LEA proteins: Versatility of form and function

Topics in Current Genetics

Volumn 21, Issue , 2010, Pages 91-108

  Tunnacliffe, Alan ^a   Hincha, Dirk K ^b   Leprince, Olivier ^c   MacHerel, David ^c  

^a UNIVERSITY OF CAMBRIDGE   (United Kingdom)

^b MAX PLANCK INSTITUTE OF MOLECULAR PLANT PHYSIOLOGY   (Germany)

^c UNIVERSITÉ D'ANGERS   (France)

Author keywords

[No Author keywords available]

Indexed keywords

EID: 77955929428     PISSN: 16102096     EISSN: 16106970     Source Type: Book Series    
DOI: 10.1007/978-3-642-12422-8_6     Document Type: Article

References (97)

1. Alpert P (2006) Constraints of tolerance: why are desiccation-tolerant organisms so small or rare? J Exp Biol 209:1575-1584
2. 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
3. Battaglia M, Olvera-Carrillo Y, Garciarrubio A, Campos F, Covarrubias AA (2008) The enigmatic LEA proteins and other hydrophilins. Plant Physiol 148:6-24
4. 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
5. Ben-Zvi AP, Goloubinoff P (2001) Review: mechanisms of disaggregation and refolding of stable protein aggregates by molecular chaperones. J Struct Biol 135:84-93
6. Bies-Ethève N, Gaubier-Comella P, Debures A, Lasserre E, Jobet E, RaynalM, Cooke R, DelsenyM (2008) Inventory, evolution and expression profiling diversity of the LEA (late embryogenesis abundant) protein gene family in Arabidopsis thaliana. Plant Mol Biol 67:107-124
7. 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 truncatula seeds during germination identifies late embryogenesis abundant proteins associated with desiccation tolerance. Plant Physiol 140:1418-1436
8. Bray EA (1993) Molecular responses to water deficit. Plant Physiol 103:1035-1040
9. Browne JA, Tunnacliffe A, Burnell AM (2002) Plant desiccation gene found in a nematode. Nature 416:38
10. Browne JA, Dolan KM, Tyson T, Goyal K, Tunnacliffe A, Burnell AM (2004) Dehydrationspecific induction of hydrophilic protein genes in the anhydrobiotic nematode Aphelenchus avenae. Eukaryot Cell 3:966-975
11. Buitink J, Leprince O (2004) Glass formation in plant anhydrobiotes: survival in the dry state. Cryobiology 48:215-220
12. Cacela C, Hincha DK (2006) Low amounts of sucrose are sufficient to depress the phase transition temperature of dry phosphatidylcholine, but not for lyoprotection of liposomes. Biophys J 90:2831-2842
13. Caprioli M, Katholm AK, Melone G, Ramløv H, Ricci C, Santo N (2004) Trehalose in desiccated rotifers: a comparison between a bdelloid and a monogonont species. Comp Biochem Physiol 139:527-532
14. Carrari F, Fernie AR, Iusem ND (2004) Heard it through the grapevine? ABA and sugar cross-talk: the ASR story. Trends Plant Sci 9:57-59
15. Chakrabortee S, Boschetti C, Walton LJ, Sarkar S, Rubinsztein DC, Tunnacliffe A (2007) Hydrophilic protein associated with desiccation tolerance exhibits broad protein stabilization function. Proc Natl Acad Sci USA 104:18073-18078
16. Cheah KSE, Osborne DJ (1978) DNA lesions occur with loss of viability in embryos of ageing rye seed. Nature 272:593-599
17. Clegg JS (2001) Cryptobiosis - a peculiar state of biological organization. Comp Biochem Physiol B 128:613-624
18. Close TJ (1996) Dehydrins: emergence of a biochemical role of a family of plant dehydration proteins. Physiol Plant 97:795-803
19. Cristofari G, Darlix JL (2002) The ubiquitous nature of RNA chaperone proteins. Prog Nucleic Acid Res Mol Biol 72:223-268
20. Crowe JH, Carpenter JF, Crowe LM (1998) The role of vitrification in anhydrobiosis. Annu Rev Physiol 60:73-103
21. Cuming AC (1999) LEA proteins. In: Shewry PR, Casey R (eds) Seed proteins. Kluwer, Dordrecht, NL, pp 753-780
22. 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
23. Dure L III (1993a) 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
24. Dure L III (1993b) A repeating 11-mer amino acid motif and plant desiccation. Plant J 3:363-369
25. Dure L III (2001) Occurrence of a repeating 11-mer amino acid sequence motif in diverse organisms. Protein Pept Lett 8:115-122
26. 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
27. 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
28. Egerton-Warburton LM, Balsamo RA, Close TJ (1997) Temporal accumulation and ultrastructural localization of dehydrins in Zea mays. Physiol Plant 101:545-555
29. Eisenberg D (1984) Three-dimensional structure of membrane and surface proteins. Ann Rev Biochem 53:595-623
30. Ellis RJ, Hartl F-U (2003) Protein folding and chaperones. In: Cooper DN (ed) Nature encyclopedia of the human genome. Nature, London, pp 806-810
31. Frankel N, Nunes-Nesi A, Balbo I, Mazuch J, Centeno D, Iusem ND, Fernie AR, Carrari F (2007) ci21A/Asr1 expression influences glucose accumulation in potato tubers. Plant Mol Biol 63:719-730
32. 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
33. 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
34. Goldgur Y, Rom S, Ghirlando R, Shkolnik D, Shadrin N, Konrad Z, Bar-Zvi D (2007) Desiccation and zinc binding induce transition of tomato abscisic acid stress ripening 1, a water stress- and salt stress-regulated plant-specific protein, from unfolded to folded state. Plant Physiol 143:617-628
35. 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
36. Goyal K, Walton LJ, Tunnacliffe A (2005) LEA proteins prevent protein aggregation due to water stress. Biochem J 388:151-157
37. 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
38. Guidetti R, Jönsson KI (2002) Long-term anhydrobiotic survival in semi-terrestrial micrometazoans. J Zool 257:181-187
39. Haaning S, Radutoiu S, Hoffmann SV, Dittmer J, Giehm L, Otzen DE, Stougaard J (2008) An unusual intrinsically disordered protein from the model legume Lotus japonicus stabilizes proteins in vitro. J Biol Chem 283:31142-31152
40. 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
41. Hara M, Fujinaga M, Kuboi T (2004) Radical scavenging activity and oxidative modification of citrus dehydrin. Plant Physiol Biochem 42:657-662
42. Hara M, Fujinaga M, Kuboi T (2005) Metal binding by citrus dehydrin with histidine-rich domains. J Exp Bot 56:2695-2703
43. Hara M, Shinoda Y, Tanaka Y, Kuboi T (2009) DNA binding of citrus dehydrin promoted by zinc ion. Plant Cell Environ 32:532-541
44. Haslbeck M, Walke S, Stromer T, Ehrnsperger M, White HE, Chen S, Saibil HR, Buchner J (1999) Hsp26: a temperature-regulated chaperone. EMBO J 18:6744-6751
45. Haymet ADJ, Ward LG, Harding MM (1999) Winter flounder "antifreeze" proteins: synthesis and ice growth inhibition of analogues that probe the relative importance of hydrophobic and hydrogen-bonding interactions. J Am Chem Soc 121:941-948
46. Haymet ADJ, Ward LG, Harding MM (2001) Hydrophobic analogues of the winter flounder "antifreeze" protein. FEBS Lett 491:285-288
47. Hengherr S, Heyer AG, Koehler HR, Schill RO (2008) Trehalose and anhydrobiosis in tardigrades - evidence for divergence in responses to dehydration. FEBS J 275:281-288
48. Hoekstra FA, Golovina EA, Buitink J (2001) Mechanisms of plant desiccation tolerance. Trends Plant Sci 6:431-438
49. Hundertmark M, Hincha DK (2008) LEA (late embryogenesis abundant) proteins and their encoding genes in Arabidopsis thaliana. BMC Genomics 9:118
50. Ivanyi-Nagy R, Lavergne J-P, Gabus C, Ficheux D, Darlix J-L (2008) RNA chaperoning and intrinsic disorder in the core proteins of Flaviviridae. Nucleic Acids Res 36:712-725
51. Kalifa Y, Gilad A, Konrad Z, Zaccai M, Scolnik PA, Bar-Zvi D (2004) The water- and salt-stress regulated Asr1 gene encodes a zinc-dependent DNA-binding protein. Biochem J 381:373-378
52. Kanias T, Acker JP (2006) Mammalian cell desiccation: facing the challenges. Cell Preserv Technol 4:253-277
53. Koag MC, 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
54. Konrad Z, Bar-Zvi D (2008) Synergism between the chaperone-like activity of the stress regulated ASR1 protein and the osmolyte glycine-betaine. Planta 227:1213-1219
55. Kovacs D, Kalmar E, Torok Z, Tompa P (2008) Chaperone activity of ERD10 and ERD14, two disordered stress-related plant proteins. Plant Physiol 147:381-390
56. Lapinski J, Tunnacliffe A (2003) Anhydrobiosis without trehalose in bdelloid rotifers. FEBS Lett 553:387-390
57. Leprince O, Colson P, Houssier C, Deltour R (1995) Changes in chromatin structure associated with germination of maize and their relation with desiccation tolerance. Plant Cell Environ 18:619-629
58. Lin C, Thomashow MF (1992) A cold-regulated Arabidopsis gene encodes a polypeptide having potent cryoprotective activity. Biochem Biophys Res Commun 183:1103-1108
59. Mattimore V, Battista JR (1996) Radioresistance of Deinococcus radiodurans: functions necessary to survive ionizing radiation are also necessary to survive prolonged desiccation. J Bacteriol 178:633-637
60. McGee BM (2006) Hydrophilic proteins in the anhydrobiosis of bdelloid rotifers. PhD thesis, University of Cambridge
61. Menze MA, Boswell L, Toner M, Hand SC (2009) Occurrence of mitochondria-targeted late embryogenesis abundant (LEA) gene in animals increases organelle resistance to water stress. J Biol Chem 284:10714-10719
62. Minton KW, Karmin P, Hahn GM, Minton AP (1982) Nonspecific stabilization of stress-susceptible proteins by stress-resistant proteins: a model for the biological role of heat shock proteins. Proc Natl Acad Sci USA 79:7107-7111
63. Mouillon J-M, Eriksson SK, Harryson P (2008) Mimicking the plant cell interior under water stress by macromolecular crowding: disordered dehydrin proteins are highly resistant to structural collapse. Plant Physiol 148:1925-1937
64. Mukhopadhyay R, Kumar S, Hoh JH (2004) Molecular mechanisms for organizing the neuronal cytoskeleton. Bioessays 26:1017-1025
65. Nakayama K, Okawa K, Kakizaki T, Inaba T (2008) Evaluation of the protective activities of a late embryogenesis abundant (LEA) related protein, Cor15am, during various stresses in vitro. Biosci Biotechnol Biochem 72:1642-1645
66. Napper DH (1983) Polymeric stabilization of colloidal dispersions. Academic, London
67. Potts M (1994) Desiccation tolerance of prokaryotes. Microbiol Rev 58:755-805
68. Pouchkina-Stantcheva NN, McGee BM, Boschetti C, Tolleter D, Chakrabortee S, Popova AV, Meersman F, Macherel D, Hincha DK, Tunnacliffe A (2007) Functional divergence of former alleles in an ancient asexual invertebrate. Science 318:268-271
69. Ramanjulu S, Bartels D (2002) Drought- and desiccation-induced modulation of gene expression in plants. Plant Cell Environ 25:141-151
70. Rao NK, Roberts EH, Ellis RH (1987) Loss of viability in lettuce seeds and the accumulation of chromosome damage under different conditions of storage. Ann Bot 60:85-96
71. Ratnakumar S, Tunnacliffe A (2006) Intracellular trehalose is neither necessary nor sufficient for desiccation tolerance in yeast. FEMS Yeast Res 6:902-913
72. 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
73. Reyes JL, Campos F, Wei H, Arora R, Yang Y, Karlson DT, Covarrubias AA (2008) Functional dissection of hydrophilins during in vitro freeze protection. Plant Cell Environ 31:1781-1790
74. 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
75. Rohrig 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 29:1606-1617
76. Rohrig H, Colby T, Schmidt J, Harzen A, Facchinelli F, Bartels D (2008) Analysis of desiccationinduced candidate phosphoproteins from Craterostigma plantagineum isolated with a modified metal oxide affinity chromatography procedure. Proteomics 8:3548-3560
77. RoratT (2006) Plant dehydrins - tissue location, structure and function.CellMol BiolLett 11:536-556
78. Sallon S, Solowey E, Cohen Y, Korchinsky R, Egli M, Woodhatch I, Simchoni O, KislevM(2008) Germination, genetics, and growth of an ancient date seed. Science 320:1464
79. 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
80. Segrest JP, Garber DW, Brouillette CG, Harvey SC, Anantharamaiah GM (1994) The amphipathic alpha helix: a multifunctional structural motif in plasma apolipoproteins. Adv Protein Chem 45:303-369
81. Sharon MA, Kozarova A, Clegg JS, Vacratsis PO, Warner AH (2009) Characterization of a group 1 late embryogenesis abundant protein in encysted embryos of the brine shrimp Artemia franciscana. Biochem Cell Biol 87(2):415-430
82. Shen-Miller J, Mudgett MB, Schopf W, Clarke S, Berger R (1995) Exceptional seed longevity and robust growth: ancient sacred lotus from China. Am J Bot 82:1367-1380
83. Shih M-D, Lin SC, Hsieh J-S, Tsou C-H, Chow T-Y, Lin T-P, Hsing Y-C (2004) Gene cloning and characterization of a soybean (Glycine max L.) LEA protein, GmPM16. Plant Mol Biol 56:689-703
84. Shih M, Hoekstra F, Hsing Y (2008) Late embryogenesis abundant proteins. Adv Bot Res 48:211-255
85. Solomon A, Solomon R, Paperna I, Glazer I (2000) Desiccation stress of entomopathogenic nematodes induces the accumulation of a novel heat-stable protein. Parasitology 121:409-416
86. 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
87. 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 19:1580-1589
88. Tompa P (2002) Intrinsically unstructured proteins. Trends Biochem Sci 27:527-533
89. Tompa P, Csermely P (2004) The role of structural disorder in the function of RNA and protein chaperones. FASEB J 18:1169-1175
90. Tompa P, Szász C, Buday L (2005) Structural disorder throws new light on moonlighting. Trends Biochem Sci 30:484-489
91. Tunnacliffe A, Wise MJ (2007) The continuing conundrum of the LEA proteins. Naturwissenschaften 94:791-812
92. 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 37:763-776
93. Uversky VN, Gillespie JR, Fink AL (2000) Why are "natively unfolded" proteins unstructured under physiologic conditions? Proteins 41:415-427
94. von Heijne G (2006) Membrane-protein topology. Nat Rev Mol Cell Biol 7:909-918
95. Wise MJ (2003) LEAping to conclusions: a computational reanalysis of late embryogenesis abundant proteins and their possible roles. BMC Bioinformatics 4:52
96. Wise MJ, Tunnacliffe A (2004) POPP the question: what do LEA proteins do? Trends Plant Sci 9:13-17
97. 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