Abstract
Dehydrins (DHNs) are part of a large group of highly hydrophilic proteins known as LEA (Late Embryogenesis Abundant). They were originally identified as group II of the LEA proteins. The distinctive feature of all DHNs is a conserved, lysine-rich 15-amino acid domain, EKKGIMDKIKEKLPG, named the K-segment. It is usually present near the C-terminus. Other typical dehydrin features are: a track of Ser residues (the S-segment); a consensus motif, T/VDEYGNP (the Y-segment), located near the N-terminus; and less conserved regions, usually rich in polar amino acids (the Φ-segments). They do not display a well-defined secondary structure. The number and order of the Y-, S-and K-segments define different DHN sub-classes: YnSKn, YnKn, SKn, Kn and KnS. Dehydrins are distributed in a wide range of organisms including the higher plants, algae, yeast and cyanobacteria. They accumulate late in embryogenesis, and in nearly all the vegetative tissues during normal growth conditions and in response to stress leading to cellular dehydration (e.g. drought, low temperature and salinity). DHNs are localized in different cell compartments, such as the cytosol, nucleus, mitochondria, vacuole, and the vicinity of the plasma membrane; however, they are primarily localized to the cytoplasm and nucleus. The precise function of dehydrins has not been established yet, but in vitro experiments revealed that some DHNs (YSKn-type) bind to lipid vesicles that contain acidic phospholipids, and others (KnS) were shown to bind metals and have the ability to scavenge hydroxyl radicals [Asghar, R. et al. Protoplasma 177 (1994) 87–94], protect lipid membranes against peroxidation or display cryoprotective activity towards freezing-sensitive enzymes. The SKn-and K-type seem to be directly involved in cold acclimation processes. The main question arising from the in vitro findings is whether each DHN structural type could possess a specific function and tissue distribution. Much recent in vitro data clearly indicates that dehydrins belonging to different subclasses exhibit distinct functions.
[1] Ingram, J. and Bartels, D. The molecular basis of dehydration tolerance in plants. Annu. Rev. Plant Physiol. Plant Mol. Biol. 47 (1996) 377–403. http://dx.doi.org/10.1146/annurev.arplant.47.1.37710.1146/annurev.arplant.47.1.377Search in Google Scholar PubMed
[2] Allagulova, Ch.R., Gilamov, F.R., Shakirova, F.M. and Vakhitov, V.A. The plant dehydrins: structure and functions. Biochemistry (Moscow) 68 (2003) 945–951. http://dx.doi.org/10.1023/A:102607782558410.1023/A:1026077825584Search in Google Scholar
[3] Garay-Arroyo A., Colmenoro-Florest J.M., Garciarrubio A. and Covarrubias A.A. Highly hydrophilic proteins in prokaryotes and eucaryotes are common during conditions of water deficit. J. Biol. Chem. 275 (2000) 5668–5674. http://dx.doi.org/10.1074/jbc.275.8.566810.1074/jbc.275.8.5668Search in Google Scholar PubMed
[4] Dure, L., Crouch, M., Harada, J., Ho, T.-H.D., Mundy, J., Quatrano, R., Thomas, T. and Sung, Z.R. Common amino acid sequence domains among the LEA proteins of higher plants. Plant Mol. Biol. 12 (1989) 475–486. http://dx.doi.org/10.1007/BF0003696210.1007/BF00036962Search in Google Scholar PubMed
[5] Cuming, A. C. LEA proteins. In Seed Proteins (Shewry, P. R. and Casey, R., Eds.), (1999) pp. 753–780, Kluwer Academic Publishers, Dordrecht. 10.1007/978-94-011-4431-5_32Search in Google Scholar
[6] Bray, E. A. Molecular responses to water deficit. Plant Physiol. 103 (1993) 1035–1040 Search in Google Scholar
[7] Wise, M.J. LEAping to conclusions: a computational reanalysis of late embryogenesis abundant proteins and their possible roles. BMC Bioinform. 4 (2003) 52. http://dx.doi.org/10.1186/1471-2105-4-5210.1186/1471-2105-4-52Search in Google Scholar PubMed PubMed Central
[8] McCubbin, W.D., Kay, C.M. and Lane, B.G. Hydrodynamic and optical properties of the wheat germ Em protein. Can. J. Biochem. Cell Biol. 63 (1985) 803–811. http://dx.doi.org/10.1139/o85-10210.1139/o85-102Search in Google Scholar
[9] DureIII, L. Occurrence of a repeating 11-mer amino acid sequence motif in diverse organisms. Protein Pept. Lett. 8 (2001) 115–122. http://dx.doi.org/10.2174/092986601340964310.2174/0929866013409643Search in Google Scholar
[10] Solomon, A., Salomon, R., Paperna, I. and Glazer, I. Desiccation stress of entomopathogenic nematodes induces the accumulation of a novel heat stable product. Parasitology 121 (2000) 409–416. http://dx.doi.org/10.1017/S003118209900656310.1017/S0031182099006563Search in Google Scholar PubMed
[11] Browne, J., Tunnacliffe, A. and Burnell, A. Plant desiccation gene found in a nematode. Nature (London) 416 (2002) 38. http://dx.doi.org/10.1038/416038a10.1038/416038aSearch in Google Scholar PubMed
[12] Goyal, K., Tisi, L., Basran, A., Browne, J., Burnell, A., Zurdo, J. and Tunnacliffe, A. Transition from natively unfolded to folded state induced by desiccation in an anhydrobiotic nematode protein. J. Biol. Chem. 278 (2003) 12977–12984. http://dx.doi.org/10.1074/jbc.M21200720010.1074/jbc.M212007200Search in Google Scholar PubMed
[13] Wolkers, W.F., McCready, S., Brandt, W.F., Lindsey, G.G. and Hoekstra, F.A. Isolation and characterization of a D-7 LEA protein that stabilizes glasses in vitro. Biochim. Biophys. Acta 1544 (2001) 196–206. Search in Google Scholar
[14] Close, T.J. Dehydrins: A commonality in the response of plants to dehydration and low temperature. Physiol. Plant 100 (1997) 291–296. http://dx.doi.org/10.1111/j.1399-3054.1997.tb04785.x10.1111/j.1399-3054.1997.tb04785.xSearch in Google Scholar
[15] Campbell, S.A. and Close, T.J. Dehydrins: genes, proteins, and association with phenotypic traits. New Phytol. 137 (1997) 61–74. http://dx.doi.org/10.1046/j.1469-8137.1997.00831.x10.1046/j.1469-8137.1997.00831.xSearch in Google Scholar
[16] Li, R., Brawley, S.H. and Close, T.J. Dehydrin-like proteins in fucoid algae. Plant Physiol. 114 (1997) 479–479. Search in Google Scholar
[17] Mitwisha, L., Brandt, W., McCread, L. and Lindsey, G.G. HSP12 is a LEA-like protein in Saccharomyces cerevisiae. Plant Mol. Biol. 37 (1998) 513–521. http://dx.doi.org/10.1023/A:100590421920110.1023/A:1005904219201Search in Google Scholar
[18] Davidson, W.S., Jonas, A., Clayton, D.F. and George, J.M. “Stabilization of alpha-synuclein secondary structure upon binding to synthetic membranes.” J. Biol. Chem. 273 (1998) 9443–9449. http://dx.doi.org/10.1074/jbc.273.16.944310.1074/jbc.273.16.9443Search in Google Scholar PubMed
[19] Segrest, J.P., Deloof, H., Dohlman, J.G., Brouilette C.G. and Anantharamaiah, G.M. Amphipathic helix motif: classes and properties. Proteins Struct. Funct. Genet. 8 (1990) 103–117. http://dx.doi.org/10.1002/prot.34008020210.1002/prot.340080202Search in Google Scholar PubMed
[20] Close, T.J., Kortt, A.A. and Chandler, P.M. A cDNA-Based Comparison of Dehydration-Induced Proteins (Dehydrins) in Barley and Corn. Plant Mol. Biol. 13 (1989) 95–108. http://dx.doi.org/10.1007/BF0002733810.1007/BF00027338Search in Google Scholar PubMed
[21] Lisse, T., Bartels, D., Kalbitzer, H.R. and Jaenicke, R. 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 (1996) 555–561. Search in Google Scholar
[22] Ismail, A.M., Hall, A.E. and Close, T.J. Purification and partial characterization of a dehydrin involved in chilling tolerance during seedling emergence of cowpea. Plant Physiol. 120 (1999a) 237–244. http://dx.doi.org/10.1104/pp.120.1.23710.1104/pp.120.1.237Search in Google Scholar PubMed PubMed Central
[23] Puhakainen, T., Hess, M.V., Mäkela, P., Svenson, J., Heino, P. and Palva, E.T. Overexpression of multiple dehydrin genes enhances tolerance to freezing stress in Arabidopsis. Plant Mol. Biol. 54 (2004) 743–753. http://dx.doi.org/10.1023/B:PLAN.0000040903.66496.a410.1023/B:PLAN.0000040903.66496.a4Search in Google Scholar
[24] Choi, D.W., Zhu, B. and Close, T.J. The barley (Hordeum vulgare L.) dehydrin multigene family: sequences, allele types, chromosome assignments, and expression characteristics of 11 Dhn genes of cv Dicktoo. Theor. Appl. Genet. 98 (1999) 1234–1247. http://dx.doi.org/10.1007/s00122005118910.1007/s001220051189Search in Google Scholar
[25] Rodriguez, E.M., Svenson, J.T., Malatrasi, M., Choi, D.-W and Close, T.J. Barley Dhn13 encodes a KS-type dehydrin with constitutive and stress responsive expression. Theor. Appl. Genet. 110 (2005) 852–858. http://dx.doi.org/10.1007/s00122-004-1877-410.1007/s00122-004-1877-4Search in Google Scholar PubMed
[26] Svenson, J., Ismail, A.M., Palva, E.T and Close, T.J. Dehydrins. In: Sensing, Signalling and Cell Adaptation (Storey, K.B. and Storey, J.M. Eds.), Elsevier Science B.V. (2002) 155–171. Search in Google Scholar
[27] Goday, A., Jensen, A.B., Culianezmacia, F.A., Alba, M.M., Figueras, M., Serratosa, J., Torrent, M. and Pages, M. The maize abscisic acid-responsive protein RAB17 is located in the nucleus and interacts with nuclear-localization signals. Plant Cell 6 (1994) 351–360. http://dx.doi.org/10.1105/tpc.6.3.35110.1105/tpc.6.3.351Search in Google Scholar PubMed PubMed Central
[28] Robertson, M. and Chandler, P.M. A dehydrin cognate protein from pea (Pisum sativum L.) with an atypical pattern of expression. Plant Mol. Biol. 26 (1994) 805–816. http://dx.doi.org/10.1007/BF0002885010.1007/BF00028850Search in Google Scholar PubMed
[29] Kiyosue, T., Yamaguchi-Shinozaki, K., Shinozaki, K., Kamada, H. and Harada, H. cDNA cloning of Ecp40, an embryogenic-cell protein in carrot, and its expression during somatic and zygotic embryogenesis. Plant Mol. Biol. 21 (1993) 1053–1068. http://dx.doi.org/10.1007/BF0002360210.1007/BF00023602Search in Google Scholar PubMed
[30] Momma, M., Haraguchi, K., Saito, M., Chikuni, K. and Harada, K. Purification and characterization of the acid soluble 26-kDa polypeptide from soybean seeds. Biosci. Biotechnol. Biochem. 61 (1997) 1286–1291. http://dx.doi.org/10.1271/bbb.61.128610.1271/bbb.61.1286Search in Google Scholar PubMed
[31] Momma, M., Kaneko, S., Haraguchi, K. and Matsukura, U. Peptide mapping and assessment of cryoprotective activity of 26/27-kDa dehydrin from soybean seeds. Biosci. Biotechnol. Biochem. 67 (2003) 1832–1835. http://dx.doi.org/10.1271/bbb.67.183210.1271/bbb.67.1832Search in Google Scholar PubMed
[32] Nylander, M., Svensson, J., Palva, E.T. and Welin, B.V. Stress-induced accumulation and tissue-specific localisation of dehydrins in Arabidopsis thaliana. Plant Mol. Biol. 45 (2001) 263–279. http://dx.doi.org/10.1023/A:100646912828010.1023/A:1006469128280Search in Google Scholar
[33] Bravo, L.A., Close, T.J., Corcuera, L.J. and Guy, C.L. Characterization of an 80-kDa dehydrin-like protein in barley responsive to cold acclimation. Physiol. Plant. 106 (1999) 177–183. http://dx.doi.org/10.1034/j.1399-3054.1999.106205.x10.1034/j.1399-3054.1999.106205.xSearch in Google Scholar
[34] Houde, M., Daniel, C., Lachapelle, M., Allard, F., Laliberte, S. and Sarhan, F. Immunolocalization of freezing-tolerance-associated proteins in the cytoplasm and nucleoplasm of wheat crown tissues. Plant J. 8 (1995) 583–593. http://dx.doi.org/10.1046/j.1365-313X.1995.8040583.x10.1046/j.1365-313X.1995.8040583.xSearch in Google Scholar
[35] Danyluk, J., Perron, A., Houde, M., Limin, A., Fowler, B., Benhamou, N. and Sarhan, F. Accumulation of an acidic dehydrin in the vicinity of the plasma membrane during cold acclimation of wheat. Plant Cell 10 (1998) 623–638. http://dx.doi.org/10.1105/tpc.10.4.62310.1105/tpc.10.4.623Search in Google Scholar PubMed PubMed Central
[36] Godoy, J.A., Lunar, R., Torresschumann, S., Moreno, J., Rodrigo, R.M. and Pintortoro, J.A. Expression, tissue distribution and subcellular-localization of dehydrin Tas14 in salt-stressed tomato plants. Plant Mol. Biol. 26 (1994) 1921–1934. http://dx.doi.org/10.1007/BF0001950310.1007/BF00019503Search in Google Scholar PubMed
[37] Rorat, T., Grygorowicz, W.J., Irzykowski, W. and Rey, P. Expression of KS-type dehydrins is primarily regulated by factors related to organ type and leaf developmental stage under vegetative growth. Planta 218 (2004) 878–885. http://dx.doi.org/10.1007/s00425-003-1171-810.1007/s00425-003-1171-8Search in Google Scholar PubMed
[38] Rorat, T., Szabala, B.M., Grygorowicz, W.J., Wojtowicz, B., Yin, Z. and Rey, P. Expression of SK3-type dehydrin in transporting organs is associated with cold acclimation in Solanum species. Planta 224 (2006) 205–221. http://dx.doi.org/10.1007/s00425-005-0200-110.1007/s00425-005-0200-1Search in Google Scholar PubMed
[39] Koag, M-C., Fenton, R.D., Wilken, S. and Close, T.J. The binding of maize DHN1 to lipid vesicles. Gain of structure and lipid specificity. Plant. Physiol. 131 (2003) 309–316. http://dx.doi.org/10.1104/pp.01117110.1104/pp.011171Search in Google Scholar PubMed PubMed Central
[40] Krüger, C., Berkowith, O., Stephan, U.W. and Hell, R. A metal-binding member of the late embryogenesis abundant protein family transports iron in the phloem of Ricuinus communis L. J. Biol. Chem. 277 (2002) 25062–25062. http://dx.doi.org/10.1074/jbc.M20189620010.1074/jbc.M201896200Search in Google Scholar PubMed
[41] Hara, M., Fujinaga, M. and Kuboi, T. Metal binding by citrus dehydrin with histidine-rich domains. J. Exp. Bot. 56 (2005) 2695–2703. http://dx.doi.org/10.1093/jxb/eri26210.1093/jxb/eri262Search in Google Scholar PubMed
[42] Hara, M., Fujinaga, M. and Kuboi, T. Radical scavenging activity and oxidative modification of citrus dehydrin. Plant. Physiol. Biol. 42 (2004) 657–662. http://dx.doi.org/10.1016/j.plaphy.2004.06.00410.1016/j.plaphy.2004.06.004Search in Google Scholar PubMed
[43] Hara, M., Terashima, S, Fukaya, T. and Kuboi, T. Enhancement of cold tolerance and inhibition of lipid peroxidation by citrus dehydrin in transgenic tobacco. Planta 217 (2003) 290–298. Search in Google Scholar
[44] Wisniewski, M., Webb, R., Balsamo, R., Close, T.J., Yu, X.M. and Griffith, M. Purification, immunolocalization, cryoprotective, and antifreeze activity of PCA60: A dehydrin from peach (Prunus persica). Physiol. Plant. 105 (1999) 600–608. http://dx.doi.org/10.1034/j.1399-3054.1999.105402.x10.1034/j.1399-3054.1999.105402.xSearch in Google Scholar
[45] Rinne, P.L.H., Kaikuranta, P.L.M., van der Plas, L.H.W. and van der Schoot, C. Dehydrins in cold-acclimated apices of birch (Betula pubescens Ehrh.): production, localization and potential role in rescuing enzyme function during dehydration. Planta 209 (1999) 377–388. http://dx.doi.org/10.1007/s00425005074010.1007/s004250050740Search in Google Scholar PubMed
[46] Hara, M., Terashima, S. and Kuboi, T. Characterization and cryoprotective activity of cold-responsive dehydrin from Citrus unshiu. J. Plant. Physiol. 158 (2001) 1333–1339. http://dx.doi.org/10.1078/0176-1617-0060010.1078/0176-1617-00600Search in Google Scholar
[47] Lang, V. and Palva, E.T. The expression of a RAB-related gene, RAB18, is induced by abscisic-acid during the cold-acclimation process of Arabidopsis thaliana (L) Heynh. Plant Mol. Biol. 20 (1992) 951–962. http://dx.doi.org/10.1007/BF0002716510.1007/BF00027165Search in Google Scholar PubMed
[48] Karlson, D.T., Fujino, T., Kimura, S., Baba, K., Itoh, T. and Ashworth, E.N. Novel plasmodesmata association of dehydrin-like proteins in cold acclimation red-osier dogwood (Cornus sericea). Tree Physiol. 23 (2003) 759–767. Search in Google Scholar
[49] Schneider, K., Wells, B., Schmelzer, E., Salamini, F. and Bartels, D. Desiccation leads to the rapid accumulation of both cytosolic and chloroplastic proteins in the resurrection plant Craterostigma plantagineum Hochst. Planta 189 (1993) 120–131. http://dx.doi.org/10.1007/BF0020135210.1007/BF00201352Search in Google Scholar
[50] Egerton-Warburton, L.M., Balsamo, R.A. and Close, T.J. Temporal accumulation and ultrastructural localization of dehydrins in Zea mays. Physiol. Plant. 101 (1997) 545–555. http://dx.doi.org/10.1111/j.1399-3054.1997.tb01036.x10.1111/j.1399-3054.1997.tb01036.xSearch in Google Scholar
[51] Borovskii, G.B., Stupnikova, I.V., Antipina, A.I. and Voinikov, V.K. Accumulation of protein, immunochemically related to dehydrins in the mitochondria of cold treated plants. Dokl. Akad. Nauk 371 (2000) 251–254. Search in Google Scholar
[52] Heyen, B.J., Alsheikh, M.K., Smith, E.A., Torvik, C.F., Seals, D.F. and Randall, S.K. The calcium-binding activity of a vacuole-associated, dehydrin-like protein is regulated by phosphorylation. Plant Physiol. 130 (2002) 675–687. http://dx.doi.org/10.1104/pp.00255010.1104/pp.002550Search in Google Scholar PubMed PubMed Central
[53] Asghar, R., Fenton, R.D., Demason, D.A. and Close, T.J. Nuclear and cytoplasmic localization of maize embryo and aleurone dehydrin. Protoplasma 177 (1994) 87–94. http://dx.doi.org/10.1007/BF0137898310.1007/BF01378983Search in Google Scholar
[54] Bracale, M., Levi, M., Savini, C., Dicorato, W. and Galli, M.G. Water deficit in pea root tips: Effects on the cell cycle and on the production of dehydrin-like proteins. Ann. Bot. 79 (1997) 593–600. http://dx.doi.org/10.1006/anbo.1996.035610.1006/anbo.1996.0356Search in Google Scholar
[55] Jensen, A.B., Goday, A., Figueras, M., Jessop, A.C. and Pages, M. Phosphorylation mediates the nuclear targeting of the maize RAB17 protein. Plant J. 13 (1998) 691–697. http://dx.doi.org/10.1046/j.1365-313X.1998.00069.x10.1046/j.1365-313X.1998.00069.xSearch in Google Scholar PubMed
[56] Mundy, J. and Chua, N.H. Abscisic acid and water-stress induce the expression of a novel rice gene. Embo J. 7 (1988) 2279–2286. Search in Google Scholar
[57] Neven, L., Haskell, G.D.W., Hofig, A., Li, Q.B. and Guy, C.L. Characterization of a spinach gene responsive to low-temperature and water-stress. Plant Mol. Biol. 21 (1993) 291–305. http://dx.doi.org/10.1007/BF0001994510.1007/BF00019945Search in Google Scholar PubMed
[58] Vilardell, J., Goday, A., Freire, M.A., Torrent, M., Martinez, M.C., Torne, J. M. and Pages, M. Gene, sequence, developmental regulation and protein phosphorylation of RAB17 in maize. Plant Mol. Biol. 14 (1990) 423–432. http://dx.doi.org/10.1007/BF0002877810.1007/BF00028778Search in Google Scholar PubMed
[59] Plana, M., Itarte, E., Eritja, R., Goday, A., Pages, M. and Martinez, M.C. Phosphorylation of maize RAB-17 protein by casein kinase-2. J. Biol. Chem. 266 (1991) 22510–22514. Search in Google Scholar
[60] Alsheikh, M.K., Heyen, B.J., Randall, S.K. Ion binding properties of the dehydrin ERD14 are dependent upon phosphorylation. J. Biol. Chem. 278 (2003) 40882–40889. http://dx.doi.org/10.1074/jbc.M30715120010.1074/jbc.M307151200Search in Google Scholar PubMed
[61] Golan-Goldhirsh, A., Peri, I., Birk, Y. and Smirnoff, P. Inflorescence bud proteins of Pistacia vera. Trees-Struct. Funct. 12 (1998) 415–419. Search in Google Scholar
[62] Levi, A., Panta, G.R., Parmentier, C.M., Muthalif, M.M. Arora, R., Shanker, S. and Rowland, L.J. Complementary DNA cloning, sequencing and expression of an unusual dehydrin from blueberry floral buds. Physiol. Plant. 107 (1999) 98–109. http://dx.doi.org/10.1034/j.1399-3054.1999.100114.x10.1034/j.1399-3054.1999.100114.xSearch in Google Scholar
[63] Sarhan, F., Oullet, F. and Vazquez-Tello, A. The wheat wcs120 gene family: a useful model to understand the molecular genetics of freezing tolerance in cereals. Physiol. Plant. 101 (1997) 439–445. http://dx.doi.org/10.1111/j.1399-3054.1997.tb01019.x10.1111/j.1399-3054.1997.tb01019.xSearch in Google Scholar
[64] Ismail, A.M., Hall, A.E. and Close, T.J. Allelic variation of a dehydrin gene cosegregates with chilling tolerance during seedling emergence. Proc. Natl. Acad. Sci. U. S. A. 96 (1999b) 13566–13570. http://dx.doi.org/10.1073/pnas.96.23.1356610.1073/pnas.96.23.13566Search in Google Scholar
[65] Whitsitt, M.S., Collins, R.G. and Mullet, J.E. Modulation of dehydration tolerance in soybean seedlings. Plant Physiol. 114 (1997) 917–925. Search in Google Scholar
[66] Cellier, F., Conéjéro, G., Breitler, J-C. and Casse, F. Molecular and physiological responses to water deficit in drought-tolerant and drought-sensitive lines of sunflower. Plant Physiol. 116 (1998) 319–328. http://dx.doi.org/10.1104/pp.116.1.31910.1104/pp.116.1.319Search in Google Scholar
[67] Ismail, A.M., Hall, A.E. and Close, T.J. Chilling tolerance during emergence of cowpea associate with a dehydrin and slow electrolyte leakage. Crop Sci. 37 (1997) 1270–1277. http://dx.doi.org/10.2135/cropsci1997.0011183X003700040041x10.2135/cropsci1997.0011183X003700040041xSearch in Google Scholar
[68] Tabaei-Aghdaei, S.R., Harrison, P. and Pearce, R.S. Expression of dehydratio-stress-related genes in the crowns of wheatgresses species [Lophopyrum elongatum (Host) A. Love and Agropyron desertorum (Fisch. Ex Link.) Schult. having contrasting acclimation to salt, cold and drought. Plant Cell Environ. 23 (2000) 561–571. http://dx.doi.org/10.1046/j.1365-3040.2000.00572.x10.1046/j.1365-3040.2000.00572.xSearch in Google Scholar
[69] Zhu, B., Choi, D.W., Fenton, R. and Close, T.J. Expression of the barley dehydrin multigene family and the development of freezing tolerance. Mol. Gen. Genet. 264 (2000) 145–153. http://dx.doi.org/10.1007/s00438000029910.1007/s004380000299Search in Google Scholar
[70] Kaye, C., Neven, L., Hofig, A., Li, Q.B., Haskell, D. and Guy, C. Characterization of a gene for spinach CAP160 and expression of two spinach cold-acclimation proteins in tobacco. Plant Physiol. 116 (1998) 1367–1377. http://dx.doi.org/10.1104/pp.116.4.136710.1104/pp.116.4.1367Search in Google Scholar
[71] Frank, W., Munnik, T., Kerkmann K., Salamini F. and Bartels D. Water deficit triggers phospholipase D activity in the resurrection plant Craterostigma plantagineum. Plant Cell 12 (2000) 111–123. http://dx.doi.org/10.1105/tpc.12.1.11110.1105/tpc.12.1.111Search in Google Scholar
[72] Munnik, T. Phosphatidic acid: an emerging plant lipid second messenger. Trends Plant Sci. 6 (2001) 227–233. http://dx.doi.org/10.1016/S1360-1385(01)01918-510.1016/S1360-1385(01)01918-5Search in Google Scholar
[73] Cullis, P.R., Hope, M.J. and Tilcock C.P.S. Lipid polymorphism and the roles of lipids in membranes. Chem. Phys. Lipids 40 (1986) 127–144 http://dx.doi.org/10.1016/0009-3084(86)90067-810.1016/0009-3084(86)90067-8Search in Google Scholar
[74] Pearce, R.S. Extracellular ice and cell shape in frost-stressed cereals leaves: a low temperature scanning-electron microscopy study. Planta 175 (1988) 313–324. http://dx.doi.org/10.1007/BF0039633610.1007/BF00396336Search in Google Scholar PubMed
[75] Pearce, R.S. and Ashworth E.N. Cell shape and localization of ice in leaves of overwintering wheat during frost stress in the field. Planta 188 (1992) 324–331. http://dx.doi.org/10.1007/BF0019279810.1007/BF00192798Search in Google Scholar PubMed
[76] Welin, B.V., Olson, A., Nylander, M. and Palva, E.T. characterization and differential expression of DHN/LEA/RAB-like genes during cold-acclimation and drought stress in Arabidopsis thaliana. Plant Mol. Biol. 26 (1994) 131–144. http://dx.doi.org/10.1007/BF0003952610.1007/BF00039526Search in Google Scholar PubMed
[77] Houde, M., Danyluk, J., Laliberte, J.F., Rassart, E., Dhindsa, R.S. and Sarhan, F. Cloning, characterization, and expression of a cDNA encoding a 50-kilodalton protein specifically induced by cold-acclimation in wheat. Plant Physiol. 99 (1992) 1381–1387. http://dx.doi.org/10.1104/pp.99.4.138110.1104/pp.99.4.1381Search in Google Scholar PubMed PubMed Central
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