Skip to main content
Log in

Hydration-state-responsive proteins link cold and drought stress in spinach

  • Published:
Planta Aims and scope Submit manuscript

Abstract

Spinach (Spinacia oleracea L.) seedlings exposed to low nonfreezing temperatures (0–10° C) that promote cold acclimation, synthesize a variety cold-acclimation proteins and at the same time acquire a greater ability to withstand cellular dehydration imposed by the freezing of tissue water. Two of these proteins (160 and 85 kDa) become more abundant over time at low temperature. In addition, a small decline in tissue water status from a maximally hydrated state also appears to be associated with an initiation of the accumulation of these proteins at a noninductive temperature. Imposing a severe water stress on young seedlings grown at 25° C by withholding water leads to substantial accumulation of the 160- and 85-kDa proteins, and maximal induction of freezing tolerance. This evidence implies that responses to cold acclimation and water stress involve common mechanisms, and further establishes the linkage of these two proteins with stresses having an osmotic component.

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

Access this article

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

Instant access to the full article PDF.

Similar content being viewed by others

Abbreviations

ABA:

abscisic acid

CAP:

cold-acclimation protein

kDa:

kilodaltons

References

  • Ackerson, R.C. (1985) Osmoregulation in cotton in response to water stress. Plant Physiol. 77, 309–312

    Google Scholar 

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

    Google Scholar 

  • Bartels, D., Schneider, K., Terstappen, G., Piakowski, D., Salamini, F. (1990) Molecular cloning of abscisic acid-modulated genes which are induced during desiccation of the resurrection plant Craterostigma plantagineum. Planta 181, 27–34

    CAS  Google Scholar 

  • Bozarth, C., Mullet, J.E., Boyer, J.S. (1987) Cell wall proteins at low water potentials. Plant Physiol. 85, 261–267

    Google Scholar 

  • Bradford, M.M. (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal. Biochem. 72, 248–254

    Google Scholar 

  • Close, T.J., Kortt, A.A., Chandler, P.M. (1989) A cDNA-based comparison of dehydration-induced proteins (dehydrins) in barley and corn. Plant Mol. Biol. 13, 95–108

    Google Scholar 

  • Cloutier, Y. (1983) Changes in the electrophoretic patterns of the soluble proteins of winter wheat and rye following cold acclimation and desiccation stress. Plant Physiol. 71, 400–403

    Google Scholar 

  • Creelman, R.A., Mason, H.S., Bensen, R.J., Boyer, J.S., Mullet, J.E. (1990) Water deficit and abscisic acid cause differential inhibition of shoot versus root growth in soybean seedlings. Analysis of growth, sugar accumulation, and gene expression. Plant Physiol. 92, 205–214

    Google Scholar 

  • Dure, L, III, Crouch, M., Harada, J., Ho, T.-H.D., Mundy, J., Quatrano, R., Thomas, T., Sung, Z.R. (1989) Common amino acid sequence domains among the LEA proteins of higher plants. Plant Mol. Biol. 12, 475–486

    Google Scholar 

  • Genty, B., Briantais, J.-M., Vieira Da Silva, J.B. (1987) Effects of drought on primary photosynthetic processes of cotton leaves. Plant Physiol. 83, 360–364

    Google Scholar 

  • Gilmour, S.J., Artus, N.N., Thomashow, M.F. (1992) cDNA sequence analysis and expression of two cold-regulated genes of Arabidopsis thaliana. Plant Mol. Biol. 18, 13–21

    Google Scholar 

  • Gomez, J., Sanchez-Martinez, D., Stiefel, V., Rigau, J., Puigdomenech, P., Pages, M. (1988) A gene induced by the plant hormone abscisic acid in response to water stress encodes a glycine-rich protein. Nature 334, 262–264

    Google Scholar 

  • Guy, C.L. (1990) Cold acclimation and freezing stress tolerance: Role of protein metabolism. Annu. Rev. Plant Physiol. Plant Mol. Biol. 41, 187–223

    Google Scholar 

  • Guy, C.L., Haskell, D. (1987) Induction of freezing tolerance in spinach is associated with the synthesis of cold acclimation induced proteins. Plant Physiol. 84, 872–878

    Google Scholar 

  • Guy, C.L., Haskell, D. (1988) Detection of polypeptides associated with the cold acclimation process in spinach. Electrophoresis 9, 787–796

    Google Scholar 

  • Hahn, M., Walbot, V. (1989) Effects of cold-treatment on protein synthesis and mRNA levels in rice leaves. Plant Physiol. 91, 930–938

    Google Scholar 

  • Hajela, R.K., Horvath, D.P., Gilmour, S.J., Thomashow, M.F. (1990) Molecular cloning and expression of cor (cold regulated) genes in Arabidopsis thaliana. Plant Physiol. 93, 1246–1252

    Google Scholar 

  • Hsiao, T.C. (1973) Plant responses to water stress. Annu. Rev. Plant Physiol. 24, 519–570

    Google Scholar 

  • Kurkela, S., Franck, M. (1990) Cloning and characterization of a cold- and ABA-inducible Arabidopsis gene. Plant Mol. Biol. 15, 137–144

    Google Scholar 

  • Läng, V., Heino, P., Palva, E.T. (1989) Low temperature acclimation and treatment with exogenous abscisic acid induce common polypeptides in Arabidopsis thaliana. Theoret. Appl. Genet. 77, 729–734

    Google Scholar 

  • Levitt, J. (1951) Frost, drought, and heat resistance. Annu. Rev. Plant Physiol. 2, 245–268

    Google Scholar 

  • Lin, C., Guo, W.W., Everson, E., Thomashow, M.F. (1990) Cold acclimation in Arabidopsis and wheat. A response associated with expression of related genes encoding “boiling stable” polypeptides. Plant Physiol. 94, 1078–1083

    Google Scholar 

  • Markhart, A.H. (1985) Comparative water relations of Phaseolus vulgaris L. and Phaseolus acutifolius Gray. Plant Physiol. 77, 113–117

    Google Scholar 

  • Mason, H.S., Mullet, J.E., Boyer, J.S. (1988) Polysomes, messenger RNA and growth in soybean stems during development and water deficit. Plant Physiol. 86, 725–733

    Google Scholar 

  • Mohapatra, S.S., Wolfraim, L., Poole, R.J., Dhindsa, R.S. (1989) Molecular cloning and relationship to freezing tolerance of cold-acclimation specific genes of alfalfa. Plant Physiol. 89, 375–380

    Google Scholar 

  • Morilla, C.A., Boyer, J.S., Hageman, R.H. (1973) Nitrate reductase activity and polyribosomal content of corn (Zea mays L.) having low leaf water potentials. Plant Physiol. 51, 817–824

    Google Scholar 

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

    Google Scholar 

  • Neven, L.G., Haskell, D.W., Guy, C.L., Denslow, N., Klein, P.A., Green, L.G., Silverman, A. (1992) Association of 70 kDa heat shock cognate proteins with cold acclimation. Plant Physiol., in press

  • Nordin, K., Heino, P., Palva E.T. (1991) Separate signal pathways regulate the expression of a low-temperature-induced gene in Arabidopsis thaliana (L.) Heynh. Plant Mol. Biol. 16, 1061–1071

    Google Scholar 

  • Oosterhuis, D.M., Wullschleger, S.D. (1987) Osmotic adjustment in cotton (Gossypium hirsutum L.) leaves and roots in response to water stress. Plant Physiol. 84, 1154–1157

    Google Scholar 

  • Rao, I.M., Sharp, R.E., Boyer, J.S. (1987) Leaf magnesium alters photosynthetic response to low water potentials in sunflower. Plant Physiol. 84, 1214–1219

    Google Scholar 

  • Saab, I.N., Sharp, R.E., Pritchard, J., Voetberg, G.S. (1990) Increased endogenous abscisic acid maintains primary root growth and inhibits shoot growth of maize seedlings at low water potentials. Plant Physiol. 93, 1329–1336

    Google Scholar 

  • Siminovitch, D., Cloutier, Y. (1982) Twenty-four-hour induction of freezing and drought tolerance in plumules of winter rye seedlings by desiccation stress at room temperature in the dark. Plant Physiol. 69, 250–255

    Google Scholar 

  • Stebbins, G.L. (1972) Flowering Plants: Evolution above the species level. Belknap, Harvard Boston

    Google Scholar 

  • Voetberg, G.S., Sharp, R.E. (1991) Growth of the maize primary root at low water potentials. III. Role of increased proline deposition in osmotic adjustment. Plant Physiol. 96, 1125–1130

    Google Scholar 

  • Yelenosky, G., Guy, C.L. (1989) Freezing tolerance of citrus, spinach, and petunia leaf tissue. Osmotic adjustment and sensitivity to freeze induced cellular dehydration. Plant Physiol. 89, 444–451

    Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Additional information

We thank T. Sinclair and K. Cline for critical reading and discussions, N. Denslow for assistance with protein sequencing methods, and L. Greene, S. Henry for preparing the monoclonal antibodies. The work was made possible by support from the USDA Competitive Grants Program No. 90-37280-5527, the Institute for Food and Agricultural Sciences, and through access to the protein sequencing and hybridoma facilities of the Interdisciplinary Center for Biotechnology Research at the University of Florida. Florida Agricultural Experiment Station Journal Series R-02399.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Guy, C., Haskell, D., Neven, L. et al. Hydration-state-responsive proteins link cold and drought stress in spinach. Planta 188, 265–270 (1992). https://doi.org/10.1007/BF00216823

Download citation

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF00216823

Key words

Navigation