Plant Molecular Biology

, Volume 26, Issue 1, pp 131–144

Characterization and differential expression of dhn/lea/rab-like genes during cold acclimation and drought stress in Arabidopsis thaliana

  • Björn V. Welin
  • Åke Olson
  • Maria Nylander
  • E. Tapio Palva
Mini-reviews

Abstract

We have characterized cDNAs for two new dhn/lea/rab (dehydrin, late embryogenesis-abundant, responsive to ABA)-related genes from Arabidopsis thaliana. The two genes were strongly induced in plants exposed to low temperature (4 °C) and were accordingly designated lti45 and lti30 (low temperature-induced). The lti45 gene product contains the conserved serine stretch and three lysine-rich repeats characteristic of DHN/LEA/RAB proteins and is very similar to another low temperature-responsive protein of A. thaliana, COR47 [17]. Both proteins have the same repeat structure and an overall amino acid identity of 64%. This structural similarity of the proteins and the tandem array of the genes suggest that this gene pair arose through a duplication. The other polypeptide, LTI30, consists of several lysine-rich repeats, a structure found in CAP85, a low temperature-and water stress-responsive protein in spinach [41] and similar proteins found in wheat [20].

The expression pattern of the five dhn/lea/rab-related genes (cor47, dhnX, lti30, lti45 and rab18) identified so far in A. thaliana, was characterized in plants exposed to low temperature, drought and abscisic acid (ABA). Expression of both lti30 and lti45 was mainly responsive to low temperature similar to cor47. The lti45 and lti30 genes show only a weak response to ABA in contrast to cor47, which is moderately induced by this hormone. The three genes were also induced in severely water-stressed plants although the expression of lti30 and lti45 was rather low. In contrast to these mainly low temperature-induced genes, the expression of rab18 was strongly induced both in water-stressed and ABA-treated plants but was only slightly responsive to cold. The dhnX gene showed a very different expression pattern. It was not induced with any of the treatments tested but exhibited a significant constitutive expression. The low-temperature induction of the genes in the first group, lti30 and lti45, is ABA-independent, deduced from experiments with the ABA-deficient (aba-1) and ABA-insensitive (abi1) mutants of A. thaliana, whereas the induction of rab18 is ABA-mediated. The expression of dhnX was not significantly affected in the ABA mutants.

Key words

abscisic acid Arabidopsis thaliana cold acclimation LEA RAB water stress 

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References

  1. 1.
    Baker J, Steele C, DureIII L: Sequence and characterization of 6 Lea proteins and their genes from cotton. Plant Mol Biol 11: 277–291 (1988).Google Scholar
  2. 2.
    Cattivelli L, Bartels D: Molecular cloning and characterization of cold-regulated genes in barley. Plant Physiol 93: 1504–1510 (1990).Google Scholar
  3. 3.
    Cattivelli L, Bartels D: Biochemistry and molecular biology of cold-inducible enzymes and proteins in higher plants. In: Wray JL (ed) Inducible Plant Proteins, pp. 267–288. Society of Experimental Biologists Seminar Series 49. Cambridge University Press, Cambridge, UK (1992).Google Scholar
  4. 4.
    Chen HH, Li PH, Brenner ML: Involvement of abscisic acid in potato cold acclimation. Plant Physiol 71: 362–365 (1983).Google Scholar
  5. 5.
    Chen HH, Gusta LV: Abscisic acid-induced freezing resistance in cultured plant cells. Plant Physiol 73: 71–75 (1983).Google Scholar
  6. 6.
    Close TJ, Kortt AA, Chandler PM: A cDNA-based comparison of dehydration-induced proteins (dehydrins) in barley and corn. Plant Mol Biol 13: 95–108 (1989).Google Scholar
  7. 7.
    Close TJ, Fenton RD, Moonan F: A view of plant dehydrins using antibodies specific to the carboxy terminal peptide. Plant Mol Biol 23: 279–286 (1993).Google Scholar
  8. 8.
    Close TJ, Lammers PJ: An osmotic stress protein of cyanobacteria is immunologically related to plant dehydrins. Plant Physiol 101: 773–779 (1993).Google Scholar
  9. 9.
    Cloutier Y, Siminovitch D: Correlation between cold-and drought-induced frost hardiness in winter wheat and rye varieties. Plant Physiol 69: 256–258 (1982).Google Scholar
  10. 10.
    Cloutier Y: Changes of protein patterns in winter rye following cold acclimation and desiccation stress. Can J Bot 62: 366–371 (1984).Google Scholar
  11. 11.
    Davies WJ, Jones HG: Abscisic Acid: Physiology and Biochemistry. BIOS Scientific Publishers, Oxford (1991).Google Scholar
  12. 12.
    Dellaporta SL, Wood J, Hicks JB: A plant DNA mini preparation: version II. Plant Mol Biol Rep 1: 19–21 (1983).Google Scholar
  13. 13.
    DureIII L, Crouch M, Harada J, Ho THD, Mundy J, Quatrano R, Thomas T, Sung ZR: Common amino acid sequence domains among the LEA proteins of higher plants. Plants Mol Biol 12: 475–486 (1989).Google Scholar
  14. 14.
    Dunn MA, Hughes MA, Pearce RS, Jack PL: Molecular characterization of a barley gene induced by cold treatment. J Exp Bot 41: 1405–1413 (1990).Google Scholar
  15. 15.
    Gilmour SJ, Hajela RK, Thomashow MF: Cold acclimation in Arabidopsis thaliana. Plant Physiol 87: 745–750 (1988).Google Scholar
  16. 16.
    Gilmour SJ, Thomashow MF: Cold acclimation and cold-regulated gene expression in ABA mutants of Arabidopsis thaliana. Plant Mol Biol 17: 1233–1240 (1991).Google Scholar
  17. 17.
    Gilmour SJ, Artus NN, Thomashow MF: cDNA sequence analysis and expression of two cold-regulated genes of Arabidopsis thaliana. Plant Mol Biol 18: 13–21 (1992).Google Scholar
  18. 18.
    Goday A, Sanchez-Martinez D, Gomez J, Puigdomenech P, Pages M: Gene expression in developing Zea mays embryos: regulation of a highly phosphorylated 23–25 kDa group of proteins. Plant Physiol 88: 564–569 (1988).Google Scholar
  19. 19.
    Godoy JA, Pardo JM, Pintor-Toro JA: A tomato cDNA clone inducible by salt stress and abscisic acid: nucleotide sequence and expression pattern. Plant Mol Biol 15: 695–705 (1990).Google Scholar
  20. 20.
    Guo W, Ward RW, Thomashow MF: Characterization of a cold-regulated wheat gene related to Arabidopsis cor47. Plant Physiol 100: 915–922 (1992).Google Scholar
  21. 21.
    Guy CL, Niemi KJ, Brambl R: Altered gene expression during cold acclimation of spinach. Proc Natl Acad Sci USA 82: 3673–3677 (1985).Google Scholar
  22. 22.
    Guy CL, Haskell D: Detection of polypeptides associated with cold acclimation process in spinach. Electrophoresis 9: 787–796 (1988).Google Scholar
  23. 23.
    Guy CL: Cold acclimation and freezing stress tolerance: role of protein metabolism. Annu Rev Plant Physiol Plant Mol Biol 41: 187–223 (1990).Google Scholar
  24. 24.
    Guy C, Haskell D, Neven L, Klein P, Smelser C: Hydration-state-responsive proteins link cold and drought stress in spinach. Planta 188: 265–270 (1992).Google Scholar
  25. 25.
    Heino P, Sandman G, Lång V, Nordin K, Palva ET: Abscisid acid deficiency prevents development of freezing tolerance in Arabidopsis thaliana (L.) Heynh. Theor Appl Genet 79: 801–806 (1990).Google Scholar
  26. 26.
    Hong B, Uknes S, Ho DT: Cloning and characterization of a cDNA encoding a mRNA rapidly induced by ABA in barley aleurone layers. Plant Mol Biol 11: 495–506 (1988).Google Scholar
  27. 27.
    Houde M, Danyluk J, Laliberté J, Rassart E, Dhindsa RS, Sarhan F: Cloning, characterization and expression of a cDNA encoding a 50-kilodalton protein specifically induced by cold acclimation in wheat. Plant Physiol 99: 1381–1387 (1992).Google Scholar
  28. 28.
    Jacobsen JV, Shaw DC: Heat-stable proteins and abscisic acid action in barley aleurone cells. Plant Physiol 91: 1520–1526 (1989).Google Scholar
  29. 29.
    Keith CM, McKersie BD: The effect of abscisic acid on the freezing tolerance of callus cultures of Lotus corniculatus L. Plant Physiol 80: 766–770 (1986).Google Scholar
  30. 30.
    Koornneef M, Jorna ML, Brinkhorst-van der Swan DLC, Karssen CM: The isolation of abscisic acid (ABA) deficient mutants by selection of induced revertants in non-germinating gibberillin sensitive lines of Arabidopsis thaliana (L.) Heynh. Theor Appl Genet 61: 385–393 (1982).Google Scholar
  31. 31.
    Koornneef M, Reuling G, Karssen CM: The isolation and characterization of abscisic acid-insensitive mutants of Arabidopsis thaliana. Physiol Plant 61: 377–383 (1984).Google Scholar
  32. 32.
    Kurkela S, Franck M, Heino P, Lång V, Palva ET: Cold induced gene expression in Arabidopsis thaliana L. Plant Cell Rep 7: 495–498 (1988).Google Scholar
  33. 33.
    Kurkela S, Franck M: Cloning and characterization of a cold-and ABA-inducible Arabidopsis gene. Plant Mol Biol 15: 137–144 (1990).Google Scholar
  34. 34.
    Levitt J: Responses of Plants to Environmental Stresses, vol. 1. Chilling, Freezing and High Temperature Stresses, 2nd ed. Academic Press, New York (1980).Google Scholar
  35. 35.
    Lin C, Guo WW, Everson E, Thomashow MF: Cold acclimation in Arabidopsis and wheat: a response associated with expression of related genes encoding ‘boiling-stable’ polypeptides. Plant Physiol 94: 1078–1083 (1990).Google Scholar
  36. 36.
    Logeman J, Schell J, Willmitzer L: Improved method for the isolation of RNA from plant tissues. Anal Biochem 163: 16–20 (1987).Google Scholar
  37. 37.
    Lång V, Heino P, Palva ET: Low temperature acclimation and treatment with exogenous abscisic acid induce common polypeptides in Arabidopsis thaliana (L.) Heynh. Theor Appl Genet 77: 729–734 (1989).Google Scholar
  38. 38.
    Lång V, Palva ET: The expression of a rab-related gene, rab18, is induced by abscisid acid during the cold acclimation process of Arabidopsis thaliana (L.) Heynh. Plant Mol Biol 20: 951–962 (1992).Google Scholar
  39. 39.
    Lång V, Mäntylä E, Welin B, Sundberg B, Palva ET: Alterations in water status, endogenous abscisic acid content and expression of rab18 during the development of freezing tolerance in Arabidopsis thaliana. Plant Physiol, in press (1994).Google Scholar
  40. 40.
    Mundy J, Chua N-H: Abscisic scid and water-stress induce the expression of a novel rice gene. EMBO J 7: 2279–2286 (1988).Google Scholar
  41. 41.
    Neven LG, Haskell DW, Hofig A, Li Q-B, Guy CL: Characterization of a spinach gene responsive to low temperature and water stress. Plant Mol Biol 21: 291–305 (1993).Google Scholar
  42. 42.
    Nordin K, Heino P, Palva ET: Separate signal pathways regulate the expression of a low-temperature-induced gene in Arabidopsis thaliana (L.) Heynh. Plant Mol Biol 16: 1061–1071 (1991).Google Scholar
  43. 43.
    Nordin K, Vahala T, Palva ET: Differential expression of two related, low-temperature-induced genes in Arabidopsis thaliana (L.) Heynh. Plant Mol Biol 21: 641–653 (1993).Google Scholar
  44. 44.
    Orr W, Keller WA, Singh J: Induction of freezing tolerance in an embryogenic cell suspension culture of Brassica napus by abscisic acid at room temperature. J Plant Physiol 126: 23–32 (1986).Google Scholar
  45. 45.
    Orr W, Iu B, White TC, Robert LS, Singh J: complementary DNA sequence of a low-temperature-induced Brassica napus gene with homology to the Arabidopsis thaliana kin1 gene. Plant Physiol 98: 1532–1534 (1992).Google Scholar
  46. 46.
    Ouellet F, Houde M, Sarhan F: Purification, characterization and cDNA cloning of the 200 kDa protein induced by cold acclimation in wheat. Plant Cell Physiol 34: 59–65 (1993).Google Scholar
  47. 47.
    Palta JP, Weiss LS: Ice formation and freezing injury: An overview on the survival mechanisms and molecular aspects of injury and cold acclimation in herbaceous plants. In: Li PH, Christersson L (eds) Advances in Plant Cold Hardiness, pp. 143–176. CRC Press, Boca Raton, FL (1993).Google Scholar
  48. 48.
    Palva ET: Gene expression under low temperature stress. In: Basra AS (ed) Stress-Induced Gene Expression in Plants, pp. 103–130. Harwood Academic Publishers, Reading (1993).Google Scholar
  49. 49.
    Piatowski D, Schneider K, Salamini F, Bartels D: Characterization of five abscisic acid-responsive cDNA clones isolated from the desiccation-tolerant plant Craterostigma plantagineum and their relationship to other water-stress genes. Plant Physiol 94: 1682–1688 (1990).Google Scholar
  50. 50.
    Reaney MJT, Gusta LV: Factors influencing the induction of freezing tolerance by abscisic acid in cell suspension cultures in Bromus inermis Leyss and Medicago sativa L. Plant Physiol 83: 423–427 (1987).Google Scholar
  51. 51.
    Rouse D, Gehring CA, Parish RW: Structure and sequence of a dehydrin-like gene in Arabidopsis thaliana. Plant Mol Biol 19: 531–532 (1992).Google Scholar
  52. 52.
    Sakai A, Larcher W: Frost Survival of Plants. Springer-Verlag, Berlin 321 pp. (1987).Google Scholar
  53. 53.
    Sambrook J, Fritsch EF, Maniatis T: Molecular Cloning: A Laboratory Manual. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY (1989).Google Scholar
  54. 54.
    Sanger F, Nicklen S, Coulsen AR: DNA sequencing with chain terminating terminators. Proc Natl Acad Sci USA 74: 5463–5467 (1977).Google Scholar
  55. 55.
    Siminovitch D, Cloutier Y: 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 (1982).Google Scholar
  56. 56.
    Skriver K, Mundy J: Gene expression in response to abscisic acid in osmotic stress. Plant Cell 2: 503–512 (1990).Google Scholar
  57. 57.
    Steponkus PL: Role of plasma membrane in freezing injury and cold acclimation. Annu Rev Plant Physiol 35: 543–584 (1984).Google Scholar
  58. 58.
    Sutton F, Ding X, Kenefick DG: Group 3 LEA gene HVA1 regulation by cold acclimation and deacclimation in two barley cultivars with varying freeze resistance. Plant Physiol 99: 338–340 (1992).Google Scholar
  59. 59.
    Thomashow MF: Molecular genetics of cold acclimation in higher plants. Adv Genet 28: 99–131 (1990).Google Scholar
  60. 60.
    Tseng MJ, Li PH: Changes in protein synthesis and translatable messenger RNA populations associated with ABA-induced cold hardiness in potato (Solanum commersonii). Physiol Plant 81: 349–358 (1991).Google Scholar
  61. 61.
    Vilardell J, Goday A, Freire MA, Torrent M, Martinez MC, Torne JM, Pages M: Gene sequence, developmental expression, and protein phosphorylation of RAB-17 in maize. Plant Mol Biol 14: 423–432 (1990).Google Scholar
  62. 62.
    Weiser CJ: Cold resistance and injury in woody plants. Science 169: 1269–1278 (1970).Google Scholar
  63. 63.
    Weretilnyk E, Orr W, White TC, Iu B, Singh J: Characterization of three related low temperature regulated cDNAs from winter Brassica napus. Plant Physiol 101: 171–177 (1993).Google Scholar
  64. 64.
    Wilhelm KS, Thomashow MF: Arabidopsis thaliana cor15b, an apparent homologue of cor15a, is strongly responsive to cold and ABA, but not drought. Plant Mol Biol 23: 1073–1077 (1993).Google Scholar
  65. 65.
    Wolfraim LA, Langis R, Tyson H, Dhindsa RS: cDNA sequence, expression and transcript stability of a cold acclimation-specific gene, cas18, of alfalfa (Medicago falcata) cells. Plant Physiol 101: 1275–1282 (1993).Google Scholar
  66. 66.
    Zeevaart JAD, Creelman RA: Metabolism and physiology of abscisic acid. Annu Rev Plant Physiol Plant Mol Biol 39: 439–473 (1988).Google Scholar
  67. 67.
    Zhu B, Chen THH, Li PH: Expression of an ABA-responsive osmotin-like gene during the induction of freezing tolerance in Solanum commersonii. Plant Mol Biol 21: 729–735 (1993).Google Scholar

Copyright information

© Kluwer Academic Publishers 1994

Authors and Affiliations

  • Björn V. Welin
    • 1
  • Åke Olson
    • 1
  • Maria Nylander
    • 1
  • E. Tapio Palva
    • 1
  1. 1.Department of Molecular Genetics, Uppsala Genetic CenterSwedish University of Agricultural SciencesUppsalaSweden

Personalised recommendations