Abstract
The expression of a gene, encoding a dehydrin protein designated as DHN24 was analyzed at the protein level in two groups of Solanum species differing in cold acclimation ability. The DHN24 protein displays consensus amino acid sequences of dehydrins, termed K- and S-segments. The S-segment precedes three K-segments, classifying the protein into SK3-type dehydrins. A group of Solanum species able to cold acclimation constituted by S. sogarandinum and S. tuberosum, cv. Aster, and a second one composed of a S. sogarandinum line, that lost ability to cold acclimation, and of S. tuberosum, cv. Irga, displaying low ability to cold acclimation were studied. Under control conditions, noticeable levels of the DHN24 protein was observed in stems, tubers, and roots of Solanum species. No protein was detected in leaves. During low temperature treatment the DHN24 protein level substantially increased in tubers, in transporting organs and in apical parts, and only a small increase was observed in leaves. The increase in protein abundance was only observed in the plants able to cold acclimate and was found to parallel the acclimation capacity. Upon drought stress, the DHN24 level decreased in stems and in leaves, but increased in apical parts. These results suggest that Dhn24 expression is regulated by organ specific factors in the absence of stress and by factors related to cold acclimation processes during low temperature treatment in collaboration with organ-specific factors. A putative function of the SK3-type dehydrin proteins during plant growth and in the tolerance to low temperature is discussed.
Similar content being viewed by others
Abbreviations
- DHN24:
-
Dehydrin protein of 24 kDa
- SK3-type dehydrin:
-
Dehydrin containing a single S-segment followed by three K-segments
- LEA:
-
Late embryogenesis abundant
References
Alsheikh MK, Heyen BJ, Randall SK (2003) Ion binding properties of the dehydrin ERD14 are dependent upon phosphorylation. J Biol Chem 278:40882–40889
Borovskii GB, Stupnikova IV, Antipina AA, Downs CA, Voinikov VK (2000) Accumulation of dehydrin-like proteins in the mitochondria of cold-treated plants. J Plant Physiol 156:797–800
Bravo LA, Close TJ, Corcuera LJ, Guy CL (1999) Characterisation of an 80-kDa dehydrin-like protein in barley responsive to cold acclimation. Physiol Plant 106:177–183
Campbell SA, Close TJ (1997) Dehydrins: genes, proteins, and association with phenotypic traits. New Phytol 137:61–74
Cellier F, Conéjéro G, Breitler J-C, Casse F (1998) Molecular and physiological responses to water deficit in drought-tolerant and drought-sensitive lines of sunflower. Plant Physiol 116:319–328
Chen RD, Campeau N, Greer AF, Bellemare G, Tabaeizadeh Z (1993) Sequence of a novel abscisic acid- and drought-induced cDNA from wild tomato (Lycopersicon chilense). Plant Physiol 103:301
Chinnusamy V, Ohta M, Kanrar S, Lee BH, Hong X, Agarwal M, Zhu JK (2003) ICE1: a regulator of cold-induced transcriptome and freezing tolerance in Arabidopsis. Genes Dev 17:1043–1054
Chung F, Kim S-Y, Yi SY, Choi D (2003) Capsicum annum dehydrin, an osmotic-stress gene in hot paper plants. Mol Cells 15:327–332
Close TJ (1996) Dehydrins: emergence of a biochemical role of a family of plant dehydration proteins. Physiol Plant 97:795–803
Close TJ (1997) Dehydrins: a commonality in the response of plants to dehydration and low temperature. Physiol Plant 100:291–296
Danyluk J, Perron A, Houde M, Lamin A, Flower 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
Davidson WS, Jonas A, Clayton DF, George JM (1998) Stabilization of alpha-synuclein secondary structure upon binding to synthetic membranes. J Biol Chem 273:9443–9449
Degenhardt J, Tobin EM (1996) A DNA binding activity for one of two closely defined phytochrome regulatory elements in an Lhcb promoter is more abundant in etiolated than in green plants. Plant Cell 8:31–41
Dubouzet JG, Sakuma Y, Ito Y, Kasuga M, Dubouzet EG, Miura S, Seki M, Shinozaki K, Yamaguchi-Shinozaki K (2003) OsDREB genes in rice, Oryza sativa L., encode transcription activators that function in drought-, high-salt- and cold-responsive gene expression. Plant J 33:751–763
Egerton-Warburton LM, Balsamo RA, Close TJ (1997) Temporal accumulation and ultrastructural localization of dehydrins in Zeya mays L. Physiol Plant 101:545–555
Foster R, Izawa T, Chua N-H (1994) Plant bZIP Proteins gather at ACGT elements. FASEB J 8:192–200
Garay-Arroyo A, Colmenero-Flores JM, Garciarrubio A, Covarrubias AA (2000) High hydrophilic proteins in prokaryotes and eukaryotes are common during conditions of water deficit. J Biol Chem 275:5668–5674
Gillet B, Eymery F, Beyly A, Peltier G, Rey P (1998) Molecular characterization of CDSP34 a chloroplastic protein induced by water deficit in Solanum tuberosum L. plants and regulation of CDSP34 expression by ABA and high illumination. Plant J 16:257–262
Gilmour SJ, Sebolt AM, Salazar MP, Everard JD, Thomashow MF (2000) Overexpression of the Arabidopsis CBF3 transcriptional activator mimics multiple biochemical changes associated with cold acclimation. Plant Physiol 124:1854–1865
Goday A, Jensen AB, Culiáñez-Macià FA, Mar Albà M, Figueras M, Serratosa J, Torrent M, Pagès M (1994) The maize abscisic acid-responsive protein Rab17 is located in the nucleus and interacts with nuclear localisation signals. Plant Cell 6:351–360
Godoy JA, Lunar R, Torres-Shumann S, Morena J, Rodrigo RM, Pintor-Toro JA (1994) Expression, tissue distribution and subcellular localisation of dehydrin TAS14 in salt-stressed tomato plants. Plant Mol Biol 26:1921–1934
Gowik U, Burscheidt J, Akyildiz M, Schlue U, Koczor M, Streubel M, Westhoff P (2004) cis-Regulatory elements for mesophyll-specific gene expression in the C4 plant Flaveria trinervia, the promoter of the C4 phosphoenolpyruvate carboxylase gene. Plant Cell 16:1077–1090
Hara M, Terashim S, Kuboi T (2001) Characterization and cryoprotective activity of cold-responsive dehydrin from Citrus unshiu. J Plant Physiol 158:1333–1339
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
Hara M, Terashim S, Fukaya T, Kuboi T (2004a) Enhancement of cold tolerance and inhibition of lipid peroxidation by citrus dehydrin in transgenic tobacco. Planta 217:290–298
Hara M, Fujinaga M, Kuboi T (2004b) Radical scavenging activity and oxidative modification of citrus dehydrin. Plant Physiol Biol 42:657–662
Hattori T, Totsuka M, Hobo T, Kagaya Y, Yamamoto-Toyoda A (2002) Experimentally determined sequence requirement of ACGT-containing abscisic acid response element. Plant Cell Physiol 43:136–140
Heino P, Palva ET (2003) Signal transduction in plant cold acclimation. In: Hirt H, Shinozaki K (eds), Topics in current genetics, vol. 4. Plant responses to abiotic stress, Springer, Berlin Heidelberg New York, pp 151–186
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
Higo K, Ugawa Y, Iwamoto M, Korenaga T (1999) Plant cis-acting regulatory DNA elements (PLACE) database. Nucleic Acid Res 27:297–300
Hoekstra FA, Golovina EA, Buitink J (2001) Mechanism of plant desiccation tolerance. Trends Plant Sci 6:431–438
Houde M, Daniel C, Lachapelle M, Allard F, Liberte S, Sarhan F (1995) Immunolocalisation of freezing tolerance associated proteins in cytoplasm and nucleoplasm of wheat crown tissues. Plant J 8:583–593
Ingram J, Bartels D (1996) The molecular basis of dehydration tolerance in plants. Annu Rev Plant Physiol Plant Mol Biol 47:377–403
Ismail AM, Hall AE, Close TJ (1997) Chilling tolerance during emergence of cowpea associate with a dehydrin and slow electrolyte leakage. Crop Sci 37:1270–1277
Ismail AM, Hall AE, Close TJ (1999) Purification and partial characterization of a dehydrin involved in chilling tolerance during seedling emergence of cowpea. Plant Physiol 120:237–244
Jaglo-Ottosen KR, Gilmour SJ, Zarka DG, Schabenberger O, Thomashow MF (1998) Arabidopsis CBF1 overexpression induces COR genes and enhances freezing tolerance. Science 280:104–106
Karlson DT, Fujino T, Kimura S, Baba K, Itoh T, Ashworth EN (2003) Novel plasmodesmata association of dehydrin-like proteins in cold acclimation red-osier dogwood (Cornus sericea). Tree Physiol 23:759–767
Kasuga M, Miura S, Shinozaki K, Yamaguchi-Shinozaki K (2004) A combination of the Arabidopsis DREB1A gene and stress-inducible rd29A promoter improved drought- and low-temperature stress tolerance in tobacco by gene transfer. Plant Cell Physiol 45:346–350
Kaye C, Neve L, Hofig A, Li Q-B, Haskell D, Guy C (1998) Characterization of a gene for spinach CAP160 and expression of two spinach cold-acclimation proteins in tobacco. Plant Physiol 116:1367–1377
Kirch H-H, van Berkel J, Glaczinki H, Salamini F, Gebhardt C (1997) Structural organization, expression and promoter activity of a cold-stress-inducible gene of potato (Solanum tuberosum L.). Plant Mol Biol 33:897–909
Kiyosue T, Yamagushi-Shinozaki K, Shinozaki K (1994) Characterization of two cDNAs (ERD10 and ERD14) corresponding to genes that respond rapidly to dehydration stress in Arabidopsis thaliana. Plant Cell Physiol 35:225–231
Kizis D, Pages M (2002) Maize DRE-binding proteins DBF1 and DBF2 are involved in rab17 regulation through the drought-responsive element in an ABA-dependent pathway. Plant J 30:679–689
Koag M-C, Fenton RD, Wilken S, Close TJ (2003) The binding of maize DHN1 to lipid vesicles. Gain of structure and lipid specificity. Plant Physiol 131:309–316
Kosugi S, Ohashi Y (1997) PCF1 and PCF2 specifically bind to cis elements in the rice proliferating cell nuclear antigen gene. Plant Cell 9:1607–1619
Kosugi S, Suzuka I, Ohashi Y (1995) Two of three promoter elements identified in a rice gene for proliferating cell nuclear antigen are essential for meristematic tissue-specific expression. Plant J 7:877–886
Krüger C, Berkowith 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
Lång V (1993) The role ABA and ABA-induced gene expression in cold acclimation of Arabidopsis thaliana. Ph.D. dissertation, Uppsala Genetic Center, Sweden
Lee SC, Lee MY, Kim SJ, Jun SH, An G, Kim SR (2005) Characterization of an abiotic stress-inducible dehydrin gene, OsDhn1, in rice (Oryza sativus L.). Mol Cells 19:212–218
Li R, Brawley SH, Close TJ (1998) Proteins immunologically related to dehydrins in fucoid algae. J Phycol 34:642–650
Liu Q, Kasuga M, Sakuma Y, Abe H, Miura S, Yamaguchi-Shinozaki K, Shinozaki K (1998) Two transcription factors, DREB1 and DREB2, with an EREBP/AP2 DNA binding domain separate two cellular signal transduction pathways in drought- and low temperature-responsive gene expression, respectively, in Arabidopsis. Plant Cell 10:1391–1406
Medina J, Bargues M, Terol J, Perez-Alonso M, Salinas J (1999) The Arabidopsis CBF gene family is composed of three genes encoding AP2 domain-containing proteins whose expression is regulated by low temperature but not by abscisic acid or dehydration. Plant Physiol 119:463–470
Mena M, Cejudo FJ, Isabel-Lamoneda I, Carbonero P (2002) A role for the DOF transcription factor BPBF in the regulation of gibberellin-responsive genes in barley aleurone. Plant Physiol 130:111–119
Menkens AE, Schindler U, Cashmore AR (1995) The G-box: a ubiquitous regulatory DNA element in plants bound by the GBF family of bzip proteins. Trends Biochem 20:506–510
Mitwisha L, Brandt W, McCread L, Lindsey GG (1998) HSP12 is a LEA-like protein in Saccharomyces cerevisiae. Plant Mol Biol 37:513–521
Monroy AF, Castonguay Y, Laberge S, Sarhan F, Vezina LP, Dhindsa RS (1993) A new cold-induced alfalfa gene is associated with enhanced hardening to subzero temperature. Plant Physiol 102:873–879
Narusaka Y, Nakashima K, Shinwari ZK, Sakuma Y, Furihata T, Abe H, Narusaka M, Shinozaki K, Yamaguchi-Shinozaki K (2003) Interaction between two cis-acting elements, ABRE and DRE, in ABA-dependent expression of Arabidopsis rd29A gene in response to dehydration and high-salinity stresses. Plant J 34:137–148
Nylander M, Svensson J, Palva ET, Welin BV (2001) Stress-induced accumulation and tissue-specific localisation of dehydrins in Arabidopsis thaliana. Plant Mol Biol 45:263–279
Piechulla B, Merforth N, Rudolph B (1998) Identification of tomato Lhc promoter regions necessary for circadian expression. Plant Mol Biol 38:655–662
Porat R, Pasentis K, Rozentzvieg D, Gerasopoulos D, Falara V, Samach A, Luric S, Kanellis AK (2004) Isolation of a dehydrin cDNA from orange and grapefruit citrus fruit that is specifically induced by the combination of heat followed by chilling temperatures. Physiol Plant 120:256–264
Prestridge DS (1991) SIGNAL SCAN: a computer program that scans DNA sequences for eucaryotic translational elements. CABIOS 7:203–206
Pruvot G, Cuiné S, Peltier G, Rey P (1996) Characterization of a novel drought-induced 34-kDa protein located in the thylakoids of Solanum tuberosum L. plants. Planta 198:471–479
Puhakainen T, Hess MV, Mäkela P, Svenson J, Heino P, Palva ET (2004) Overexpression of multiple dehydrin genes enhances tolerance to freezing stress in Arabidopsis. Plant Mol Biol 54:743–753
Qin F, Sakuma Y, Li J, Liu Q, Li YQ, Shinozaki K, Yamaguchi-Shinozaki K (2004) Cloning and functional analysis of a novel DREB1/CBF transcription factor involved in cold-responsive gene expression in Zea mays L. Plant Cell Physiol 45:1042–1052
Richard S, Morency M-J, Drevet C, Jouanin L, Séguin A (2000) Isolation and characterization of a dehydrin gene from white spurs induced upon wounding, drought and cold stress. Plant Mol Biol 43:1–10
Rinne PLH, Kaikuranta PLM, ven 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
Rodriguez EM, Svenson JT, Malatrasi M, Choi D-W, Close TJ (2005) Barley Dhn13 encodes a KS-type dehydrin with constitutive and stress responsive expression. Theor Appl Genet 110:852–858
Rorat T (2001) Changes in gene expression in a wild potato (S. sogarandinum) during cold acclimation. Acta Plant Physiol 23:117–126
Rorat T, Irzykowski W (1996) Changes in mRNA population during cold acclimation in two potato lines of Solanum sogarandinum differing by their cold hardiness. Acta Physiol Plant 18:25–32
Rorat T, Irzykowski W, Grygorowicz WJ (1997) Identification and isolation of novel cold induced genes in potato (Solanum sogarandinum). Plant Sci 124:69–78
Rorat T, Grygorowicz WJ, Berbezy P, Irzykowski W (1998) Isolation and expression of cold specific genes in potato (Solanum sogarandinum). Plant Sci 133:57–67
Rorat T, Irzykowski W, Cuiné S, Becuwe N, Rey P (2001) PSII-S gene expression, photosynthetic activity and abundance of plastid thiredoxin and lipid-associated proteins during chilling stress in Solanum species differing in freezing tolerance. Physiol Plant 113:72–78
Rorat T, Grygorowicz WJ, Irzykowski W, Rey P (2004) Expression of KS-type dehydrins is primarily regulated by factors related to organ type and leaf developmental stage under vegetative growth. Planta 218:878–885
Sakai H, Aoyama T, Oka A (2000) Arabidopsis ARR1 and ARR2 response regulators operate as transcriptional activators. Plant J 24:703–711
Sarhan F, Oullet F, Vazquez-Tello A (1997) The wheat wcs120 gene family: a useful model to understand the molecular genetics of freezing tolerance in cereals. Physiol Plant 101:439–445
Shirsat A, Wilford N, Croy R, Boulter D (1989) Sequences responsible for the tissue specific promoter activity of a pea legumin gene in tobacco. Mol Gen Genet 215:326–331
Simpson SD, Nakashima K, Narusaka Y, Seki M, Shinozaki K, Yamaguchi-Shinozaki K (2003) Two different novel cis-acting elements of erd1, a clpA homologous Arabidopsis gene function in induction by dehydration stress and dark-induced senescence. Plant J 33:259–270
Soulages JL, Kim K, Walters C, Cushman JC (2002) Temperature-induced extended helix/random coil transitions in a group 1 late embryogenesis abundant proteins from soybean. Plant Physiol 128:822–832
Soulages JL, Kim K, Arrese EL, Walters C, Cushman JC (2003) Conformation of a group 2 late embryogenesis abundant protein from soybean. Evidence of poly (l-proline)-type II structure. Plant Physiol 131:963–975
Stalberg K, Ellerstom M, Ezcurra I, Ablov S, Rask L (1996) Disruption of an overlapping E-box/ABRE motif abolished high transcription of the napA storage-protein promoter in transgenic Brassica napus seeds. Planta 199:515–519
Steponkus PL, Uemura M, Joseph RA, Gilmour SJ, Thomashow MF (1998) Mode of action of the COR15a gene on the freezing tolerance of the Arabidopsis thaliana. Proc Natl Acad Sci USA 95:14570–14575
Stockinger EJ, Gilmour SJ, Thomashow MF (1997) Arabidopsis thaliana CBF1 encodes an AP2 domain-containing transcriptional activator that binds to the C-repeat DRE, a cis-acting DNA regulatory element that stimulates transcription in response to low temperature and water deficit. Proc Natl Acad Sci USA 94:1035–1040
Svenson J, Ismail AM, Palva ET, Close TJ (2002) Dehydrins. In: Storey KB, Storey JM (eds), Sensing, signalling and cell adaptation. Elsevier, Amsterdam, pp 155–171
Tabaei-Aghdaei SR, Harrison P, Pearce RS (2000) Expression of dehydration-stress-related genes in the crowns of wheatgrasses species [Lophopyrum elongatum (Host) A. Love and Agropyron desertorum (Fisch. Ex Link.) Schult.] having contrasting acclimation to salt, cold and drought. Plant Cell Environ 23:561–571
Takahashi R, Shimosaka E (1997) cDNA sequence analysis and expression of two cold-regulated genes in soybean. Plant Sci 123:93–104
Tan S-K, Sage-Ono K, Kamada H (2000) Cloning and characterization of ECPP44, a cDNA encoding a 44-kilodalton phosphoprotein relating to somatic embryogenesis in carrot. Plant Biotechnol 17:61–68
Teakle GR, Manfield IW, Graham JF, Gilmartin PM (2002) Arabidopsis thaliana GATA factors: organisation, expression and DNA-binding characteristics. Plant Mol Biol 50:43–57
Thomashow MF (1999) Plant cold acclimation. Freezing tolerance genes and regulatory mechanisms. Annu Rev Plant Physiol Plant Mol Biol 50:571–599
Vieweg MF, Fruhling M, Quandt HJ, Heim U, Baumlein H, Puhler A, Kuster H, Andreas MP (2004) The promoter of the Vicia faba L. leg hemoglobin gene VfLb29 is specifically activated in the infected cells of root nodules and in the arbuscule-containing cells of mycorrhizal roots from different legume and non-legume plants. Mol Plant Microbe Interact 17:62–69
Wang Z-Y, Kenigsbuch D, Sun L, Harel E, Ong MS, Tobin EM (1997) A myb-related transcription factor is involved in the phytochrome regulation of an Arabidopsis Lhcb gene. Plant cell 9:491–507
Whitsitt MS, Collins RG, Mullet JE (1997) Modulation of dehydration tolerance in soybean seedlings. Plant Physiol 114:917–925
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). Physiol Plant 105:600–608
Zhou DX (1999) Regulatory mechanism of plant gene transcription by GT-elements and GT-factors. Trends Plant Sci 4:210–214
Zhu B, Choi DW, Fenton R, Close TJ (2000) Expression of the barley dehydrin multigene family and the development of freezing tolerance. Mol Gen Genet 264:145–153
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Rorat, T., Szabala, B.M., Grygorowicz, W.J. et al. Expression of SK3-type dehydrin in transporting organs is associated with cold acclimation in Solanum species. Planta 224, 205–221 (2006). https://doi.org/10.1007/s00425-005-0200-1
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00425-005-0200-1