Nothing Special   »   [go: up one dir, main page]

Skip to main content

Advertisement

Log in

Plant responses to drought, salinity and extreme temperatures: towards genetic engineering for stress tolerance

  • Review
  • Published:
Planta Aims and scope Submit manuscript

Abstract

Abiotic stresses, such as drought, salinity, extreme temperatures, chemical toxicity and oxidative stress are serious threats to agriculture and the natural status of the environment. Increased salinization of arable land is expected to have devastating global effects, resulting in 30% land loss within the next 25 years, and up to 50% by the year 2050. Therefore, breeding for drought and salinity stress tolerance in crop plants (for food supply) and in forest trees (a central component of the global ecosystem) should be given high research priority in plant biotechnology programs. Molecular control mechanisms for abiotic stress tolerance are based on the activation and regulation of specific stress-related genes. These genes are involved in the whole sequence of stress responses, such as signaling, transcriptional control, protection of membranes and proteins, and free-radical and toxic-compound scavenging. Recently, research into the molecular mechanisms of stress responses has started to bear fruit and, in parallel, genetic modification of stress tolerance has also shown promising results that may ultimately apply to agriculturally and ecologically important plants. The present review summarizes the recent advances in elucidating stress-response mechanisms and their biotechnological applications. Emphasis is placed on transgenic plants that have been engineered based on different stress-response mechanisms. The review examines the following aspects: regulatory controls, metabolite engineering, ion transport, antioxidants and detoxification, late embryogenesis abundant (LEA) and heat-shock proteins.

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

Access this article

Subscribe and save

Springer+ Basic
$34.99 /Month
  • Get 10 units per month
  • Download Article/Chapter or eBook
  • 1 Unit = 1 Article or 1 Chapter
  • Cancel anytime
Subscribe now

Buy Now

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1

Similar content being viewed by others

Abbreviations

HSF:

heat-shock factor

Hsp:

heat-shock protein

LEA protein:

late embryogenesis abundant protein

ROS:

reactive oxygen species

SP1:

stable protein 1

TF:

transcription factor

References

  • Abe H, Urao T, Ito T, Seki M, Shinozaki K, Yamaguchi-Shinozaki K (2003) Arabidopsis AtMYC2 (bHLH) and AtMYB2 (MYB) function as transcriptional activators in abscisic acid signaling. Plant Cell 15:63–78

    Article  CAS  PubMed  Google Scholar 

  • Alamillo J, Almoguera C, Bartels D, Jordano J (1995) Constitutive expression of small heat shock proteins in vegetative tissues of the resurrection plant Craterostigma plantagineum. Plant Mol Biol 29:1093–1099

    CAS  PubMed  Google Scholar 

  • Alia, Hayashi H, Sakamoto A, Murata N (1998a) Enhancement of the tolerance of Arabidopsis to high temperatures by genetic engineering of the synthesis of glycinebetaine. Plant J 16:155–161

    Article  PubMed  Google Scholar 

  • Alia, Hayashi H, Chen THH, Murata N (1998b) Transformation with a gene for choline oxidase enhances the cold tolerance of Arabidopsis during germination and early growth. Plant Cell Environ 21:232–239

    CAS  Google Scholar 

  • Almoguera C, Coca MA, Jordano J (1993) Tissue-specific expression of sunflower heat shock proteins in response to water stress. Plant J 4:947–958

    CAS  Google Scholar 

  • Apse MP, Aharon GS, Snedden WA, Blumwald E (1999) Salt tolerance conferred by overexpression of a vacuolar Na+/H+ antiport in Arabidopsis. Science 285:1256–1258

    Google Scholar 

  • Artus NN, Uemura M, Steponkus PL, Gilmour SJ, Lin C, Thomashow MF (1996) Constitutive expression of the cold-regulated Arabidopsis thaliana COR15a gene affects both chloroplast and protoplast freezing tolerance. Proc Natl Acad Sci USA 93:13404–13409

    Article  CAS  PubMed  Google Scholar 

  • Barak T (2003) The possible function of SP1 in sp1-transgenic aspen plants that express high or low levels of this protein. MSc thesis, Hebrew University of Jerusalem

  • Bartels D (2001) Targeting detoxification pathways: an efficient approach to obtain plants with multiple stress tolerance. Trends Plant Sci 6:284–286

    Article  CAS  PubMed  Google Scholar 

  • Blumwald E (2000) Sodium transport and salt tolerance in plants. Curr Opin Cell Biol 12:431–434

    Google Scholar 

  • Bohnert HJ, Shen B (1999) Transformation and compatible solutes. Sci Hort 78:237–260

    CAS  Google Scholar 

  • Bohnert HJ, Sheveleva E (1998) Plant stress adaptations — making metabolism move. Curr Opin Plant Biol 1:267–274

    CAS  PubMed  Google Scholar 

  • Bohnert HJ, Ayoubi P, Borchert C, Bressan RA, Burnap RL, Cushman JC, Cushman MA, Deyholos M, Fischer R, Galbraith DW (2001) A genomics approach towards salt stress tolerance. Plant Physiol Biochem 39:295–311

    Article  CAS  Google Scholar 

  • Bordas M, Montesinos C, Debauza M, Salvador A, Roig LA, Serrano R, Moreno V (1997) Transfer of the yeast salt tolerance gene HAL1 to Cucumis melo L. cultivars and in vitro evaluation of salt tolerance. Transgenic Res 6:41–50

    Article  CAS  PubMed  Google Scholar 

  • Boston RS, Viitanen PV, Vierling E (1996) Molecular chaperones and protein folding in plants. Plant Mol Biol 32:191–222

    CAS  PubMed  Google Scholar 

  • Bowler C, Van Montagu M, Inzé D (1992) Superoxide dismutases and stress tolerance. Annu Rev Plant Physiol Plant Mol Biol 43:83–116

    CAS  Google Scholar 

  • Boyer JS (1982) Plant productivity and environment. Science 218:443–448

    Google Scholar 

  • Bray EA, Bailey-Serres J, Weretilnyk E (2000) Responses to abiotic stresses. In: Gruissem W, Buchannan B, Jones R (eds) Biochemistry and molecular biology of plants. American Society of Plant Physiologists, Rockville, MD, pp 1158–1249

  • Ceccardi TL, Meyer NC, Close TJ (1994) Purification of a maize dehydrin. Protein Express Purif 5:266–269

    Article  CAS  Google Scholar 

  • Chapman D (1998) Phospholipase activity during plant growth and development and in response to environmental stress. Trends Plant Sci. 3:419–426

    Google Scholar 

  • Chauhan S, Forsthoefel N, Ran Y, Quigley F, Nelson DE, Bohnert HJ (2000) Na+/myo-inositol symporters and Na+/H+-antiport in Mesembryanthemum crystallinum Plant J 24:511–522

    Google Scholar 

  • Chen Q, Osteryoung K, Vierling E (1994) A 21-kDa chloroplast heat shock protein assembles into high molecular weight complexes in vitro and in organelle. J Biol Chem 269:13216–13233

    CAS  PubMed  Google Scholar 

  • Chen THH, Murata N (2002) Enhancement of tolerance of abiotic stress by metabolic engineering of betaines and other compatible solutes. Curr Opin Plant Biol 5:250–257

    Article  CAS  PubMed  Google Scholar 

  • Chen W, Provart NJ, Glazebrook J, Katagiri F, Chang HS, Eulgem T, Mauch F, Luan Sh, Zou G, Whitham SA, Budworth PR, Tao Y, Xie Z, Chen X, Lam S, Kreps JA, Harper JF, Si-Ammour A, Mauch-Mani B, Heinlein M, Kobayashi K, Hohn T, Dangl JL, Wang X, Zhu T (2002) Expression profile matrix of arabidopsis transcription factor genes suggests their putative functions in response to environmental stresses. Plant Cell 14:559–574

    CAS  PubMed  Google Scholar 

  • Choi HI, Hong JH, Ha J, Kang JY, Kim SY (2000) ABFs, a family of ABA-responsive element binding factors. J Biol Chem 275:1723–1730

    Article  CAS  PubMed  Google Scholar 

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

    CAS  PubMed  Google Scholar 

  • Collada C, Gomez L, Casado R, Aragoncillo C (1997) Purification and in vitro chaperone activity of a class I small heat-shock protein abundant in recalcitrant chestnut seeds. Plant Physiol 115:71–77

    Article  CAS  PubMed  Google Scholar 

  • Cushman JC, Bohnert HJ (2000) Genomic approaches to plant stress tolerance. Curr Opin Plant Biol 3:117–124

    CAS  PubMed  Google Scholar 

  • Davison PA, Hunter CN, Horton P (2002) Overexpression of β-carotene hydroxylase enhances stress tolerance in Arabidopsis. Nature 418:203–206

    Article  CAS  PubMed  Google Scholar 

  • Diamant S, Eliahu N, Rosenthal D, Goloubinoff P (2001) Chemical chaperones regulate molecular chaperones in vitro and in cells under combined salt and heat stresses. J Biol Chem 276:39586–39591

    CAS  PubMed  Google Scholar 

  • Ding L, Candido EPM (2000) HSP25, a small heat shock protein associated with dense bodies and M-lines of body wall muscle in Caenorhabditis elegans. J Biol Chem 275:9510–9517

    Article  CAS  PubMed  Google Scholar 

  • Dunwell JM (2000) Transgenic approaches to crop improvement. J Exp Bot 51:487–496

    Article  CAS  PubMed  Google Scholar 

  • Dure III L (1993a) Structural motifs in Lea proteins. In: Close TJ, Bray EA (eds) Plant response to cellular dehydration during environmental stress. American Society of Plant Physiologists, Rockville, MD, pp 91–103

  • Dure III L (1993b) A repeating 11-mer amino acid motif and plant desiccation. Plant J 3:363–369

    Article  PubMed  Google Scholar 

  • Ehrnsperger M, Gräber S, Gaestel M, Buchner J (1997) Binding of non-native protein to Hsp25 during heat shock creates a reservoir of folding intermediates for reactivation. EMBO J 16:221–229

    PubMed  Google Scholar 

  • Finkelstein RR, Lynch TJ (2000) The Arabidopsis abscisic acid response gene ABI5 encodes a basic leucine zipper transcription factor. Plant Cell 12:599–609

    Article  CAS  PubMed  Google Scholar 

  • Fowler S, Thomashow MF (2002) Arabidopsis transcriptome profiling indicates that multiple regulatory pathways are activated during cold acclimation in addition to the CBF cold response pathway. Plant Cell 14:1675–1690

    Article  CAS  PubMed  Google Scholar 

  • Frank W, Munnik T, Kerkmann K, Salamini F, Bartels D (2000) Water deficit triggers phospholipase D activity in the resurrection plant Craterostigma plantagineum. Plant Cell 12:111–124

    Google Scholar 

  • Fukuda A, Nakamura A, Tanaka Y (1999) Molecular cloning and expression of the Na+/H+ exchanger gene in Oryza sativa. Biochim Biophys Acta 1446:149–155

    Article  PubMed  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  CAS  PubMed  Google Scholar 

  • Garg AK, Kim JK, Owens TG, Ranwala AP, Choi YD, Kochian LV, Wu RJ (2002) Trehalose accumulation in rice plants confers high tolerance levels to different abiotic stresses. Proc Natl Acad Sci USA 99:15898–15903

    Article  CAS  PubMed  Google Scholar 

  • Gaxiola RA, Rao R, Sherman A, Grisafi P, Alper SL, Fink GR (1999) The Arabidopsis thaliana proton transporters, AtNhx1 and Avp1, can function in cation detoxification in yeast. Proc Natl Acad Sci USA. 96:1480–1485

    Google Scholar 

  • Gaxiola RA, Li J, Undurraga S, Dang LM, Allen GJ, Alper SL, Fink GR (2001) Drought- and salt-tolerant plants result from overexpression of the AVP1 H+-pump. Proc Natl Acad Sci USA 98:11444–11449

    Article  CAS  PubMed  Google Scholar 

  • Gilmour SJ, Zarka DG, Stockinger EJ, Salazar MP, Houghton JM, Thomashow MF (1998) Low temperature regulation of the Arabidopsis CBF family of AP2 transcriptional activators as an early step in cold-induced COR gene expression. Plant J 16:433–442

    CAS  PubMed  Google Scholar 

  • 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

    CAS  PubMed  Google Scholar 

  • Gisbert C, Rus AM, Bolarín MC, López-Coronado JM, Arrillaga I, Montesinos C, Caro M, Serrano R, Moreno V (2000) The yeast HAL1 gene improves salt tolerance of transgenic tomato. Plant Physiol 123:393–402

    Article  CAS  PubMed  Google Scholar 

  • Guiltinan MJ, Marcotte WR, Quatrano RS (1990) A plant leucine zipper protein that recognizes an abscisic acid response element. Science 250:267–271

    CAS  PubMed  Google Scholar 

  • Gupta AS, Heinen JL, Holaday AS, Burke JJ, Allen RD (1993a) Increased resistance to oxidative stress in transgenic plants that overexpress chloroplastic Cu/Zn superoxide dismutase. Proc Natl Acad Sci USA 90:1629–1633

    CAS  PubMed  Google Scholar 

  • Gupta AS, Webb RP, Holaday AS, Allen RD (1993b) Overexpression of superoxide dismutase protects plants from oxidative stress. Plant Physiol 103:1067–1073

    PubMed  Google Scholar 

  • Haake V, Cook D, Riechmann JL, Pineda O, Thomashow MF, Zhang JZ (2002) Transcription factor CBF4 is a regulator of drought adaptation in Arabidopsis. Plant Physiol 130:639–648

    Article  CAS  PubMed  Google Scholar 

  • Hamada A, Shono M, Xia T, Ohta M, Hayashi Y, Tanaka A, Hayakawa T (2001) Isolation and characterization of a Na+/H+ antiporter gene from the halophyte Atriplex gmelini. Plant Mol Biol 46:35–42

    Article  CAS  PubMed  Google Scholar 

  • Hamilton III EW, Heckathorn SA (2001) Mitochondrial adaptations to NaCl. Complex I is protected by anti-oxidants and small heat shock proteins, whereas complex II is protected by proline and betaine. Plant Physiol 126:1266–1274

    Article  CAS  PubMed  Google Scholar 

  • Hare PD, Cress WA, Van Staden J (1998) Dissecting the roles of osmolyte accumulation during stress. Plant Cell Environ 21:535–553

    Google Scholar 

  • Härndahl U, Hall RB, Osteryoung KW, Vierling E, Bornman JF, Sundby C (1999) The chloroplast small heat shock protein undergoes oxidation-dependent conformational changes and may protect plants from oxidative stress. Cell Stress Chaperones 4:129–138

    Article  PubMed  Google Scholar 

  • Hartl FU (1996) Molecular chaperones in cellular protein folding. Nature 381:571–579

    Google Scholar 

  • Hasegawa PM, Bressan AB, Zhu JK, Bohnert HJ (2000) Plant cellular and molecular responses to high salinity. Annu Rev Plant Physiol Plant Mol Biol 51:463–499

    CAS  Google Scholar 

  • Haslbeck M, Walke S, Stromer T, Ehrnsperger M, White HE, Chen S, Saibil HR, Buchner J (1999) Hsp26: a temperature-regulated chaperone. EMBO J 18:6744–6751

    PubMed  Google Scholar 

  • Hayashi H, Mustardy L, Deshnium P, Ida M, Murata N (1997) Transformation of Arabidopsis thaliana with the codA gene for choline oxidase: accumulation of glycinebetaine and enhanced tolerance to salt and cold stress. Plant J 12:133–142

    CAS  PubMed  Google Scholar 

  • Hendrick JP, Hartl FU (1993) Molecular chaperone functions of heat-shock proteins. Annu Rev Biochem 62:349–384

    CAS  PubMed  Google Scholar 

  • Hobo T, Kowyama Y, Hattori T (1999) A bZIP factor, TRAB1, interacts with VP1 and mediates abscisic acid-induced transcription. Proc Natl Acad Sci USA 96:15348–15353

    Article  CAS  PubMed  Google Scholar 

  • Hoekstra FA, Golovina EA, Buitink J (2001) Mechanisms of plant desiccation tolerance. Trends Plant Sci 6:431–438

    CAS  PubMed  Google Scholar 

  • Hong Z, Lakkineni K, Zhang K, Verma DPS (2000) Removal of feedback inhibition of Δ1-pyrroline-5-carboxylate synthetase results in increased proline accumulation and protection of plants from osmotic stress. Plant Physiol 122:1129–1136

    CAS  PubMed  Google Scholar 

  • Hook DWA, Harding JJ (1998) Protection of enzymes by α-crystallin acting as a molecular chaperone. Int J Biol Macromol 22:295–306

    Article  CAS  PubMed  Google Scholar 

  • Horwitz J (1992) α-Crystallin can function as a molecular chaperone. Proc Natl Acad Sci USA 89:10449–10453

    CAS  PubMed  Google Scholar 

  • Houde M, Daniel C, Lachapelle M, Allard F, Laliberte S, Sarhan F (1995) Immunolocalization of freezing-tolerance-associated proteins in the cytoplasm and nucleoplasm of wheat crown tissue. Plant J 8:583–593

    Article  CAS  PubMed  Google Scholar 

  • Hsieh TH, Lee JT, Yang PT, Chiu LH, Charng YY, Wang YC, Chan MT (2002) Heterology expression of the Arabidopsis C-repeat/dehydration response element binding factor 1 gene confers elevated tolerance to chilling and oxidative stresses in transgenic tomato. Plant Physiol 129:1086–1094

    Article  CAS  PubMed  Google Scholar 

  • Huang J, Hirji R, Adam L, Rozwadowski KL, Hammerlindl JK, Keller WA, Selvaraj G (2000) Genetic engineering of glycinebetaine production toward enhancing stress tolerance in plants: metabolic limitations. Plant Physiol 122:747–756

    CAS  PubMed  Google Scholar 

  • Ingram J, Bartels D (1996) The molecular basis of dehydration tolerance in plants. Annu Rev Plant Biol 47:377–403

    Article  CAS  Google Scholar 

  • Iturriaga G, Schneider K, Salamini F, Bartels D (1992) Expression of desiccation-related proteins from the resurrection plant in transgenic tobacco. Plant Mol Biol 20:555–558

    CAS  PubMed  Google Scholar 

  • Jaglo KR, Kleff S, Amundsen KL, Zhang X, Haake V, Zhang JZ, Deits T, Thomashow MF (2001) Components of the Arabidopsis C-repeat/dehydration-responsive element binding factor cold-response pathway are conserved in Brassica napus and other plant species. Plant Physiol 127:910–917

    Article  CAS  PubMed  Google Scholar 

  • 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

    CAS  PubMed  Google Scholar 

  • Kang JY, Choi HI, Im MY, Kim SY (2002) Arabidopsis basic leucine zipper proteins that mediate stress-responsive abscisic acid signaling. Plant Cell 14:343–357

    Article  CAS  PubMed  Google Scholar 

  • Kasuga M, Liu Q, Miura S, Yamaguchi-Shinozaki K, Shinozaki K (1999) Improving plant drought, salt, and freezing tolerance by gene transfer of a single stress-inducible transcription factor. Nature Biotech 17:287–291

    Google Scholar 

  • Kazuoka T, Oeda K (1994) Purification and characterization of COR85-oligomeric complex from cold-acclimated spinach. Plant Cell Physiol 35:601–611

    Google Scholar 

  • Kishor KPB, Hong Z, Miao GH, Hu CAA, Verma DPS (1995) Overexpression of Δ1-pyrroline-5-carboxylate synthetase increase proline production and confers osmotolerance in transgenic plants. Plant Physiol 108:1387–1394

    CAS  Google Scholar 

  • Knight H, Knight MR (2001) Abiotic stress signalling pathways: specificity and cross-talk. Trends Plant Sci 6:262–267

    Article  CAS  PubMed  Google Scholar 

  • Konstantinova T, Parvanova D, Atanassov A, Djilianov D (2002) Freezing tolerant tobacco, transformed to accumulate osmoprotectants. Plant Sci 163:157–164

    Article  CAS  Google Scholar 

  • Kreps JA, Wu Y, Chang HS, Zhu T, Wang X, Harper JF (2002) Transcriptome changes for Arabidopsis in response to salt, osmotic, and cold stress. Plant Physiol 130:2129–2141

    Article  CAS  PubMed  Google Scholar 

  • Lee GJ, Pokala N, Vierling E (1995) Structure and in vitro molecular chaperone activity of cytosolic small heat shock proteins from pea. J Biol Chem 270:10432–10438

    PubMed  Google Scholar 

  • Lee GJ, Roseman AM, Saibil HR, Vierling E (1997) A small heat shock protein stably binds heat-denatured model substrates and can maintain a substrate in a folding-competent state. EMBO J 3:659–671

    Article  Google Scholar 

  • Lee JH, Hübel A, Schöffl F (1995) Derepression of the activity of genetically engineered heat shock factor causes constitutive synthesis of heat shock proteins and increased thermotolerance in transgenic Arabidopsis. Plant J 8:603–612

    Article  CAS  PubMed  Google Scholar 

  • Leung J, Giraudat J (1998) Abscisic acid signal transduction. Annu Rev Plant Biol 49:199–222

    Article  CAS  Google Scholar 

  • Lilius G, Holmberg N, Bülow L (1996) Enhanced NaCl stress tolerance in transgenic tobacco expressing bacterial choline dehydrogenase. Bio-Technology 14:177–180

    Google Scholar 

  • 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

    CAS  PubMed  Google Scholar 

  • Lopez-Molina L, Chua NH (2000) A null mutation in a bZIP factor confers ABA-insensitivity in Arabidopsis thaliana. Plant Cell Physiol 41:541–547

    CAS  PubMed  Google Scholar 

  • Malik MK, Slovin JP, Hwang CH, Zimmerman JL (1999) Modified expression of a carrot small heat shock protein gene, Hsp17.7, results in increased or decreased thermotolerance. Plant J 20:89–99

    Article  CAS  PubMed  Google Scholar 

  • Marini I, Moschini R, Corso AD, Mura U (2000) Complete protection by α-crystallin of lens sorbitol dehydrogenase undergoing thermal stress. J Biol Chem 275:32559–32565

    Article  CAS  PubMed  Google Scholar 

  • Maurel C, (1997) Aquaporins and water permeability of plant membranes. Annu Rev Plant Biol 48:399–429

    Article  CAS  Google Scholar 

  • McCue KF, Hanson AD (1990) Drought and salt tolerance: toward understanding and application. Trends Biotechnol 8:358–362

    CAS  Google Scholar 

  • McKersie BD, Bowley SR, Harjanto E, Leprince O (1996) Water-deficit tolerance and field performance of transgenic alfalfa overexpressing superoxide dismutase. Plant Physiol 111:1177–1181

    CAS  PubMed  Google Scholar 

  • McKersie BD, Bowley SR, Jones KS (1999) Winter survival of transgenic alfalfa overexpressing superoxide dismutase. Plant Physiol 119:839–848

    Article  CAS  PubMed  Google Scholar 

  • McKersie BD, Murnaghan J, Jones KS, Bowley SR (2000) Iron-superoxide dismutase expression in transgenic alfalfa increases winter survival without a detectable increase in photosynthetic oxidative stress tolerance. Plant Physiol 122:1427–1438

    Article  CAS  PubMed  Google Scholar 

  • McNeil SD, Nuccio ML, Hanson AD (1999) Betaines and related osmoprotectants: targets for metabolic engineering of stress resistance. Plant Physiol 120:945–949

    PubMed  Google Scholar 

  • Mishra SK, Tripp J, Winkelhaus S, Tschiersch B, Theres K, Nover L, Scharf KD (2002) In the complex family of heat stress transcription factors, HsfA1 has a unique role as master regulator of thermotolerance in tomato. Gene Dev 16:1555–1567

    Article  CAS  Google Scholar 

  • Mittler R (2002) Oxidative stress, antioxidants and stress tolerance. Trends Plant Sci 7:405–410

    Article  CAS  PubMed  Google Scholar 

  • Mitsuhara I, Malik KA, Miura M, Ohashi Y (1999) Animal cell-death suppressors Bcl-xL and Ced-9 inhibit cell death in tobacco plants. Curr Biol 9:775–778

    CAS  Google Scholar 

  • Moran JF, Becana M, Iturbe-Ormaetxe I, Frechilla S, Klucas RV, Aparicio-Tejo P (1994) Drought induces oxidative stress in pea plants. Planta 194:346–352

    CAS  Google Scholar 

  • Morimoto RI (1998) Regulation of the heat shock transcriptional response: cross talk between family of heat shock factors, molecular chaperones, and negative regulators. Genes Dev 12:3788–3796

    CAS  PubMed  Google Scholar 

  • Muchowski PJ, Clark JI (1998) ATP-enhance molecular chaperone functions of the small heat shock protein human αB crystallin. Biochemistry 95:1004–1009

    Article  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

    CAS  PubMed  Google Scholar 

  • Mundy J, Yamaguchi-Shinozaki K, Chua, NH (1990) Nuclear proteins bind conserved elements in the abscisic acid-responsive promoter of a rice rab gene. Proc. Natl Acad Sci USA 87:406–410

    Google Scholar 

  • Munnik T, Ligterink W, Meskiene I, Calderini O, Beyerly J, Musgrave A, Hirt H (1999) Distinct osmo-sensing protein kinase pathways are involved in signaling moderate and severe hyper-osmotic stress. Plant J 20:381–388

    Article  CAS  PubMed  Google Scholar 

  • Nanjo T, Kobayashia M, Yoshibab Y, Kakubaric Y, Yamaguchi-Shinozaki K, Shinozaki K (1999) Antisense suppression of proline degradation improves tolerance to freezing and salinity in Arabidopsis thaliana. FEBS Lett 461:205–210

    Article  CAS  PubMed  Google Scholar 

  • Ndong C, Danyluk J, Wilson KE, Pocock T, Huner NPA, Sarhan F (2002) Cold-regulated cereal chloroplast late embryogenesis abundant-like proteins. Molecular characterization and functional analyses. Plant Physiol 129:1368–1381

    Article  CAS  PubMed  Google Scholar 

  • Noctor G, Foyer C (1998) Ascorbate and glutathione: keeping active oxygen under control. Annu Rev Plant Physiol Plant Mol Biol 49:249–279

    CAS  Google Scholar 

  • Nover L, Bharti K, Döring P, Mishra SK, Ganguli A, Scharf KD (2001) Arabidopsis and the heat stress transcription factor world: How many heat stress transcription factors do we need? Cell Stress Chaperones 6:177–189

    CAS  PubMed  Google Scholar 

  • Nuccio ML, Russell BL, Nolte KD, Rathinasabapathi B, Gage DA, Hanson AD (1998) The endogenous choline supply limits glycine betaine synthesis in transgenic tobacco expressing choline monooxygenase. Plant J 16:487–498

    CAS  PubMed  Google Scholar 

  • Oberschall A, Deák M, Török K, Sass L, Vass I, Kovács I, Fehér A, Dudits D, Horváth GV (2000) A novel aldose/aldehyde reductase protects transgenic plants against lipid peroxidation under chemical and drought stresses. Plant J 24:437–446

    Article  CAS  PubMed  Google Scholar 

  • Piao HL, Lim JH, Kim SJ, Cheong GW, Hwang I (2001) Constitutive over-expression of AtGSK1 induces NaCl stress responses in the absence of NaCl stress and results in enhanced NaCl tolerance in Arabidopsis. Plant J 27:305–314

    Article  CAS  PubMed  Google Scholar 

  • Pitcher LH, Zilinskas BA (1996) Overexpression of copper/zinc superoxide dismutase in the cytosol of transgenic tobacco confers partial resistance to ozone-induced foliar necrosis. Plant Physiol 110:583–588

    CAS  PubMed  Google Scholar 

  • Prändl R, Hinderhofer K, Eggers-Schumacher G, Schöffl F (1998) HSF3, a new heat shock factor from Arabidopsis thaliana, derepresses the heat shock response and confers thermotolerance when overexpressed in transgenic plants. Mol Gen Genet 258:269–278

    Article  PubMed  Google Scholar 

  • Price AM, Atherton NM, Hendry GAF (1989) Plants under drought-stress generate activated oxygen. Free Rad Res Commun 8:61–66

    CAS  Google Scholar 

  • Qiao J, Mitsuhara I, Yazaki Y, Sakano K, Gotoh Y, Miura M, Ohashi Y (2002) Enhanced resistance to salt, cold and wound stresses by overproduction of animal cell death suppressors Bcl-xL and Ced-9 in tobacco cells — their possible contribution through improved function of organella. Plant Cell Physiol 43:992–1005

    Article  CAS  PubMed  Google Scholar 

  • Riechmann JL, Heard J, Martin G, Reuber L, Jiang C, Keddie J, Adam L, Pineda O, Ratcliffe OJ, Samaha RR. (2000) Arabidopsis transcription factors: genome-wide comparative analysis among eukaryotes. Science 290:2105–2110

    CAS  PubMed  Google Scholar 

  • Roxas VP, Smith RK Jr, Allen ER, Allen RD (1997) Overexpression of glutathione S-transferase/glutathione peroxidase enhances the growth of transgenic tobacco seedlings during stress. Nature Biotech 15:988–991

    CAS  Google Scholar 

  • Rus AM, Estaño MT, Gisbert C, Garcia-Sogo B, Serrano R, Caro M, Moreno V, Bolarín MC (2001) Expressing the yeast HAL1 gene in tomato increases fruit yield and enhances K+/Na+ selectivity under salt stress. Plant Cell Environ 24:875–880

    Article  CAS  Google Scholar 

  • Russell BL, Rathinasabapathi B, Hanson AD (1998) Osmotic stress induces expression of choline monooxygenase in sugar beet and amaranth. Plant Physiol 116:859–865

    CAS  PubMed  Google Scholar 

  • Sabehat A, Lurie S, Weiss D (1998) Expression of small heat-shock proteins at low temperatures. Plant Physiol 117:651–658

    CAS  PubMed  Google Scholar 

  • Saijo Y, Hata S, Kyozuka J, Shimamoto K, Izui K (2000) Over-expression of a single Ca2+-dependent protein kinase confers both cold and salt/drought tolerance on rice plants. Plant J 23:319–327

    Article  CAS  PubMed  Google Scholar 

  • Sakamoto A, Murata N (2001) The use of bacterial choline oxidase, a glycinebetaine-synthesizing enzyme, to create stress-resistant transgenic plants. Plant Physiol 125:180–188

    CAS  PubMed  Google Scholar 

  • Sakamoto A, Murata N (2002) The role of glycine betaine in the protection of plants from stress: clues from transgenic plants. Plant Cell Environ 25:163–171

    Article  CAS  PubMed  Google Scholar 

  • Sakamoto A, Alia, Murata N (1998) Metabolic engineering of rice leading to biosynthesis of glycinebetaine and tolerance to salt and cold. Plant Mol Biol 38:1011–1019

    CAS  PubMed  Google Scholar 

  • Sakamoto A, Valverde R, Alia, Chen THH, Murata N (2000) Transformation of Arabidopsis with the codA gene for choline oxidase enhances freezing tolerance of plants. Plant J 22:449–453

    PubMed  Google Scholar 

  • Schöffl F, Prändl R, Reindl A (1998) Regulation of the heat-shock response. Plant Physiol 117:1135–1141

    PubMed  Google Scholar 

  • Seki M, Narusaka M, Abe H, Kasuga M, Yamaguchi-Shinozaki K, Carninci P, Hayashizaki Y, Shinozaki K (2001) Monitoring the expression pattern of 1,300 Arabidopsis genes under drought and cold stresses by using a full-length cDNA microarray. Plant Cell 13:61–72

    CAS  PubMed  Google Scholar 

  • Serrano R, Rodriguez-Navarro A (2001) Ion homeostasis during salt stress in plants. Curr Opin Cell Biol 13:399–404

    Google Scholar 

  • Serrano R, Mulet JM, Rios G, Marquez JA, de Larrinoa IF, Leube MP, Mendizabal I, Pascual-Ahuir A, Proft M, Ros R, Montesinos C (1999) A glimpse of the mechanisms of ion homeostasis during salt stress. J Exp Bot 50:1023–1036

    Article  CAS  Google Scholar 

  • Sheveleva E, Chmara W, Bohnert HJ, Jensen RG (1997) Increased salt and drought tolerance by d-ononitol production in transgenic Nicotiana tabacum L. Plant Physiol 115:1211–1219

    CAS  Google Scholar 

  • Sheveleva EV, Marquez S, Chmara W, Zegeer A, Jensen RG, Bohnert HJ (1998) Sorbitol-6-phosphate dehydrogenase expression in transgenic tobacco. Plant Physiol 117:831–839

    Article  CAS  PubMed  Google Scholar 

  • Shi H, Ishitani M, Kim C, Zhu JK (2000) The Arabidopsis thaliana salt tolerance gene SOS1 encodes a putative Na+/H+ antiporter. Proc Natl Acad Sci USA 97:6896–6901

    CAS  PubMed  Google Scholar 

  • Shi H, Quintero FJ, Pardo JM, Zhu JK (2002) Role of SOS1 as a plasma membrane Na+/H+ antiporter that controls long distance Na+ transport in plant. Plant Cell 14:465–477

    Article  CAS  PubMed  Google Scholar 

  • Shi H, Lee BH, Wu SJ and Zhu JK (2003) Overexpression of a plasma membrane Na+/H+ antiporter gene improves salt tolerance in Arabidopsis thaliana. Nature Biotech 21:81–85

    Article  CAS  Google Scholar 

  • Shinozaki K, Yamaguchi-Shinozaki K (1997) Gene expression and signal transduction in water-stress response. Plant Physiol 115:327–334

    CAS  Google Scholar 

  • Shinozaki K, Yamaguchi-Shinozaki K (2000) Molecular responses to dehydration and low temperature: differences and cross-talk between two stress signalling pathways. Curr Opin Plant Biol 3:217–223

    CAS  PubMed  Google Scholar 

  • Sivamani E, Bahieldin A, Wraithc JM, Al-Niemia T, Dyera WE, Hod THD, 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

    CAS  PubMed  Google Scholar 

  • Skriver K, Mundy J (1990) Gene expression in response to abscisic acid and osmotic stress. Plant Cell 2:503–512

    CAS  PubMed  Google Scholar 

  • Smirnoff N (1998) Plant resistance to environmental stress. Curr Opin Biotech 9:214–219

    Article  CAS  PubMed  Google Scholar 

  • Smýkal P, Mašín J, Hrdý I, Konopásek I, Žárský V (2000) Chaperone activity of tobacco HSP18, a small heat-shock protein, is inhibited by ATP. Plant J 23:703–713

    Article  PubMed  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  CAS  PubMed  Google Scholar 

  • 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 94:1035–40

    CAS  PubMed  Google Scholar 

  • Studer S, Narberhaus F (2000) Chaperone activity and homo- and hetero-oligomer formation of bacterial small heat shock proteins. J Biol Chem 275:37212–37218

    CAS  PubMed  Google Scholar 

  • Sugino M, Hibino T, Tanaka Y, Nii N, Takabe T (1999) Overexpression of DnaK from a halotolerant cyanobacterium Aphanothece halophytice acquires resistance to salt stress in transgenic tobacco plants. Plant Sci 146:81–88

    Article  CAS  Google Scholar 

  • Sun W, Bernard C, van de Cotte B, Van Montagu M, Verbruggen, N (2001) At-HSP17.6A, encoding a small heat-shock protein in Arabidopsis, can enhance osmotolerance upon overexpression. Plant J 27:407–415

    Article  CAS  PubMed  Google Scholar 

  • Suzuki TC, Denise C, Krawitz DC, Vierling E (1998) The chloroplast small heat-shock protein oligomer is not phosphorylated and does not dissociate during heat stress in vivo. Plant Physiol 116:1151–1161

    Article  CAS  PubMed  Google Scholar 

  • Sze H, Lia X, Palmgrenb MG (1999) Energization of plant cell membranes by H-pumping ATPases: regulation and biosynthesis. Plant Cell 11:677–690

    Article  CAS  PubMed  Google Scholar 

  • Tarczynski MC, Jensen RG, Bohnert HJ (1993) Stress protection of transgenic tobacco by production of the osmolyte mannitol. Science 259:508–510

    CAS  Google Scholar 

  • Thomashow MF (1998) Role of cold-responsive genes in plant freezing tolerance. Plant Physiol 118:1–7

    Article  CAS  PubMed  Google Scholar 

  • Thomashow MF (1999) Plant cold acclimation: freezing tolerance genes and regulatory mechanisms. Annu Rev Plant Biol 50:571–599

    Article  CAS  Google Scholar 

  • Thomashow MF, Gilmour SJ, Stockinger EJ, Jaglo-Ottosen KR, Zarka DG (2001) Role of the Arabidopsis CBF transcriptional activators in cold acclimation. Physiol Plant 112:171–175

    CAS  Google Scholar 

  • Török Z, Goloubinoff P, Horváth I, Tsvetkova NM, Glatz A, Balogh G, Varvasovszki V, Los DA, Vierling E, Crowe JH, Vígh L (2001) Synechocystis HSP17 is an amphitropic protein that stabilizes heat-stressed membranes and binds denatured proteins for subsequent chaperone-mediated refolding. Proc Natl Acad Sci USA 98:3098–3103

    Article  PubMed  Google Scholar 

  • Tyerman SD, Bohnert HJ, Maurel C, Steudle E, Smith JAC (1999) Plant aquaporins: their molecular biology, biophysics and significance for plant water relations. J Exp Bot 50:1055–1071

    CAS  Google Scholar 

  • Uno Y, Furihata T, Abe H, Yoshida R, Shinozaki K, Yamaguchi-Shinozaki K (2000) Novel Arabidopsis bZIP transcription factors involved in an abscisic-acid-dependent signal transduction pathway under drought and high salinity conditions. Proc Natl Acad Sci USA 97:11632–11637

    CAS  PubMed  Google Scholar 

  • Van Camp W, Capiau K, Van Montagu M, Inze D, Slooten L. (1996) Enhancement of oxidative stress tolerance in transgenic tobacco plants overproducing Fe-superoxide dismutase in chloroplasts. Plant Physiol 112:1703–1714

    PubMed  Google Scholar 

  • Veinger L, Diamant S, Buchner J, Goloubinoff P (1998) The small heat-shock protein IbpB from Escherichia coli stabilizes stress-denatured proteins for subsequent refolding by a multichaperone network. J Biol Chem 273:11032–11037

    Article  CAS  PubMed  Google Scholar 

  • Vierling E (1991) The roles of heat-shock proteins in plants. Annu Rev Plant Biol 42:579–620

    Article  CAS  Google Scholar 

  • Vierling E, Kimpel JA (1992) Plant responses to environmental stress. Curr Opin Biotech 3:164–170

    CAS  PubMed  Google Scholar 

  • Wang WX, Vinocur B, Shoseyov O, Altman A (2001a) Biotechnology of plant osmotic stress tolerance: physiological and molecular considerations. Acta Hort 560:285–292

    CAS  Google Scholar 

  • Wang WX, Pelah D, Alergand T, Shoseyov O, Altman A (2001b) Denaturate stable and/or protease resistant, chaperone-like oligomeric proteins, polynucleotides encoding same and their uses. Provisional Patent Application No. 60/272,771, USA

  • Wang WX, Pelah D, Alergand T, Shoseyov O, Altman A (2002) Characterization of SP1, a stress-responsive, boiling-soluble, homo-oligomeric protein from aspen (Populus tremula L.). Plant Physiol 130:865–875

    Article  CAS  PubMed  Google Scholar 

  • Wang WX, Barak T, Vinocur B, Shoseyov O, Altman A (2003) Abiotic resistance and chaperones: possible physiological role of SP1, a stable and stabilizing protein from Populus. In: Vasil IK (ed) Plant biotechnology 2000 and beyond. Kluwer, Dordrecht, pp 439–443

  • Waters ER, Lee GJ, Vierling E (1996) Evolution, structure and function of the small heat shock proteins in plants. J Exp Bot 47:325–338

    CAS  Google Scholar 

  • Xu D, Duan X, Wang B, Hong B, Ho THD, 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

    CAS  Google Scholar 

  • Yamanouchi U, Yano M, Lin H, Ashikari M, Yamada K (2002) A rice spotted leaf gene, Spl7, encodes a heat stress transcription factor protein. Proc Natl Acad Sci USA 99:7530–7535

    Article  CAS  PubMed  Google Scholar 

  • Zhang HX, Blumwald E (2001) Transgenic salt-tolerant tomato plants accumulate salt in foliage but not in fruit. Nature Biotech 19:765–768

    Article  CAS  Google Scholar 

  • Zhang HX, Hodson JN, Williams JP, Blumwald E (2001) Engineering salt-tolerant Brassica plants: characterization of yield and seed oil quality in transgenic plants with increased vacuolar sodium accumulation. Proc Natl Acad Sci USA 98:12832–12836

    CAS  Google Scholar 

  • Zhu JK (2001a) Plant salt tolerance. Trends Plant Sci 6:66–71

    CAS  PubMed  Google Scholar 

  • Zhu JK (2001b) Cell signaling under salt, water and cold stresses. Curr Opin Plant Biol 4:401–406

    CAS  PubMed  Google Scholar 

  • Zhu JK (2002) Salt and drought stress signal transduction in plants. Annu Rev Plant Biol 53:247–73

    Article  CAS  PubMed  Google Scholar 

  • Zhu JK, Hasegawa PM, Bressan RA (1997) Molecular aspects of osmotic stress in plants. Crit Rev Plant Sci 16:253–277

    CAS  Google Scholar 

  • Zimmermann S, Sentenac H (1999) Plant ion channels: from molecular structures to physiological functions. Curr Opin Plant Biol 2:477–482

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgements

This work was supported by the European Union (grant no. QLK5-2000-01377-ESTABLISH), and by the Horowitz Fund, Yissum, Israel.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Arie Altman.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Wang, W., Vinocur, B. & Altman, A. Plant responses to drought, salinity and extreme temperatures: towards genetic engineering for stress tolerance. Planta 218, 1–14 (2003). https://doi.org/10.1007/s00425-003-1105-5

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00425-003-1105-5

Keywords

Navigation