Advertisement

Naturwissenschaften

, Volume 94, Issue 10, pp 791–812 | Cite as

The continuing conundrum of the LEA proteins

  • Alan Tunnacliffe
  • Michael J. Wise
Review

Abstract

Research into late embryogenesis abundant (LEA) proteins has been ongoing for more than 20 years but, although there is a strong association of LEA proteins with abiotic stress tolerance particularly dehydration and cold stress, for most of that time, their function has been entirely obscure. After their initial discovery in plant seeds, three major groups (numbered 1, 2 and 3) of LEA proteins have been described in a range of different plants and plant tissues. Homologues of groups 1 and 3 proteins have also been found in bacteria and in certain invertebrates. In this review, we present some new data, survey the biochemistry, biophysics and bioinformatics of the LEA proteins and highlight several possible functions. These include roles as antioxidants and as membrane and protein stabilisers during water stress, either by direct interaction or by acting as molecular shields. Along with other hydrophilic proteins and compatible solutes, LEA proteins might also serve as “space fillers” to prevent cellular collapse at low water activities. This multifunctional capacity of the LEA proteins is probably attributable in part to their structural plasticity, as they are largely lacking in secondary structure in the fully hydrated state, but can become more folded during water stress and/or through association with membrane surfaces. The challenge now facing researchers investigating these enigmatic proteins is to make sense of the various in vitro defined functions in the living cell: Are the LEA proteins truly multi-talented, or are they still just misunderstood?

Keywords

Anhydrobiosis Desiccation tolerance Drought stress Cold stress Water stress 

Notes

Acknowledgement

We would like to thank Dirk Hincha, David Macherel, Al Warner and Shahin Zibaee for permission to cite results from their laboratories before publication.

References

  1. Alban C, Job D, Douce R (2000) Biotin metabolism in plants. Annu Rev Plant Physiol Plant Mol Biol 51:17–47PubMedGoogle Scholar
  2. Alpert P (2005) The limits and frontiers of desiccation-tolerant life. Integr Comp Biol 45:685–695Google Scholar
  3. Alsheikh MK, Heyen BJ, Randall SK (2003) Ion binding properties of the dehydrin ERD14 are dependent upon phosphorylation. J Biol Chem 278:40882–40889PubMedGoogle Scholar
  4. Alsheikh MK, Svensson JT, Randall SK (2005) Phosphorylation regulated ion-binding is a property shared by the acidic subclass dehydrins. Plant Cell Environ 28:1114–1122Google Scholar
  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 93:13404–13409PubMedGoogle Scholar
  6. Asai GN (1943) A study of frost injury and frost resistance in garden roses. Ph.D. Thesis. Cornell UniversityGoogle Scholar
  7. Asghar R, Fenton RD, DeMason DA, Close TJ (1994) Nuclear and cytoplasmic localization of maize embryo and aleurone dehydrin. Protoplasma 177:87–94Google Scholar
  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 166:855–862Google Scholar
  9. Baker J, Steele C, Dure L III (1988) Sequence and characterization of 6 Lea proteins and their genes from cotton. Plant Mol Biol 11:277–291Google Scholar
  10. Bartels D (2005) Desiccation tolerance studied in the resurrection plant Craterostigma plantagineum. Integr Comp Biol 45:696–701Google Scholar
  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–D141PubMedGoogle Scholar
  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 43:133–139PubMedGoogle Scholar
  13. Berjak P (2006) Unifying perspectives of some mechanisms basic to desiccation tolerance across life forms. Seed Sci Res 16:1–15Google Scholar
  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 49:1925–1933Google Scholar
  15. Blackman SA, Obendorf RL, Leopold AC (1995) Desiccation tolerance in developing soybean seeds—the role of stress proteins. Physiol Plant 93:630–638Google Scholar
  16. Bochicchio B, Tamburro AM (2002) Polyproline II structure in proteins: identification by chiroptical spectroscopies, stability, and functions. Chirality 14:782–792PubMedGoogle Scholar
  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 88:2030–2037PubMedGoogle Scholar
  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 140:1418–1436PubMedGoogle Scholar
  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 118:262–269Google Scholar
  20. Bray EA (1993) Molecular responses to water deficit. Plant Physiol 103:1035–1040PubMedGoogle Scholar
  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 1–23Google Scholar
  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 1158–1203Google Scholar
  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 172:20–28Google Scholar
  24. Browne JA, Tunnacliffe A, Burnell AM (2002) Plant desiccation gene found in a nematode. Nature 416:38PubMedGoogle Scholar
  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 3:966–975PubMedGoogle Scholar
  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 358–364Google Scholar
  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 342:406–413PubMedGoogle Scholar
  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 30:373–383PubMedGoogle Scholar
  29. Ceccardi TL, Meyer NC, Close TJ (1994) Purification of a maize dehydrin. Protein Expr Purif 5:266–269PubMedGoogle Scholar
  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 10:71–82Google Scholar
  31. Clayton DF, George JM (1999) Synucleins in synaptic plasticity and neurodegenerative disorders. J Neurosci Res 58:120–129PubMedGoogle Scholar
  32. Close TJ (1996) Dehydrins: emergence of a biochemical role of a family of plant dehydration proteins. Physiol Plant 97:795–803Google Scholar
  33. Close TJ (1997) Dehydrins: a commonalty in the response of plants to dehydration and low temperature. Physiol Plant 100:291–296Google Scholar
  34. Close TJ, Kortt AA, Chandler PM (1989) A cDNA-based comparison of dehydration-induced proteins (dehydrins) in barley and corn. Plant Mol Biol 13:95–108PubMedGoogle Scholar
  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 3:20–30Google Scholar
  36. Crowe JH, Carpenter JF, Crowe LM (1998) The role of vitrification in anhydrobiosis. Annu Rev Physiol 60:73–103PubMedGoogle Scholar
  37. Cuming AC (1999) LEA proteins. In: Shewry PR, Casey R (eds) Seed proteins. Kluwer, Dordrecht, The Netherlands, pp 753–780Google Scholar
  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 344:20–24PubMedGoogle Scholar
  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 10:623–638PubMedGoogle Scholar
  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 19:26–59Google Scholar
  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 91–103Google Scholar
  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 20:4162–4168PubMedGoogle Scholar
  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 12:475–486Google Scholar
  44. Dyson HJ, Wright PE (2002) Coupling of folding and binding for unstructured proteins. Curr Opin Struct Biol 12:54–60PubMedGoogle Scholar
  45. Edgar RC (2004) MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res 32:1792–1797PubMedGoogle Scholar
  46. Egerton-Warburton LM, Balsamo RA, Close TJ (1997) Temporal accumulation and ultrastructural localization of dehydrins in Zea mays L. Physiol Plant 101:545–555Google Scholar
  47. Eisenberg D (1984) Three-dimensional structure of membrane and surface proteins. Ann Rev Biochem 53:595–623PubMedGoogle Scholar
  48. Ellis RJ (2004) From chloroplasts to chaperones: how one thing led to another. Photosynth Res 80:333–343Google Scholar
  49. Ellis RJ, Vandervies SM (1991) Molecular chaperones. Annu Rev Biochem 60:321–347PubMedGoogle Scholar
  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 115:17–24Google Scholar
  51. Felsenstein J (2004) PHYLIP (Phylogeny Inference Package) version 3.6. Distributed by the author. Department of Genome Sciences, University of Washington, SeattleGoogle Scholar
  52. Felsenstein J, Churchill GA (1996) A hidden Markov model approach to variation among sites in rate of evolution. Mol Biol Evol 13:93–104PubMedGoogle Scholar
  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 144:251–257Google Scholar
  54. Finch-Savage WE, Pramanik SK, Bewley JD (1994) The expression of dehydrin proteins in desiccation-sensitive (recalcitrant) seeds of temperate trees. Planta 193:478–485Google Scholar
  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 218:143–151PubMedGoogle Scholar
  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 89:761–766PubMedGoogle Scholar
  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 577:21–26PubMedGoogle Scholar
  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 20:4169–4178PubMedGoogle Scholar
  59. Galau GA, Hughes DW, Dure L III (1986) Abscisic acid induction of cloned cotton late embryogenesis-abundant (Lea) mRNAs. Plant Mol Biol 7:155–170Google Scholar
  60. Galau GA, Wang HY-C, Hughes DW (1993) Cotton Lea5 and Lea14 encode atypical late embryogenesis-abundant proteins. Plant Physiol 101:695–696PubMedGoogle Scholar
  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 275:5668–5674PubMedGoogle Scholar
  62. Gerstein M (1998) How representative are the known structures of the proteins in a complete genome? A comprehensive structural census. Fold Des 3:497–512PubMedGoogle Scholar
  63. Gething MJ, Sambrook J (1992) Protein folding in the cell. Nature 355:33–45PubMedGoogle Scholar
  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 6:351–360PubMedGoogle Scholar
  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 26:1921–1934PubMedGoogle Scholar
  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 278:12977–12984PubMedGoogle Scholar
  67. Goyal K, Walton LJ, Tunnacliffe A (2005a) LEA proteins prevent protein aggregation due to water stress. Biochem J 388:151–157PubMedGoogle Scholar
  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 579:4093–4098PubMedGoogle Scholar
  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 137:157–167PubMedGoogle Scholar
  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 45:8500–8508PubMedGoogle Scholar
  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:1–5Google Scholar
  72. Hara M, Terashima S, Kuboi T (2001) Characterization and cryoprotective activity of cold-responsive dehydrin from Citrus unshiu. J Plant Physiol 158:1333–1339Google Scholar
  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 217:290–298PubMedGoogle Scholar
  74. Hara M, Fujinaga M, Kuboi T (2004) Radical scavenging activity and oxidative modification of citrus dehydrin. Plant Physiol Biochem 42:657–662PubMedGoogle Scholar
  75. Hara M, Fujinaga M, Kuboi T (2005) Metal binding by citrus dehydrin with histidine-rich domains. J Exp Bot 56:2695–2703PubMedGoogle Scholar
  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 29:598–609Google Scholar
  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 28:232–240PubMedGoogle Scholar
  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 130:675–687PubMedGoogle Scholar
  79. Hoekstra FA, Golovina EA, Buitink J (2001) Mechanisms of plant desiccation tolerance. Trends Plant Sci 6:431–438PubMedGoogle Scholar
  80. Holm L, Sander C (1998) Removing near-neighbour redundancy from large protein sequence collections. Bioinformatics 14:423–429PubMedGoogle Scholar
  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 18:663–674PubMedGoogle Scholar
  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 155:509–512Google Scholar
  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 64:1656–1663PubMedGoogle Scholar
  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 8:583–593PubMedGoogle Scholar
  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 2:381–387Google Scholar
  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 29:863–868PubMedGoogle Scholar
  87. Hughes DW, Galau GA (1989) Temporally modular gene expression during cotyledon development. Genes Dev 3:358–369PubMedGoogle Scholar
  88. Hundertmark M, Hincha DK (2007) LEA (late embryogenesis abundant) proteins and their encoding genes in Arabidopsis thaliana. Plant Physiol (in press)Google Scholar
  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 45:771–787Google Scholar
  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 170:243–248PubMedGoogle Scholar
  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–S185PubMedGoogle Scholar
  92. Ismail AM, Hall AE, Close TJ (1997) Chilling tolerance during emergence of cowpea associated with a dehydrin and slow electrolyte leakage. Crop Sci 37:1270–1277CrossRefGoogle Scholar
  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 96:13566–13570PubMedGoogle Scholar
  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 120:237–244PubMedGoogle Scholar
  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 116:173–181Google Scholar
  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 20:555–558PubMedGoogle Scholar
  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 101:8331–8336PubMedGoogle Scholar
  98. Jensen AB, Goday A, Figueras M, Jessop AC, Pagès M (1998) Phosphorylation mediates the nuclear targeting of the maize Rab17 protein. Plant J 13:691–697PubMedGoogle Scholar
  99. Kazuoka T, Oeda K (1994) Purification and characterization of COR85-oligomeric complex from cold-acclimated spinach. Plant Cell Physiol 35:601–611Google Scholar
  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 348:56–61PubMedGoogle Scholar
  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 131:309–316PubMedGoogle Scholar
  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 305:567–580PubMedGoogle Scholar
  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 277:25062–25069PubMedGoogle Scholar
  104. Kyte J, Doolittle RF (1982) A simple method for displaying the hydropathic character of a protein. J Mol Biol 157:105–132PubMedGoogle Scholar
  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 47:613–621Google Scholar
  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, SwedenGoogle Scholar
  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 14:267–305Google Scholar
  108. Lin C, Thomashow MF (1992a) A cold-regulated Arabidopsis gene encodes a polypeptide having potent cryoprotective activity. Biochem Biophys Res Commun 183:1103–1108PubMedGoogle Scholar
  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 99:519–525PubMedGoogle Scholar
  110. Lindquist S (1986) The heat-shock response. Annu Rev Biochem 55:1151–1191PubMedGoogle Scholar
  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 377:555–561PubMedGoogle Scholar
  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 331:325–332PubMedGoogle Scholar
  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 140:140–149PubMedGoogle Scholar
  114. Marttila S, Tenhola T, Mikkonen A (1996) A barley (Hordeum vulgare L) LEA3 protein, HVA1, is abundant in protein storage vacuoles. Planta 199:602–611Google Scholar
  115. McCubbin WD, Kay CM, Lane BG (1985) Hydrodynamic and optical properties of the wheat germ Em protein. Can J Biochem Cell Biol 63:803–811CrossRefGoogle Scholar
  116. McGee BM (2006) Hydrophilic proteins in the anhydrobiosis of bdelloid rotifers. Ph.D. Thesis. University of CambridgeGoogle Scholar
  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 269:7185–7191PubMedGoogle Scholar
  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 67:1832–1835PubMedGoogle Scholar
  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 141:638–650Google Scholar
  120. Mukhopadhyay R, Kumar S, Hoh JH (2004) Molecular mechanisms for organizing the neuronal cytoskeleton. BioEssays 26:1017–1025PubMedGoogle Scholar
  121. Mundy J, Chua N-H (1988) Abscisic acid and water-stress induce the expression of a novel rice gene. EMBO J 7:2279–2286PubMedGoogle Scholar
  122. Nair R, Rost B (2004) LOCnet and LOCtarget: Sub-cellular localization for structural genomics targets. Nucleic Acids Res 32(Database issue):W517–W521Google Scholar
  123. Napper DH (1983) Polymeric stabilization of colloidal dispersions. Academic, LondonGoogle Scholar
  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 129:1368–1381PubMedGoogle Scholar
  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 45:263–279PubMedGoogle Scholar
  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 5:89PubMedGoogle Scholar
  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 169:553–558Google Scholar
  128. Pelah D, Cohen E (2005) Cellular response of Chlorella zofingiensis to exogenous selenium. Plant Growth Regul 45:225–232Google Scholar
  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 21:3435–3438PubMedGoogle Scholar
  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 54:743–753PubMedGoogle Scholar
  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 23:423–428PubMedGoogle Scholar
  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 28:709–718Google Scholar
  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 101:9879–9884PubMedGoogle Scholar
  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 209:377–388PubMedGoogle Scholar
  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 5:769–780PubMedGoogle Scholar
  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 219:579–589PubMedGoogle Scholar
  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 163:525–532Google Scholar
  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 29:1606–1619PubMedGoogle Scholar
  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 5:137–144CrossRefGoogle Scholar
  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 7:117–123Google Scholar
  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 45:237–249PubMedGoogle Scholar
  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 1463:267–278PubMedGoogle Scholar
  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 52:1950–1957PubMedGoogle Scholar
  144. Scheef ED, Fink JL (2003) Fundamentals of protein structure. In: Bourne PE, Weissig H (eds) Structural bioinformatics. Wiley-Liss, Hoboken NJ pp 15–39Google Scholar
  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 56:689–703PubMedGoogle Scholar
  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 28:177–200PubMedGoogle Scholar
  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 14:2601–2609PubMedGoogle Scholar
  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 155:1–9PubMedGoogle Scholar
  149. Small I, Peeters N, Legeai F, Lurin C (2004) Predotar: A tool for rapidly screening proteomes for N-terminal targeting sequences. Proteomics 4:1581–1590PubMedGoogle Scholar
  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 128:822–832PubMedGoogle Scholar
  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 131:963–975PubMedGoogle Scholar
  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 206:476–478PubMedGoogle Scholar
  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 95:14570–14575PubMedGoogle Scholar
  154. Svensson J, Palva ET, Welin B (2000) Purification of recombinant Arabidopsis thaliana dehydrins by metal ion affinity chromatography. Protein Expr Purif 20:169–178PubMedGoogle Scholar
  155. Swire-Clark GA, Marcotte WR Jr (1999) The wheat LEA protein Em functions as an osmoprotective moledule in Saccharomyces cerevisiae. Plant Mol Biol 39:117–128PubMedGoogle Scholar
  156. Taylor RM, Cuming AC (1993a) Selective proteolysis of the wheat Em polypeptide. Identification of an endopeptidase activity in germinating wheat embryos. FEBS Lett 331:71–75PubMedGoogle Scholar
  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 331:76–80PubMedGoogle Scholar
  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)Google Scholar
  159. Tompa P (2002) Intrinsically unstructured proteins. Trends Biochem Sci 27:527–533PubMedGoogle Scholar
  160. Tompa P, Szász C, Buday L (2005) Structural disorder throws new light on moonlighting. Trends Biochem Sci 30:484–489PubMedGoogle Scholar
  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 91:2243–2249PubMedGoogle Scholar
  162. Tunnacliffe A, Lapinski J, McGee B (2005) A putative LEA protein, but no trehalose, is present in anhydrobiotic bdelloid rotifers. Hydrobiologia 546:315–321Google Scholar
  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)Google Scholar
  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 126:1588–1597PubMedGoogle Scholar
  165. Uversky VN, Gillespie JR, Fink AL (2000) Why are “natively unfolded” proteins unstructured under physiologic conditions? Proteins 41:415–427PubMedGoogle Scholar
  166. Vicré M, Farrant JM, Driouich A (2004) Insights into the cellular mechanisms of desiccation tolerance among angiosperm resurrection plant species. Plant Cell Environ 27:1329–1340Google Scholar
  167. Walton LJ (2005) The role of the LEA proteins in anhydrobiosis. Ph.D. Thesis. University of CambridgeGoogle Scholar
  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 26:131–144PubMedGoogle Scholar
  169. Wise MJ (2003) LEAping to conclusions: a computational reanalysis of late embryogenesis abundant proteins and their possible roles. BMC Bioinformatics 4:52PubMedGoogle Scholar
  170. Wise MJ, Tunnacliffe A (2004) POPP the question: what do LEA proteins do? Trends Plant Sci 9:13–17PubMedGoogle Scholar
  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 105:600–608Google Scholar
  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 1425:127–136PubMedGoogle Scholar
  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 1544:196–206PubMedGoogle Scholar
  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 110:249–257PubMedGoogle Scholar
  175. Yin Z, Rorat T, Szabala BM, Ziólkowska A, Malepszy S (2006) Expression of a Solanum sogarandinum SK3-type dehydrin enhances cold tolerance in transgenic cucumber seedlings. Plant Sci 170:1164–1172Google Scholar
  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 127:611–616PubMedGoogle Scholar
  177. Zhang Y, Li J, Yu F, Cong L, Wang L, Burkard G, Chai T (2006) Cloning and expression analysis of SKn-type dehydrin gene from bean in response to heavy metals. Mol Biotechnol 32:205–217PubMedGoogle Scholar

Copyright information

© Springer-Verlag 2007

Authors and Affiliations

  1. 1.Institute of BiotechnologyUniversity of CambridgeCambridgeUK
  2. 2.Biomolecular, Biomedical and Chemical SciencesUniversity of Western AustraliaPerthAustria

Personalised recommendations