Skip to main content
SpringerLink
Log in
Book cover

Salt Stress in Plants pp 79–112Cite as

LEA Proteins in Salt Stress Tolerance

  • Chapter
  • First Online:

Abstract

In late embryogenesis, the water content of living cell is reduced tremendously that leads to a state of dehydration and thus, might impose severe irreparable damage to cellular and macromolecular structures. However, the mature orthodox seeds can withstand severe desiccation due to role of osmoprotectants viz., reducing sugars, prolines, glycinebetaines or Late Embryogenesis Abundant (LEA) proteins. These operate on the virtue of intrinsic molecular mechanisms that alleviate multiple abiotic stresses in plants such as protein desiccation, membrane degradation, salt stress and cold and chilling stress. The LEA proteins are a group of versatile, adaptive, hydrophilic proteins considerably defined as ‘molecular shields’ for their anti-stress properties attributable to partial or complete structural randomness. On the basis of their amino acid composition and sequencing, LEA proteins have been clubbed into seven groups that are further sub divided into a number of protein sub families. Out of these, Group 2 LEA proteins called the ‘Dehydrins’ are of prime importance in the plant kingdom. The latent and unique stress remediating characteristics of this class of proteins has been further enhanced by transgenic studies, wherein the target LEA genes have been identified, sequenced to understand their molecular role in plants. Further investigations into the behavior of LEA proteins and mode of their regulation in stressed plants will facilitate in elucidating the function of LEA proteins. The present chapter reviews the versatility and role of LEA proteins in plant stress protection.

This is a preview of subscription content, log in via an institution.

Chapter
USD   29.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD   169.00
Price excludes VAT (USA)
  • Available as EPUB and PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD   219.99
Price excludes VAT (USA)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info
Hardcover Book
USD   219.99
Price excludes VAT (USA)
  • Durable hardcover edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Learn about institutional subscriptions

References

  • Allagulova CR, Gilamov FR, Shakirova FM, Vakhitov VA (2003) The plant dehydrins: structure and functions. Biochem 68:945–951

    CAS  Google Scholar 

  • Alsheikh MK, Heyen BJ, Randall SK (2003) Ion binding properties of the dehydrin ERD14 are dependent upon phosphorylation. J Biol Chem 278:40882–40889

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • Amara I, Odena A, Eliandre Oliveira E, Moreno A, Masmoudi K, Montserrat Pagès M, Goday A (2012) Insights into maize LEA proteins: from proteomics to functional approaches. Plant Cell Physiol 53(2):312–329

    Article  PubMed  CAS  Google Scholar 

  • Amitai-Zeigerson H, Scolnik PA, Bar-Zvi D (1994) Genomic nucleotide sequence of tomato Asr2, a second member of the stress/ripeninginduced Asr1 gene family. Plant Physiol 106:1699–1700

    Article  PubMed  CAS  Google Scholar 

  • Asai GN (1943) A study of frost injury and frost resistance in garden roses. Ph.D. thesis, Cornell University

    Google Scholar 

  • Asghar R, Fenton R, DeMason D, Close T (1994) Nuclear and cytoplasmic localization of maize embryo and aleurone dehydrin. Protoplasma 177:87–94

    Article  CAS  Google Scholar 

  • 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 L.) via cell membrane protection. Plant Sci 166:855–862

    Article  CAS  Google Scholar 

  • Baker J, Steele C, Dure L (1988) Sequence and characterization of 6 LEA proteins and their genes from cotton. Plant Mol Biol 11:277–291

    Article  CAS  Google Scholar 

  • Baker EH, Bradford KJ, Bryant JA, Rost TL (1995) A comparison of desiccation-related proteins (dehydrin and QP47) in pea (Pisum sativum). Seed Sci Res 5:185–193

    Article  CAS  Google Scholar 

  • Bartels D (2005) Desiccation tolerance studied in the resurrection plant Craterostigma plantagineum. Integr Comp Biol 45(5):696–701

    Article  PubMed  CAS  Google Scholar 

  • Battaglia M, Olvera-Carrillo Y, Garciarrubio A, Campos F, Covarrubias AA (2008) The enigmatic LEA proteins and other hydrophilins. Plant Physiol 148:6–24

    Article  PubMed  CAS  Google Scholar 

  • Bies-Etheve N, Gaubier-Comella P, Debures A, Lasserre E, Jobet E, Raynal M, Cooke R, Delseny M (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

    Article  PubMed  CAS  Google Scholar 

  • Bishnoi SK, Kumar B, Rani C, Datta KS, Kumari P, Sheoran IS, Angrish R (2006) Changes in protein profile of pigeonpea genotypes in response to NaCl and boron stress. Biol Plant 50:135–137

    Article  CAS  Google Scholar 

  • Bokor M, Csizmok V, Kovacs D, Banki P, Friedrich P, Tompa P, Tompa K (2005) NMR relaxation studies on the hydrate layer of intrinsically unstructured proteins. Biophys J 88:2030–2037

    Article  PubMed  CAS  Google Scholar 

  • Bray EA (1993) Molecular responses to water deficit. Plant Physiol 103:1035–1040

    PubMed  CAS  Google Scholar 

  • Brini F, Hanin M, Lumbreras V, Irar S, Pages M, Masmondi K (2007) Functional characterization of DHN-5, a dehydrin showing a differential phosphorylation pattern in two Tunisian durum wheat (Triticum durum Desf.). Plant Sci 172:20–28

    Article  CAS  Google Scholar 

  • Browne J, Tunnacliffe A, Burnell A (2002) Plant desiccation gene found in a nematode. Nature 38:416

    Google Scholar 

  • Burrieza HP, Koyro HW, Tosar LM, Kobayashi K, Maldonado S (2012) High salinity induces dehydrin accumulation in Chenopodium quinoa Willd. cv. Hualhuas embryos. Plant Soil 555:1–11

    Article  PubMed  CAS  Google Scholar 

  • Cakir B, Agasse A, Gaillard C, Saumonneau A, Delrot S, Atanassova R (2003) A grape ASR protein involved in sugar and abscisic acid signaling. Plant Cell 15:2165–2180

    Article  PubMed  CAS  Google Scholar 

  • Canel C, Bailey-Serres JN, Roose ML (1995) Pummelo fruit transcript homologous to ripening-induced genes. Plant Physiol 108:1323–1324

    Article  PubMed  CAS  Google Scholar 

  • Caramelo JJ, Iusem ND (2009) When cells lose water: lessons from biophysics and molecular biology. Prog Biophys Mol Biol 99:1–6

    Article  PubMed  CAS  Google Scholar 

  • Carrillo Y, Campos F, Reyers J, Garciarrubio A, Covarrubias AA (2010) Functional analysis of the group 4 late embryogenesis abundant proteins reveals their relevance in the adaptive response during water deficit in Arabdiopsis. Plant Physiol 154:373–390

    Article  CAS  Google Scholar 

  • Carrillo Y, Reyes JR, Covarrubias AA (2011) Late embryogenesis abundant proteins versatile players in the plant adaptation to water limiting environments. Plant Signal Behav 6(4):586–589

    Article  CAS  Google Scholar 

  • Cattivelli L, Bartels D (1990) Molecular cloning and characterization of cold-regulated genes in barley. Plant Physiol 93:1504–1510

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • Chakrabortee S, Tripathi R, Watson M, Schierle GS, Kurniawan DP, Kaminski CF, Wise MJ, Tunnacliffe A (2012) Intrinsically disordered proteins as molecular shields. Mol Biosyst 8(1):210–219

    Article  PubMed  CAS  Google Scholar 

  • Chandra Babu R, Zhang JX, Blum A, Ho DT-H, Wu R, Nguyen HT (2004) HVA1, aLEAgene from barley confers dehydration tolerance in transgenic rice (Oryza sativa L.) via cell membrane protection. Plant Sci 166:855–862

    Article  PubMed  CAS  Google Scholar 

  • Chatelain E, Hundertmark M, Leprince O, Gall SL, Satour P, Penninck SD, Rogniaux H, Buitink J (2012) Temporal profiling of the heat-stable proteome during late maturation of Medicago truncatula seeds identifies a restricted subset of late embryogenesis abundant proteins associated with longevitypce. Plant Cell Environ. doi:10.1111/j.1365-3040.2012.02501.x

    Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • Cherian S, Reddy MP, Ferreira RB (2006) Transgenic plants with improved dehydration stress tolerance: progress and future prospects. Plant Biol 50:481–495

    Article  CAS  Google Scholar 

  • Chourey K, Ramani S, Apte SK (2003) Accumulation of LEA proteins in salt (NaCl) stressed young seedlings of rice (Oryza sativa L.) cultivar Bura Rata and their degradation during recovery from salinity stress. Plant Physiol 160:1165–1174

    Article  CAS  Google Scholar 

  • Clayton DF, George JM (1999) Synucleins in synaptic plasticity and neurodegenerative disorders. J Neurosci Res 58:120–129

    Article  PubMed  CAS  Google Scholar 

  • Close TJ (1996) Dehydrins: emergence of a biochemical role of a family of plant dehydration proteins. Plant Physiol 97:795–803

    Article  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • Cohen A, Plant AL, Moses MS, Bray EA (1991) Organ-specific and environmentally regulated expression of two abscisic acid-induced genes of tomato: nucleotide sequence and analysis of the corresponding cDNAs. Plant Physiol 97:1367–1374

    Article  PubMed  CAS  Google Scholar 

  • Colmenero-Flores JM, Campos F, Garciarrubio A, Covarrubias AA (1997) Characterization of Phaseolus vulgaris cDNA clones responsive to water deficit: identification of a novel late embryogenesis abundant-like protein. Plant Mol Biol 35:393–405

    Article  PubMed  CAS  Google Scholar 

  • Colmenero-Flores JM, Moreno LP, Smith C, Covarrubias AA (1999) PvLEA-18, a member of a new late-embryogenesis-abundant protein family that accumulates during water stress and in the growing regions of well-irrigated bean seedlings. Plant Physiol 120:93–103

    Article  PubMed  CAS  Google Scholar 

  • Cuming AC (1999) LEA proteins. In: Shewry PR, Casey R (eds) Seed proteins. Kluwer, Dordrecht, pp 753–780

    Chapter  Google Scholar 

  • Curry J, Walker-Simmons MK (1993) Unusual sequence of group 3 LEA (II) mRNA inducible by dehydration stress in wheat. Plant Mol Biol 21:907–912

    Article  PubMed  CAS  Google Scholar 

  • Curry J, Morris CF, Walker-Simmons MK (1991) Sequence analysis of a cDNA encoding a group 3 LEA mRNA inducible by ABA or dehydration stress in wheat. Plant Mol Biol 16:1073–1076

    Article  PubMed  CAS  Google Scholar 

  • Dang NX, Hincha DK (2011) Identification of two hydrophilins that contribute to the desiccation and freezing tolerance of yeast (Saccharomyces cerevisiae) cells. Cryobiology 62: 188–193

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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

    PubMed  CAS  Google Scholar 

  • De Souza Filho GA, Ferreira BS, Dias JM, Queiroz KS, Bressan-Smith RE, Oliveira JG, Garcia AB (2003) Accumulation of SALT protein in rice plants as a response to environmental stresses. Plant Sci 164:623–628

    Article  CAS  Google Scholar 

  • Dehaye L, Duval M, Viguier D, Yaxley J, Job D (1997) Cloning and expression of the pea gene encoding SBP65, a seed-specific biotinylated protein. Plant Mol Biol 35:605–621

    Article  PubMed  CAS  Google Scholar 

  • Doczi R, Kondrak M, Kovacs G, Beczner F, Banfalvi Z (2005) Conservation of the drought-inducible DS2 genes and divergences from their ASR paralogues in solanaceous species. Plant Physiol Biochem 43:269–276

    Article  PubMed  CAS  Google Scholar 

  • Dong JZ, Dunstan DI (1997) Characterization of cDNAs representing five abscisic acid-responsive genes associated with somatic embryogenesis in Picea glauca, and their responses to abscisic acid stereostructure. Planta 203:448–453

    Article  PubMed  CAS  Google Scholar 

  • Dunker AK (2001) Intrinsically disordered protein. J Mol Graph Model 19:26–59

    Article  PubMed  CAS  Google Scholar 

  • 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, pp 91–103

    Google Scholar 

  • Dure L III (2001) Occurrence of a repeating 11-mer amino acid sequence motif in diverse organisms. Protein Pept Lett 8:115–122

    Article  CAS  Google Scholar 

  • Dyson HJ, Wright PE (2002) Coupling of folding and binding for unstructured proteins. Curr Opin Struct Biol 12:54–60

    Article  PubMed  CAS  Google Scholar 

  • Eisenberg D (1984) Three-dimensional structure of membrane and surface proteins. Annu Rev Biochem 53:595–623

    Article  PubMed  CAS  Google Scholar 

  • Ellis RJ (2004) From chloroplasts to chaperones: how one thing led to another. Photosynth Res 80:333–343

    Article  CAS  Google Scholar 

  • Eom J, Baker W, Kintanar A, Wurtele ES (1996) The embryo-specific EMB-1 protein of Daucus carota is flexible and unstructured. Plant Sci 115:17–24

    Article  CAS  Google Scholar 

  • Eriksson SK, Kutzer M, Procek J, Gröbner G, Harryson P (2011) Tunable membrane binding of the intrinsically disordered dehydrin Lti30, a cold-induced plant stress protein. Plant Cell 23:2391–2404

    Article  PubMed  CAS  Google Scholar 

  • Espelund M, Saeboe-Larssen S, Hughes DW, Galau GA, Larsen F, Jakobsen KS (1992) Late embryogenesis-abundant genes encoding proteins with different numbers of hydrophilic repeats are regulated differentially by abscisic acid and osmotic stress. Plant J 2: 241–252

    PubMed  CAS  Google Scholar 

  • Farrant JM, Pammenter NW, Berjak P, Farnsworth EJ, Vertucci CW (1996) Presence of dehydrin-like proteins and levels of abscisic acid in recalcitrant (desiccation sensitive) seeds may be related to habitat. Seed Sci Res 6:175–182

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    Article  Google Scholar 

  • Frankel N, Carrari F, Hasson E, Iusem ND (2006) Evolutionary history of the Asr gene family. Gene 378:74–83

    Article  PubMed  CAS  Google Scholar 

  • 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(5):719–730

    Article  PubMed  CAS  Google Scholar 

  • Furuki T, Shimizu T, Chakrabortee S, Yamakawa K, Hatanaka R, Takahashi T, Kikawada T, Okuda T, Mihara H, Tunnacliffe A, Sakurai M (2012) Effects of group 3 LEA protein model peptides on desiccation-induced protein aggregation. Biochim Biophys Acta – Proteins and Proteomics. doi:10.1016/j.bbapap. 2012.04.013

    Google Scholar 

  • Galau GA, Wang HY, Hughes DW (1992) Cotton Lea4 (D19) and LeaA2 (D132) group 1 Lea genes encoding water stress-related proteins containing a 20-amino acid motif. Plant Physiol 99:783–788

    Article  PubMed  CAS  Google Scholar 

  • Galau GA, Wang HY, Hughes DW (1993) Cotton Lea5 and Lea74 encode a typical late embryogenesis-abundant proteins. Plant Physiol 101:695–696

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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(6):1921–1934

    Article  PubMed  CAS  Google Scholar 

  • Golan-Goldhirsh A, Peri I, Birk Y, Smirnoff P (1998) Inflorescence bud proteins of Pistacia vera. Trees-Struct Funct 12:415–419

    Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • Goyal K, Tisi L, Basran A, Browne J, Burnell A, Zurdo J (2003) Transition from natively unfolded to folded state induced by desiccation in an anhydrobiotic nematode protein. J Biol Chem 278:12977–12984

    Article  PubMed  CAS  Google Scholar 

  • Goyal K, Browne JA, Burnell AM, Tunnacliffe A (2005a) Dehydration-induced tps gene transcripts from an anhydrobiotic nematode contain novel spliced leaders and encode atypical GT-20 family proteins. Biochimie 87:565–574

    Article  PubMed  CAS  Google Scholar 

  • Goyal K, Walton LJ, Tunnacliffe A (2005b) LEA proteins prevent protein aggregation due to water stress. Biochem J 388:151–157

    Article  PubMed  CAS  Google Scholar 

  • Grelet J, Benamar A, Teyssier E, Avelange-Macherel MH, 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

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • Hand SC, Menze MA, Toner M, Boswell L, Moore D (2011) LEA proteins during water stress: not just for plants anymore. Annu Rev Physiol 73:115–134

    Article  PubMed  CAS  Google Scholar 

  • Hara M, Terashima S, Kuboi T (2001) Characterization and cryoprotective activity of cold-responsive dehydrin from Citrus unshiu. J Plant Physiol 158:1333–1339

    Article  CAS  Google Scholar 

  • 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

    PubMed  CAS  Google Scholar 

  • Hara M, Fujinaga M, Kuboi T (2004) Radical scavenging activity and oxidative modification of citrus dehydrin. Plant Physiol Biochem 42:657–662

    Article  PubMed  CAS  Google Scholar 

  • Hara M, Fujinaga M, Kuboi T (2005) Metal binding by citrus dehydrin with histidine-rich domains. J Exp Bot 56:2695–2703

    Article  PubMed  CAS  Google Scholar 

  • Harada JJ, DeLisle A, Baden C, Crouch M (1989) Unusual sequence of an abscisic acid inducible mRNA which accumulates late in Brassica napus seed development. Plant Mol Biol 12:395–401

    Article  CAS  Google Scholar 

  • He S, Tan L, Hu Z, Chen G, Wang G, Hu T (2012) Molecular characterization and functional analysis by heterologous expression in E. coli under diverse abiotic stresses for OsLEA5, the atypical hydrophobic LEA protein from Oryza sativa L. Mol Genet Genomics 287:39–54

    Article  PubMed  CAS  Google Scholar 

  • Hellwege EM, Dietz KJ, Hartung W (1996) Abscisic acid causes changes in gene expression involved in the induction of the landform of the liverwort Riccia fluitans L. Planta 198: 423–432

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • Hoekstra FA, Golovina EA, Tetteroo FA, Wolkers WF (2001) Induction of desiccation tolerance in plant somatic embryos: how exclusive is the protective role of sugars? Cryobiology 43:140–150

    Article  PubMed  CAS  Google Scholar 

  • Hollung K, Espelund M, Jakobsen KS (1994) Another Lea B19 gene (group 1 LEA) from barley containing a single 20 amino acid hydrophilic motif. Plant Mol Biol 25:559–564

    Article  PubMed  CAS  Google Scholar 

  • Hong SH, Kim IJ, Yang DC, Chung WI (2002) Characterization of an abscisic acid responsive gene homologue from Cucumis melo. J Exp Bot 53:2271–2272

    Article  PubMed  CAS  Google Scholar 

  • Hong-Bo S, Zong-Suo L, Ming-An S (2005) Lea proteins in higher plants: structure, function, gene expression and regulation. Colloid Surf B 45:131–135

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • Hughes S, Graether SP (2011) Cryoprotective mechanism of a small intrinsically disordered dehydrin protein. Protein Sci 20:42–50

    Article  PubMed  CAS  Google Scholar 

  • Hunault G, Jaspard E (2010) LEAPdb: a database for the late embryogenesis abundant proteins. BMC Genomics 11:221–230

    Article  PubMed  CAS  Google Scholar 

  • Hundertmark M, Hincha DK (2008) LEA (late embryogenesis abundant) proteins and their encoding genes in Arabidopsis thaliana. BMC Genomics 9:118

    Article  PubMed  CAS  Google Scholar 

  • Hundertmark M, Popova AV, Rausch S, Seckler R, Hincha DK (2012) Influence of drying on the secondary structure of intrinsically disordered and globular proteins. Biochem Biophys Res Commun 417:122–128

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • Iusem ND, Bartholomew DM, Hitz WD, Scolnik PA (1993) Tomato (Lycopersicon esculentum) transcript induced by water deficit and ripening. Plant Physiol 102:1353–1354

    Article  PubMed  CAS  Google Scholar 

  • Jensen AB, Goday A, Figueras M, Jessop AC, Pages M (1998) Phosphorylation mediates the nuclear targeting of the maize RAB17 protein. Plant J 13:691–697

    Article  PubMed  CAS  Google Scholar 

  • Joh T, Honjoh K, Yoshimoto M, Funabashi J, Miyamoto T, Hatano S (1995) Molecular-cloning and expression of hardening-induced genes in Chlorella-vulgaris C-27: the most abundant clone encodes a late embryogenesis abundant protein. Plant Cell Physiol 36:85–93

    PubMed  CAS  Google Scholar 

  • Jyothsnakumari G (2005) Studies on biochemical responses and proteome analysis of two high yielding genotypes of mulberry (Morus alba L.) with differential salt sensitivity. Ph.D. thesis, Sri Krishnadevaraya University, Anantapur

    Google Scholar 

  • Jyothsnakumari G, Thippeswamy G, Veeranagamallaiah G, Sudhakar C (2009) Differential expression of LEA proteins in two genotypes of mulberry under salinity. Biol Plant 3(1):145–150

    Article  CAS  Google Scholar 

  • Kalifa Y, Perlson E, Gilad A, Konrad Z, Scolnik PA, Bar-Zvi D (2004) Over-expression of the water and salt stress-regulated Asr1 gene confers an increased salt tolerance. Plant Cell Environ 27:1459–1468

    Article  CAS  Google Scholar 

  • Karlson DT (2001) Characterization and environmental regulation of a 24-kDa Cornus sericea dehydrin-like protein and its relationship to freeze-tolerance. Ph.D. thesis, Purdue University, West Lafayette

    Google Scholar 

  • Karlson DT, Zeng Y, Stirm VE, Joly RJ, Ashworth EN (2003) Photoperiodic regulation of a 24-kDa dehydrin-like proteinin red-osier dogwood (Cornus sericea L.) xylem with relation to freeze-tolerance. Plant Cell Physiol 44:25–34

    Article  PubMed  CAS  Google Scholar 

  • Kermode AR (1997) Approaches to elucidate the basis of desiccation-tolerance in seeds. Seed Sci Res 7:75–95

    Article  PubMed  CAS  Google Scholar 

  • Kim HS, Lee JH, Kim JJ, Kim CH, Jun SS, Hong YN (2005) Molecular and functional characterization of CaLEA6, the gene for a hydrophobic LEA protein from Capsicum annuum. Gene 344:115–123

    Article  PubMed  CAS  Google Scholar 

  • Kim IJ, Lee J, Han JA, Kim CS, Hur Y (2011) Citrus LEA promoter confers fruit proferrential and stress- inducible gene expression in Arabdiopsis. Can J Plant Sci 91:459–466

    Article  CAS  Google Scholar 

  • Kiyosue T, Yamaguchi-Shinozaki K, Shinozaki K, Higashi K, Satoh S, Kamada H, Harada H (1992) Isolation and characterization of a cDNA that encodes ECP31, an embryogenic-cell protein from carrot. Plant Mol Biol 19:239–249

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • Koag MC, Wilkens S, Fenton RD, Resnik J, Vo E, Close TJ (2009) The K-segment of maize DHN1 mediates binding to anionic phospholipid vesicles and concomitant structural changes. Plant Physiol 150:1503–1514

    Article  PubMed  CAS  Google Scholar 

  • Kosová K, Vítámvás P, Prásil IT (2007) The role of dehydrins in plant response to cold. Plant Biol 51(4):601–617

    Article  Google Scholar 

  • Kosová K, Vítámvás P, Prášil IT (2011) Expression of dehydrins in wheat and barley under different temperatures. Plant Sci 180:46–52

    Article  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • Kyte J, Doolittle RF (1982) A simple method for displaying the hydropathic character of a protein. J Mol Biol 157:105–132

    Article  PubMed  CAS  Google Scholar 

  • 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

    Google Scholar 

  • Layton BE, Boyd MB, Tripepi MS, Bitonti BM, Dollahon MNR, Balsamo RA (2010) Dehydration-induced expression of a 31-KDA dehydrin in Polypodium polypdioides (polypodiaceae) may enable large, reversible deformation of cell walls. Am J Bot 97(4):535–544

    Article  PubMed  CAS  Google Scholar 

  • Leprince O, Buitink J (2010) Desiccation tolerance: from genomics to the field. Plant Sci 179:554–564

    Article  CAS  Google Scholar 

  • Levi A, Panta GR, Parmentier CM, Muthalif MM, Arora R, Shanker S, Rowland LJ (1999) Complementary DNA cloning, sequencing and expression of an unusual dehydrin from blueberry floral buds. Plant Physiol 107:98–109

    Article  CAS  Google Scholar 

  • Lin C, Thomashow MF (1992) A cold-regulated Arabidopsis gene encodes a polypeptide having potent cryoprotective activity. Biochem Biophys Res Commun 183:1103–1108

    Article  PubMed  CAS  Google Scholar 

  • Lisse T, Bartels D, Kalbitzer HR, Jaenicke R (1996) The recombinant dehydrinlike desiccation stress protein from the resurrection plant Craterostigma plantagineum displays no defined three-dimensional structure in its native state. Biol Chem 377:555–561

    PubMed  CAS  Google Scholar 

  • Liu Y, Chakrabortee S, Li R, Zheng Y, Tunnacliffe A (2011a) Both plant and animal LEA proteins act as kinetic stabilizers of polyglutamine-dependent protein aggregation. FEBS Lett 585:630–634

    Article  PubMed  CAS  Google Scholar 

  • Liu G, Xu H, Zhang L, Zheng Y (2011b) Fe binding properties of two soybean (Glycine max L.) LEA4 proteins associated with antioxidant activity. Plant Cell Physiol 52(6):994–1002

    Article  PubMed  CAS  Google Scholar 

  • López-Martínez G, Rodríguez-Porrata B, Margalef-Català M, Cordero-Otero R (2012) The STF2p hydrophilin from Saccharomyces cerevisiae is required for dehydration stress tolerance. PLoS One 7:e33324

    Article  PubMed  CAS  Google Scholar 

  • Maitra N, Cushman JC (1994) Isolation and characterization of a drought induced soybean cDNA encoding a D95 family late-embryogenesis abundant protein. Plant Physiol 106:805–806

    Article  PubMed  CAS  Google Scholar 

  • Manfre AJ, LaHatte GA, Climer CR, Marcotte WR (2009) Seed dehydration and the establishment of desiccation tolerance during seed maturation is altered in the Arabidopsis thaliana mutant atem6-1. Plant Cell Physiol 50:243–253

    Article  PubMed  CAS  Google Scholar 

  • Maruyama K, Todaka D, Mizoi J, Yoshida T, Kidokoro S, Matsukura S, Ttakasaki H, Sakurai T, Yamamoto YY, Yoshiwara K, Kojima M, Sakakibara H, Shinozaki K, Shinozaki KY (2012) Identification of Cis-acting promoter elements in cold- and dehydration- induced transcriptional pathways in Arabidopsis, rice, and soybean. DNA Res 19:37–49

    Article  PubMed  CAS  Google Scholar 

  • Maskin L, Maldonado S, Iusem ND (2008) Tomato leaf spatial expression of stress-induced Asr genes. Mol Biol Rep 35:501–505

    Article  PubMed  CAS  Google Scholar 

  • Mbeguie-A-Mbeguie D, Gomez RM, Fils-Lycaon B (1997) Molecular cloning and nucleotide sequence of a protein from apricot fruit (accession no. U82760) homologous to LEC14B protein isolated from Lithospermum gene expression during fruit ripening (PGR 97–161). Plant Physiol 115:1287–1289

    Article  Google Scholar 

  • McCubbin WD, Kay CM, Lane B (1985) Hydrodynamic and optical properties of the wheat germ Em protein. Can J Biochem Cell Biol 63:803–811

    Article  CAS  Google Scholar 

  • Melgar JC, Syvertsen JP, Martínez V, García-Sánchez F (2008) Leaf gas exchange, water relations, nutrient content and growth in citrus and olive seedlings under salinity. Plant Biol 52:385–390

    Article  CAS  Google Scholar 

  • Min DH, Zhang XH, Xu XH, Zhao Y, Chen Y, Li LC, Chen M, Ma YZ (2012) Induction kinetics of a novel stress-related LEA gene in wheat. Plant Mol Biol Rep. doi:10.1007/s11105-012-0446-2

    Google Scholar 

  • 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 Biotech Biochem 67:1832–1835

    Article  CAS  Google Scholar 

  • Moons A, Bauw G, Prinsen E, Van Montagu M, Van der Straeten D (1995) Molecular and physiological responses to abscisic acid and salts in roots of salt-sensitive and salt tolerant Indica rice varieties. Plant Physiol 107:177–186

    Article  PubMed  CAS  Google Scholar 

  • Moons A, Gielen J, Van der Kerckhove J, Van der Straeten D, Gheysen G, Van Montagu M (1997a) An abscisic acid and salt stress responsive rice cDNA from a novel plant gene family. Planta 202:443–454

    Article  PubMed  CAS  Google Scholar 

  • Moons A, Prinsen E, Bauw G, Van Montagu M (1997b) Antagonistic effects of abscisic acid and jasmonates on salt stress inducible transcripts in rice roots. Plant Cell 9:2243–2259

    PubMed  CAS  Google Scholar 

  • Mouillon JM, 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

    Article  PubMed  CAS  Google Scholar 

  • Mueller JK, Heckathorn SA, Fernando D (2003) Identification of a chloroplast dehydrin in leaves of mature plants. Int J Plant Sci 164:535–542

    Article  CAS  Google Scholar 

  • Mukhopadhyay A, Vij S, Tyagi AK (2004) Overexpression of a zinc-finger protein gene from rice confers tolerance to cold, dehydration and salt stress in transgenic tobacco. Proc Natl Acad Sci USA 101:6309–6314

    Article  PubMed  CAS  Google Scholar 

  • Mundy J, Chua NH (1988) Abscisic acid and water-stress induce the expression of a novel rice gene. EMBO J 7:2279–2286

    PubMed  CAS  Google Scholar 

  • Muñoz-Mayor A, Pineda B, Garcia-Abellán JO, Antón T, Garcia-Sogo B, Sanchez-Bel P, Flores FB, Atarés A, Angosto T, Pintor-Toro JA, Moreno V, Bolarin MC (2012) Overexpression of dehydrin tas14 gene improves the osmotic stress imposed by drought and salinity in tomato. J Plant Physiol 169(5):459–468

    Article  PubMed  CAS  Google Scholar 

  • Nakayama K, Okawa K, Kakizaki T, Honma T, Itoh H, Inaba T (2007) Arabidopsis Cor15am is a chloroplast stromal protein that has cryoprotective activity and forms oligomers. Plant Physiol 144:513–523

    Article  PubMed  CAS  Google Scholar 

  • Niknam V, Razavi N, Ebrahimzadeh H, Sharifizadeh B (2006) Effect of NaCl on biomass, protein and proline contents, and antioxidant enzymes in seedlings and calli of two Trigonella species. Plant Biol 50:594–596

    Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • Olvera-Carrillo Y, Reyes JS, Covarrubia AA (2011) Late embryogenesis abundant proteins: versatile players in the plant adaptation to water limiting environments. Plant Signal Behav 6(4):586–589

    Article  PubMed  CAS  Google Scholar 

  • Padmanabhan V, Dias DM, Newton RJ (1997) Expression analysis of a gene family in loblolly pine (Pinus taeda L.) induced by water deficit stress. Plant Mol Biol 35:801–807

    Article  PubMed  CAS  Google Scholar 

  • Panza V, Distéfano AJ, Carjuzaa P, Láinez V, del Vas M, Maldonado S (2007) Detection of dehydrin-like proteins in embryos and endosperm of mature Euterpe edulis seeds. Protoplasma 231:1–5

    Article  PubMed  CAS  Google Scholar 

  • Park JA, Cho SK, Kim JE, Chung HS, Hong JP, Hwang B, Hong CB, Kim WT (2003) Isolation of cDNAs differentially expressed in response to drought stress and characterization of the Ca-LEAL1 gene encoding a new family of atypical LEA-like protein homologue in hot pepper (Capsicum annuum L. cv. Pukang). Plant Sci 165:471–481

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • Piatkowski D, Schneider K, Salamini F, Bartels D (1990) Characterization of five abscisic acid-responsive cDNA clones isolated from the desiccation- tolerant plant Craterostigma plantagineum and their relationship to other water-stress genes. Plant Physiol 94:1682–1688

    Article  PubMed  CAS  Google Scholar 

  • Plana M, Itarte E, Eritja R, Goday A, Pages M, Martinez MC (1991) Phosphorylation of maize RAB-17 protein by casein kinase-2. J Biol Chem 266:22510–22514

    PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • Prieto-Dapena P, Almoguera C, Rojas A, Jordano J (1999) Seed-specific expression patterns and regulation by ABI3 of an unusual late embryogenesis-abundant gene in sunflower. Plant Mol Biol 39:615–627

    Article  PubMed  CAS  Google Scholar 

  • Puhakainen T, Hess MW, Makela P, Svensson J, Heino P, Palva ET (2004) Overexpression of multiple dehydrin genes enhances tolerance to freezing stress in Arabidopsis. Plant Mol Biol 54:743–775

    Article  PubMed  CAS  Google Scholar 

  • Reddy PS, Reddy GM, Pandey P, Chandrasekhar K, Reddy MK (2012) Cloning and molecular characterization of a gene encoding late embryogenesis abundant protein from Pennisetum glaucum: protection against abiotic stresses. Mol Biol Rep 39:7163–7174

    Article  PubMed  CAS  Google Scholar 

  • Reyes JL, Rodrigo MJ, Colmenero-Flores JM, Gil JV, 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

    Article  CAS  Google Scholar 

  • Riccardi F, Gazeau P, Vienne DD, Zivy M (1998) Protein changes in response to progressive water deficit in maize: quantitative variation and polypeptide identification. Plant Physiol 117:1253–1263

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • Roberts JK, DeSimone NA, Lingle WL, Dure L (1993) Cellular concentrations and uniformity of cell-type accumulation of two LEA proteins in cotton embryos. Plant Cell 5:769–780

    PubMed  CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • Romanenko AS, Borovskii GB, Ukolova IV, Lomovatskaya LA (2010) Subcellular localization of dehydrins in wheat plant seedlings subjected to low-temperature adaptation. Biochem (Moscow) suppl ser A: Membr Cell Biol. doi:10.1134/S 1990747810020066

    Google Scholar 

  • Romo S, Labrador E, Dopico B (2001) Water stress-regulated gene expression in Cicer arietinum seedlings and plants. Plant Physiol Biochem 39:1017–1026

    Article  CAS  Google Scholar 

  • Rorat T (2006) Plant dehydrins: tissue location, structure and function. Cel Mol Biol Lett 11:536–556

    Article  CAS  Google Scholar 

  • Rorat T, Szabala BM, Grygorowicz WJ, Wojtowicz B, Yin Z, Rey P (2006) Expression of SK3-type dehydrin in transporting organs is associated with cold acclimation in Solanum species. Planta 224:205–221

    Article  PubMed  CAS  Google Scholar 

  • 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 I protein: its conformation is not affected by exposure to high temperature. Seed Sci Res 7:117–123

    Article  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • Salleh MF, Evans K, Goodall B, Machin H, Mowla S, Mur L, Runions J, Theodoulou F, Foyer C, Rogers H (2011) A novel function for a redox-related LEA protein (SAG21/AtLEA5) in root development and biotic stress responses. Plant Cell Environ 35:418–429

    Article  PubMed  CAS  Google Scholar 

  • Salmi ML, Bushart TJ, Stout SC, Roux SJ (2005) Profile and analysis of gene expression changes during early development in germinating spores of Ceratopteris richardii. Plant Physiol 138:1734–1745

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • Sarnighausen E, Karlson D, Ashworth E (2002) Seasonal regulation of a 24-kDa protein from red-osier dogwood (Cornus sericea L.) xylem. Tree Physiol 22:423–430

    Article  PubMed  CAS  Google Scholar 

  • Scheef ED, Fink JL (2003) Fundamentals of protein structure. In: Bourne PE, Weissig H (eds) Structural bioinformatics. Wiley- Liss, Hoboken, pp 15–39

    Google Scholar 

  • Segrest JP, Deloof H, Dohlman JG, Brouilette CG, Anantharamaiah GM (1990) Amphipathic helix motif: classes and properties. Proteins Struct Funct Genet 8:103–117

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • Shih MD, Linm SC, Hsieh JS, Tsou CH, Chow TY, Lin TP (2004) Gene cloning and characterization of a soybean (Glycine max L.) LEA protein, GmPM16. Plant Mol Biol 56:689–703

    Article  PubMed  CAS  Google Scholar 

  • Shih M, Hoekstra F, Hsing Y (2008) Late embryogenesis abundant proteins. Adv Bot Res 48:211–255

    Article  CAS  Google Scholar 

  • Shih MD, Huang LT, Wei FJ, Wu MT, Hoekstra FA, Hsing YC (2010) OsLEA1a, a new Em-like protein of cereal plants. Plant Cell Physiol 51(12):2132–2144

    Article  PubMed  CAS  Google Scholar 

  • Silhavy D, Hutvagner G, Barta E, Banfalvi Z (1995) Isolation and characterization of a water-stress-inducible cDNA clone from Solanum chacoense. Plant Mol Biol 27:587–595

    Article  PubMed  CAS  Google Scholar 

  • 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 the development of hardiness. Plant Physiol 28:177–200

    Article  PubMed  CAS  Google Scholar 

  • Singh J, Whitwill S, Lacroix G, Douglas J, Dubuc E, Allard G, Keller W, Schernthaner JP (2009) The use of group 3 LEA proteins as fusion partners in facilitating recombinant expression of recalcitrant proteins in E. coli. Protein Expr Purif 67(1):15–22

    Article  PubMed  CAS  Google Scholar 

  • Sivamani E, Bahieldin A, Wraith JM, Al-Niemi T, Dyer WE, Ho T-H D, 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

    Article  PubMed  CAS  Google Scholar 

  • Sotiropoulos TE (2007) Effect of NaCl and CaCl2 on growth and contents of minerals, chlorophyll, proline and sugars in the apple rootstock M4 cultured in vitro. Plant Biol 51:177–180

    Article  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • Stacy RAP, Nordeng TW, Culianez-Macia FA, Aalen RB (1999) The dormancy-related peroxiredoxin anti-oxidant, PER1, is localized to the nucleus of barley embryo and aleurone cells. Plant J 19:1–8

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • Svensson J, Palva ET, Welin B (2000) Purification of recombinant Arabidopsis thaliana dehydrins by metal ion affinity chromatography. Protein Expr Purif 20:169–178

    Article  PubMed  CAS  Google Scholar 

  • Svensson J, Ismail AM, Palva ET, Close TJ (2002) Dehydrins. In: Storey KB, Storey JM (eds) Sensing, signaling and cell adaptation. Elsevier Science, Amsterdam, pp 155–171

    Chapter  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • Tantos A, Friedrich P, Tompa P (2009) Cold stability of intrinsically disordered proteins. FEBS Lett 583:465–469

    Article  PubMed  CAS  Google Scholar 

  • Todaka D, Nakashima K, Shinozaki K, Shinozaki KY (2012) Toward understanding transcriptional regulatory networks in abiotic stress responses and tolerance in rice. Rice 5:6

    Article  Google Scholar 

  • Tolleter D, Jaquinod M, Mangavel C, Passirani C, Saulnier P, Manon S, Teyssier E, Payet N, Avelange-Macherel MH, Macherel D (2007) Structure and function of a mitochondrial late embryogenesis abundant protein are revealed by desiccation. Plant Cell 19:1580–1589

    Article  PubMed  CAS  Google Scholar 

  • Tolleter D, Hincha DK, Macherel D (2010) A mitochondrial late embryogenesis abundant protein stabilizes model membranes in the dry state. Biochim Biophys Acta 1798:1926–1933

    Article  PubMed  CAS  Google Scholar 

  • Tompa P (2002) Intrinsically unstructured proteins. Trends Biochem Sci 27:527–533

    Article  PubMed  CAS  Google Scholar 

  • Tompa P (2005) The interplay between structure and function in intrinsically unstructured proteins. FEBS Lett 579:3346–3354

    Article  PubMed  CAS  Google Scholar 

  • Tompa P, Kovacs D (2010) Intrinsically disordered chaperones in plants and animals. Biochem Cell Biol 88(2):167–174

    Article  PubMed  CAS  Google Scholar 

  • Tunnacliffe A, Wise MJ (2007) The continuing conundrum of the LEA proteins. Naturwissenschaften 94:791–812

    Article  PubMed  CAS  Google Scholar 

  • Tunnacliffe A, Hincha DK, Leprince O, Macherel M (2010) LEA proteins: versatility of form and function. In: Lubzens E, Cerda J, Clark MS (eds) Dormancy and resistance in harsh environments. Springer, Berlin/Heidelberg, pp 91–108

    Chapter  Google Scholar 

  • Ulrich TU, Wurtele ES, Nikolau BJ (1990) Sequence of EMB-1, an mRNA accumulating specifically in embryos of carrot. Nucleic Acids Res 18:2826

    Article  PubMed  CAS  Google Scholar 

  • Uversky VN, Gillespie JR, Fink AL (2000) Why are “natively unfolded” proteins unstructured under physiologic conditions. Proteins 41:415–427

    Article  PubMed  CAS  Google Scholar 

  • Vaidyanathan R, Kuruvilla S, Thomas G (1999) Characterization and expression pattern of an abscisic acid and osmotic stress responsive gene from rice. Plant Sci 140:21–30

    Article  CAS  Google Scholar 

  • Veeranagamalliaiah G, Prasanthi J, Reddy KE, Pandurangaiah M, Babu OS, Sudhakar C (2011) Group 1 and 2 LEA protein expression correlates with a decrease in water stress induced protein aggregation in horsegram during germination and seedling growth. J Plant Physiol 168(7):671–677

    Article  CAS  Google Scholar 

  • Vicient CM, Hull G, Guilleminot J, Devic M, Delseny M (2000) Differential expression of the Arabidopsis genes coding for Em-like proteins. J Exp Bot 51:1211–1220

    Article  PubMed  CAS  Google Scholar 

  • Vilardell J, Goday A, Freire MA, Torrent M, Martinez MC, Torne JM, Pages M (1990) Gene, sequence, developmental regulation and protein phosphorylation of RAB17 in maize. Plant Mol Biol 14:423–432

    Article  PubMed  CAS  Google Scholar 

  • Viner RI, Clegg JS (2000) Influence of trehalose on the molecular chaperone activity of p26, a small heat shock/alpha-crystallin protein. Cell Stress Chaperones 6:126–135

    Article  Google Scholar 

  • Wahid A, Close TJ (2007) Expression of dehydrins under heat stress and their relationship with water relations of sugarcane leaves. Plant Biol 51:104–109

    Article  CAS  Google Scholar 

  • Wang CS, Liau YE, Huang JC, Wu TD, Su CC, Lin CH (1998) Characterization of a desiccation-related protein in lily pollen during development and stress. Plant Cell Physiol 39(12):1307–1314

    Article  CAS  Google Scholar 

  • Wang Y, Jiang J, Zhao X, Liu G, Yang C, Zhan L (2006) A novel LEA gene from Tamarix androssowii confers drought tolerance in transgenic tobacco. Plant Sci 171:655–662

    Article  CAS  Google Scholar 

  • Welin BV, Olson A, Nylander M, Palva ET (1994) Characterisation and differential expression of DHN/LEA/RAB-like genes during cold-acclimation and drought stress in Arabidopsis thaliana. Plant Mol Biol 26:131–144

    Article  PubMed  CAS  Google Scholar 

  • Welling A, Rinne P, Vihera-Aarnio A, Kontunen-Soppela S, Heino P, Palva ET (2004) Photoperiod and temperature differentially regulate the expression of two dehydrin genes during overwintering of birch (Betula pubescens Ehrh.). J Exp Bot 55:507–516

    Article  PubMed  CAS  Google Scholar 

  • Williams BA, Tsang A (1994) Analysis of multiple classes of abscisic acid responsive genes during embryogenesis in Zea mays. Dev Genet 15:415–424

    Article  CAS  Google Scholar 

  • Wise MJ (2003) LEAping to conclusions: a computational reanalysis of late embryogenesis abundant proteins and their possible roles. BMC Bioinformatics 4:52

    Article  PubMed  Google Scholar 

  • Wise MJ, Tunnacliffe A (2004) POPP the question: what do LEA proteins do? Trends Plant Sci 9:13–17

    Article  PubMed  CAS  Google Scholar 

  • Wisniewski M, Webb R, Balsamo R, Close TJ, Yu XM, Griffith M (1999) Purification, immunolocalization, cryoprotective, and antifreeze activity of PCA60: a dehydrin from peach (Prunus persica). Plant Physiol 105:600–608

    Article  CAS  Google Scholar 

  • Wolkers WF, McCready S, Brandt WF, Lindsey GG, Hoekstra FA (2001) Isolation and characterization of a D-7 LEA protein that stabilizes glasses in vitro. Biochim Biophys Acta 1544:196–206

    Article  PubMed  CAS  Google Scholar 

  • Wurtele ES, Wang H, Durgerian S, Nikolau BJ, Ulrich TH (1993) Characterization of a gene that is expressed early in somatic embryogenesis of Daucus carota. Plant Physiol 102:303–312

    Article  PubMed  CAS  Google Scholar 

  • 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 deficit and salt stress in transgenic rice. Plant Physiol 110:249–257

    PubMed  CAS  Google Scholar 

  • Yang L, Zheng B, Mao C, Qi X, Liu F, Wu P (2004) Analysis of transcripts that are differentially expressed in three sectors of the rice root system under water deficit. Mol Genet Genomics 272:433–442

    Article  PubMed  CAS  Google Scholar 

  • 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 170:1164–1172

    Article  CAS  Google Scholar 

  • Yoshida Y, Sato T, Hashimoto T, Ichikawa N, Nakai S, Yoshikawa H, Imamoto F, Tagawa K (1990) Isolation of a gene for a regulatory 15-kDa subunit of mitochondrial F1F0-ATPase and construction of mutant yeast lacking the protein. Eur J Biochem 192:49–53

    Article  PubMed  CAS  Google Scholar 

  • Zegzouti H, Jones B, Marty C, Lelievre JM, Latche A, Pech JC, Bouzayen M (1997) ER5, a tomato cDNA encoding an ethylene-responsive LEA like protein: characterization and expression in response to drought, ABA and wounding. Plant Mol Biol 35:847–854

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • Zhao PS, Liu F, Chang G, Zheng C, Liu H (2011) Group 3 late embryogenesis abundant protein in Arabidopsis: structure, regulation, and function. Acta Physiol Plant 3:1063–1073

    Article  CAS  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Department of Botanical and Environmental Sciences, Guru Nanak Dev University, Amritsar, 143005, Punjab, India

    Renu Bhardwaj, Indu Sharma, Mukesh Kanwar, Resham Sharma, Neha Handa, Harpreet Kaur, Dhriti Kapoor &  Poonam

Authors
  1. Renu Bhardwaj
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Indu Sharma
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Mukesh Kanwar
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Resham Sharma
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Neha Handa
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Harpreet Kaur
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Dhriti Kapoor
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Poonam
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Renu Bhardwaj .

Editor information

Editors and Affiliations

  1. Department of Botany A.S. College, University of Kashmir, Srinagar, India

    Parvaiz Ahmad

  2. Department of Botany Faculty of Science, South Valley University, Qena, Egypt

    M. M. Azooz

  3. Department of Biological Sciences Faculty of Science, King Faisal University, Al Hassa, Saudi Arabia

    M. M. Azooz

  4. Department of Plant Sciences, University of Hyderabad, Hyderabad, India

    M. N. V. Prasad

Rights and permissions

Reprints and permissions

Copyright information

© 2013 Springer Science+Business Media New York

About this chapter

Cite this chapter

Bhardwaj, R. et al. (2013). LEA Proteins in Salt Stress Tolerance. In: Ahmad, P., Azooz, M.M., Prasad, M.N.V. (eds) Salt Stress in Plants. Springer, New York, NY. https://doi.org/10.1007/978-1-4614-6108-1_5

Download citation

Publish with us

Policies and ethics

Search

Navigation