Advertisement

Springer Nature is making SARS-CoV-2 and COVID-19 research free. View research | View latest news | Sign up for updates

The accumulation of a cold-regulated chloroplastic protein is light-dependent

Abstract

The protein encoded by cDNA clone pt59 and induced in barley (Hordeum vulgare L.) by cold was overexpressed in coli to produce the matching antibody, which in vivo recognized a cold-induced protein of 14 kDa (COR 14) that was found in the chloroplast stroma. The accumulation of COR14 occurred only at low temperatures after even a brief exposure of the plants to light. Plants grown and fully hardened in the dark accumulated a reduced amount of pt59-corresponding mRNA and only traces of COR14. Light exposure for as short as 5 min was enough to normalize the expression of pt59-corresponding mRNA and increase the accumulation of COR14. These findings indicate that one or more light-dependent factors are involved in transcription of the gene and accumulation of the protein. The COR14 protein was stored in amounts only slightly greater in the resistant barley cultivar Onice than in the susceptible cultivar Gitane, although the former had a higher induction-temperature threshold for COR14 than the latter. This fact is an evolutionary advantage, enabling the resistant varieties in the field to prepare for the cold well ahead of the susceptible ones.

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

Abbreviations

COR:

cold regulated

COR14:

cold-induced protein of 14 kDa

ORF:

open reading frame

PMSF:

phenyl-methylsulfonyl fluoride

References

  1. Angenent, G.C., Busscher, M., Franken, J., Mol, J.N.M., Van Tunen, A.J. (1992) Differential expression of two MADS box genes in wild-type and mutant petunia flowers. Plant cell 4, 983–993

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

  3. Cattivelli, L. Bartels D. (1992) Biochemistry and molecular biology of cold-inducible enzymes and proteins in higher plants. In: Inducible plant proteins (S.E.B. Seminar Ser. 49), pp. 267–288, Wray, J.L., ed. Cambridge University Press

  4. Cerovic, Z.G., Plesnicar, M. (1984) An improved procedure for the isolation of intact chloroplasts of high photosynthetic capacity. Biochem. J. 223, 543–545

  5. Chauvin, L.-P., Houde, M., Sarhan, F. (1993) A leaf-specific gene stimulated by light during wheat acclimation to low temperature. Plant Mol. Biol. 23, 255–265

  6. Crosatti, C., Rizza, F., Cattivelli, L. (1994) Accumulation and characterization of the 75 kDa protein induced by low temperature in barley. Plant Sci. 97, 39–46

  7. Dunn, M.A., Hughes, M.A., Pearce, R.S., Jack, P.L. (1990) Molecular characterization of a barley gene induced by cold treatment. J. Exp. Bot. 41, 1405–1413

  8. Dunn, M.A., Hughes, M.A., Zhang, L., Pearce, R.S., Quigley, A.S., Jack, P.L. (1991) Nucleotide sequence and molecular analysis of the low temperature induced cereal gene, BLT4. Mol. Gen. Genet. 229, 389–394

  9. Feinberg, A.P., Vogelstein, B. (1984) A technique for radiolabelling DNA restriction endonuclease fragments to high specific activity. Anal. Biochem. 137, 266–267

  10. Gavel, Y., von Heijne, G. (1990) A conserved cleavage-site motif in chloroplast transit peptides. FEBS Lett. 261, 455–458

  11. Grossi, M., Cattivelli, L., Terzi, V., Stanca, A.M. (1992) Modification of gene expression induced by ABA, in relation to drought and cold stress in barley shoots. Plant Physiol. Biochem. 30, 97–103

  12. Hincha, D.K., Schmitt, J.M. (1988) Mechanical freeze-thaw damage and frost hardening in leaves and isolated thylakoids from spinach. II. Frost hardening reduces solute permeability and increases extensibility of thylakoid membranes. Plant Cell Environ. 11, 48–50

  13. Hincha, D.K., Schmitt, J.M. (1992) Cryoprotective leaf proteins: assay methods and heat stability. J. Plant Physiol. 140, 236–240

  14. Hincha, D.K., Heber, U., Schmitt, J.M. (1990) Proteins from frosthardy leaves protect thylakoids against mechanical freeze-thaw damage in vitro. Planta 180, 416–419

  15. Houde, M., Danyluk, J., Laliberte, J.F., Rassart, E., Dhindsa, R.S., Sarhan, F. (1992a) Cloning, characterization and expression of a cDNA encoding a 50-kilodalton protein specifically induced by cold acclimation in wheat. Plant Physiol. 99, 1381–1387

  16. Houde, M., Dhindsa, R.S., Sarhan, F. (1992b) A molecular marker to select for freezing tolerance in Gramineae. Mol. Gen. Genet. 234, 43–48

  17. Huner, N.P.A., Öquist, G., Hurry, V.M., Krol, M., Falk, S., Griffit, M. (1993) Photosynthesis, photoinhibition and low temperature acclimation in cold tolerant plants. Photosynth. Res. 19–39

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

  19. Laemmli, U.K. (1970) Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227, 680–685

  20. Láng, V., Palva, E.T. (1992) 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, 951–962

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

  22. Lapointe, L., Huner, N.P.A., Carpentier, R., Ottander, C. (1991) Resistance to low temperature photoinhibition is not associated with isolated thylakoid membranes of winter rye. Plant Physiol. 97, 804–810

  23. Levitt, J. (1980) Response of plants to environmental stresses. Vol. 1: Chilling, freezing, and high temperature stresses. Academic Press, New York

  24. Lin, C., Thomashow, M (1992) DNA sequence analysis of a complementary DNA for cold-regulated Arabidopsis COR15 and characterization of the CPR15 polypeptide. Plant Physiol. 99, 519–525

  25. 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. 83, 375–380

  26. Neven, L.G., Haskell, D.W., Hofig, A., Li, Q.B., Guy, C.L. (1993) Characterization of a spinach gene responsive to low temperature and water stress. Plant Mol. Biol. 21, 291–305

  27. Öquist, G., Huner, N.P.A. (1993) Cold-hardening-induced resistance to photoinhibition of photosynthesis in winter rye is dependent upon an increased capacity for photosynthesis. Planta 189, 150–156

  28. Rizza, F., Crosatti, C., Stanca, A.M., Cattivelli, L. (1994) Studies for assessing the influence of hardening on cold tolerance of barley genotypes. Euphytica 75, 131–138

  29. Rohde, W., Rosch, K., Kröger, K., Salamini, F. (1991) Nucleotide sequence of a Hordeum vulgare gene encoding a glycine-rich protein with homologue to vertebrate cytokeratins. Plant Mol. Biol. 14, 1057–1059

  30. Sambrook, J., Fritsch, E.F., Maniatis, T. (1989) A laboratory manual, 2nd edn. Cold Spring Harbor Laboratory, Cold Spring Harbor, N.Y.

  31. Smith, D.B., Johnson, K.S. (1988) Single-step purification of polypeptides expressed in Escherichia coli as fusions with glutathione S-transferase. Gene 67, 31–40

  32. Weretilnyk, E.A., Hanson, A.D. (1990) Molecular cloning of a plant betaine-aldehyde dehydrogenase, an enzyme implicated in adaptation to salinity and drought. Proc. Natl. Acad. Sci. USA 87, 2745–2749

  33. aguchi-Shinozaki, K., Shinozaki, K. (1994) A novel cis-acting element in an Arabidopsis gene is involved in responsiveness to drought, low-temperature, or high-salt stress. Plant Cell 6, 251–264

Download references

Author information

Additional information

The authors wish to thank Prof. S. Cavirani (Istituto di Malattie Infettive, Facolta di Medicina Veterinaria University of Parma, Italy) for his help in antibody preparation. This work was funded wholly by the EC's BIOTECH Programme, as part of the project of Technological Priority 1993–1996

Rights and permissions

Reprints and Permissions

About this article

Cite this article

Crosatti, C., Soncini, C., Stanca, A.M. et al. The accumulation of a cold-regulated chloroplastic protein is light-dependent. Planta 196, 458–463 (1995). https://doi.org/10.1007/BF00203644

Download citation

Abstract

  • Barley
  • Hordeum
  • Cold acclimation
  • Cold-regulated protein