant protein from soybean. Evidence of poly (L-proline)-type II structure. Plant Physiol 131:963-975
152. Stacy RAP, Aalen RB (1998) Identification of sequence homology between the internal hydrophilic repeated motifs of group 1 late-embryogenesis-abundant proteins in plants and hydrophilic repeats of the general stress protein GsiB of Bacillus subtilis. Planta 206:476-478
153. Steponkus PL, Uemura M, Joseph RA, Gilmour SJ, Thomashow MF (1998) Mode of action of the COR15a gene on the freezing tolerance of Arabidopsis thaliana. Proc Natl Acad Sci USA 95:14570-14575
154. Svensson J, Palva ET, Welin B (2000) Purification of recombinant Arabidopsis thaliana dehydrins by metal ion affinity chromatography. Protein Expr Purif 20:169-178
155. Swire-Clark GA, Marcotte WR Jr (1999) The wheat LEA protein Em functions as an osmoprotective moledule in Saccharomyces cerevisiae. Plant Mol Biol 39:117-128
156. Taylor RM, Cuming AC (1993a) Selective proteolysis of the wheat Em polypeptide. Identification of an endopeptidase activity in germinating wheat embryos. FEBS Lett 331:71-75
157. Taylor RM, Cuming AC (1993b) Purification of an endopeptidase that digests the wheat 'Em' protein in vitro, and determination of its cleavage sites. FEBS Lett 331:76-80
158. Tolleter D, Jaquinod M, Mangavel C, Passirani C, Payet N, Avelange-Macherel M-H, Macherel D (2007) Drying reveals structure and function of a plant mitochondrial protein. Plant Cell (in press)
159. Tompa P (2002) Intrinsically unstructured proteins. Trends Biochem Sci 27:527-533
160. Tompa P, Szász C, Buday L (2005) Structural disorder throws new light on moonlighting. Trends Biochem Sci 30:484-489
161. Tompa P, Bánki P, Bokor M, Kamasa P, Kovács, Lasanda G, Tompa K (2006) Protein-water and protein-buffer interactions in the aqueous solution of an intrinsically unstructured plant dehydrin: NMR intensity and DSC aspects. Biophys J 91:2243-2249
162. Tunnacliffe A, Lapinski J, McGee B (2005) A putative LEA protein, but no trehalose, is present in anhydrobiotic bdelloid rotifers. Hydrobiologia 546:315-321
163. Tyson T, Reardon W, Browne JA, Burnell AM (2007) Gene induction by desiccation stress in the entomopathogenic nematode Steinernema carpocapsae reveals parallels with drought tolerance mechanisms in plants. Int J Parasitol (in press)
164. Ukaji N, Kuwabara C, Takezawa D, Arakawa K, Fujikawa S (2001) Cold acclimation-induced WAP27 localized in endoplasmic reticulum in cortical parenchyma cells of mulberry tree was homologous to Group 3 late-embryogenesis abundant proteins. Plant Physiol 126:1588-1597
165. Uversky VN, Gillespie JR, Fink AL (2000) Why are "natively unfolded" proteins unstructured under physiologic conditions? Proteins 41:415-427
166. Vicré M, Farrant JM, Driouich A (2004) Insights into the cellular mechanisms of desiccation tolerance among angiosperm resurrection plant species. Plant Cell Environ 27:1329-1340
167. Walton LJ (2005) The role of the LEA proteins in anhydrobiosis. Ph.D. Thesis. University of Cambridge
168. Welin BV, Olson A, Nylander M, Palva ET (1994) Characterization and differential expression of dhn/lea/rab-like genes during cold acclimation and drought stress in Arabidopsis thaliana. Plant Mol Biol 26:131-144
169. Wise MJ (2003) LEAping to conclusions: a computational reanalysis of late embryogenesis abundant proteins and their possible roles. BMC Bioinformatics 4:52
170. Wise MJ, Tunnacliffe A (2004) POPP the question: what do LEA proteins do? Trends Plant Sci 9:13-17
171. Wisniewsk M, Webb R, Balsamo R, Close TJ, Yu XM, Griffith M (1999) Purification, imunolocalization, cryoprotective, and antifreeze activity of PCA60: a dehydrin from peach (Prunus persica). Physiol Plant 105:600-608
172. Wolkers WF, van Kilsdonk MG, Hoekstra FA (1998) Dehydration-induced conformational changes of poly-L-lysine as influenced by drying rate and carbohydrates. Biochim Biophys Acta 1425:127-136
173. Wolkers WF, McCready S, Brandt WF, Lindsey GG, Hoekstra FA (2001) Isolation and characterization of a D-7 LEA protein from pollen that stabilizes glasses in vitro. Biochim Biophys Acta 1544:196-206
174. Xu D, Duan X, Wang B, Hong B, Ho T-HD, Wu R (1996) Expression of a late embryogenesis abundant protein gene, HVA1, from barley confers tolerance to water defecit and salt stress in transgenic rice. Plant Physiol 110:249-257
175. 3-type dehydrin enhances cold tolerance in transgenic cucumber seedlings. Plant Sci 170:1164-1172
176. Zhang L, Ohta A, Takagi M, Imai R (2000) Expression of plant Group 2 and Group 3 lea genes in Saccharomyces cerevisiae revealed functional divergence among LEA proteins. J Biochem 127:611-616
177. n-type dehydrin gene from bean in response to heavy metals. Mol Biotechnol 32:205-217