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Differential transcript induction of parsley pathogenesis-related proteins and of a small heat shock protein by ozone and heat shock

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Abstract

Parsley (Petroselinum crispum L.) is known to respond to pathogen attack by the synthesis of furanocoumarins and to UV irradiation by the synthesis of flavone glycosides whereas ozone treatment results in the induction of both pathways. A cDNA library from parsley plants was differentially screened using labelled reverse-transcribed poly(A)+ RNA isolated from ozone-treated parsley plants. This resulted in the isolation of 13 independent cDNA clones representing ozone-induced genes and of 11 cDNA clones representing ozone-repressed genes. DNA sequencing of several clones resulted in the identification of pathogenesis-related protein 1-3 (PR1-3), of a new member of PR1 cDNAs (PR1-4) and of a small heat shock protein (sHSP). Northern blot analyses showed a transient induction of the three mRNA species after ozone fumigation. In contrast, heat shock treatment of parsley plants resulted in an increase of sHSP mRNA whereas no increase for transcripts of PR1-3 and PR1-4 could be observed. This is the first characterized sHSP cDNA clone for plants induced by heat shock, as well as by oxidative stress caused by ozone.

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References

  1. Almoguera C, Jordano J: Developmental and environmental concurrent expression of sunflower dry-seed-stored low-molecular-weight heat-shock protein and Lea mRNAs. Plant Mol Biol 19: 781–792 (1992).

    Google Scholar 

  2. Apostol I, Heinstein PF, Low PS: Rapid stimulation of an oxidative burst during elicitation of cultured plant cells. Plant Physiol 90: 109–116 (1989).

    Google Scholar 

  3. Benton WD, Davis RW: Screening λgt recombinant clones by hybridization to single plaques in situ. Science 196: 180–182 (1977).

    Google Scholar 

  4. Bollmann J, Hahlbrock K: Timing of changes in protein synthesis pattern in elicitor-treated cell suspension cultures of parsley (Petroselinum crispum). Z Naturforsch 45c: 1011–1020 (1990).

    Google Scholar 

  5. Brederode FTh, Linthorst HJM, Bol JF: Differential induction of acquired resistance and PR gene expression in tobacco by virus infection, etephon treatment, UV light and wounding. Plant Mol Biol 17: 1117–1126 (1991).

    Google Scholar 

  6. Cajone F, Bernelli-Zazzera A: Oxidative stress induces a subset of heat shock proteins in rat hepatocytes and MH1C1 cells. Chem-Biol Interact 65: 235–246 (1988).

    Google Scholar 

  7. Chen Q, Lauzon LM, DeRocher AE, Vierling E: Accumulation, stability, and localization of a major chloroplast heat-shock protein. J Cell Biol 110: 1873–1883 (1990).

    Google Scholar 

  8. Conklin PL, Last RL: Differential accumulation of antioxidant mRNAs in Arabidopsis thaliana exposed to ozone. Plant Physiol 109: 203–212 (1995).

    Google Scholar 

  9. Courgeon A-M, Rollet E, Becker J, Maisonhaute C, Best-Belpomme M: Hydrogen-peroxide (H2O2) induces actin and some heat-shock proteins in Drosophila cells. Eur J Biochem 171: 163–170 (1988).

    Google Scholar 

  10. DeRocher AE, Helm KW, Lauzon LM, Vierling E: Expression of a conserved family of cytoplasmic low molecular weight heat shock proteins during heat stress and recovery. Plant Physiol 96: 1038–1047 (1991).

    Google Scholar 

  11. DeRocher AE, Vierling E: Developmental control of small heat shock protein expression during pea seed maturation. Plant J 5: 93–102 (1994).

    Google Scholar 

  12. Dixon RA, Lamb CJ: Molecular communication in interactions between plants and microbial pathogens. Annu Rev Plant Physiol Plant Mol Biol 41: 339–367 (1990).

    Google Scholar 

  13. Eckey-Kaltenbach H, Ernst D, Heller W, Sandermann H: Biochemical plant responses to ozone. IV. Cross-induction of defensive pathways in parsley (Petroselinum crispum L.) plants. Plant Physiol 104: 67–74 (1994).

    Google Scholar 

  14. Eckey-Kaltenbach H, Großkopf E, Sandermann H, Ernst D: Induction of pathogen defence genes in parsley (Petroselinum crispum L.) plants by ozone. Proc Royal Soc Edinburgh 102B: 63–74 (1994).

    Google Scholar 

  15. Ernst D, Schraudner M, Langebartels C, Sandermann H: Ozone-induced changes of mRNA levels of β-1,3-glucanase, chitinase and ‘pathogenesis-related’ protein 1b in tobacco plants. Plant Mol Biol 20: 673–682 (1992).

    Google Scholar 

  16. Feinberg AP, Vogelstein B: A technique for radiolabeling DNA restriction endonuclease fragments to high specific activity. Anal Biochem 132: 6-13 (1983).

    Google Scholar 

  17. Galliano H, Cabané M, Eckerskorn C, Lottspeich F, Sandermann H, Ernst D: Molecular cloning, sequence analysis and elicitor-/ozone-induced accumulation of cinnamyl alcohol dehydrogenase from spruce (Picea abies L.). Plant Mol Biol 23: 145–156 (1993).

    Google Scholar 

  18. Gross P, Julius C, Schmelzer E, Hahlbrock K: Translocation of cytoplasm and nucleus to fungal penetration sites is associated with depolymerization of microtubules and defence gene activation in infected, cultured parsley cells. EMBO J 12: 1735–1744 (1993).

    Google Scholar 

  19. Gubler U, Hoffman BJ: A simple and very efficient method for generating cDNA libraries. Gene 25: 263–269 (1983).

    Google Scholar 

  20. Hahlbrock K, Scheel D: Physiology and molecular biology of phenylpropanoid metabolism. Annu Rev Plant Physiol Plant Mol Biol 40: 347–369 (1989).

    Google Scholar 

  21. Heath RL: The biochemistry of ozone attack on the plasma membrane of plant cells. Recent Adv Phytochem 21: 29–54 (1989).

    Google Scholar 

  22. Hernandez LD, Vierling E: Expression of low molecular weight heat-shock proteins under field conditions. Plant Physiol 101: 1209–1216 (1993).

    Google Scholar 

  23. Jacobson A: Purification and fractionation of poly(A)+ RNA. Meth Enzymol 152: 254–261 (1987).

    Google Scholar 

  24. Kangasjärvi J, Talvinen J, Utriainen M, Karjalainen R: Plant defence systems induced by ozone. Plant Cell Environ 17: 783–794 (1994).

    Google Scholar 

  25. Kärenlampi SO, Airaksinen K, Miettinen ATE, Kokko HI, Holopainen JK, Kärenlampi LV, Karjalainen, RO: Pathogenesis-related proteins in ozone-exposed Norway spruce [Picea abies (Karst) L.]. NewPhytol 126: 81–89 (1994).

    Google Scholar 

  26. Krishna P, Felsheim RF, Larkin JC, Das A: Structure and light-induced expression of a small heat-shock protein gene of Pharbitis nil. Plant Physiol 100: 1772–1779 (1992).

    Google Scholar 

  27. Kube A, Saji H, Tanaka K, Kondo N: Expression of Arabidopsis cytosolic ascorbate peroxidase in response to ozone or sulfur dioxide. Plant Mol Biol 29: 479–489 (1995).

    Google Scholar 

  28. Kuhn DN, Chappell J, Boudet A, Hahlbrock K: Induction of phenylalanine ammonia-lyase and 4-coumarate:CoA ligase mRNAs in cultured plant cells by UV light or fungal elicitor. Proc Natl Acad Sci USA 81: 1102–1106 (1984).

    Google Scholar 

  29. Langebartels C, Kerner K, Leonardi S, Schraudner M, Trost M, Heller W, Sandermann H: Biochemical plant responses to ozone. I. Differential induction of polyamine and ethylene biosynthesis in tobacco. Plant Physiol 95: 882–889 (1991).

    Google Scholar 

  30. Lindquist S, Craig EA: The heat-shock proteins. Annu Rev Genet 22: 631–677 (1988).

    Google Scholar 

  31. Moiseyev GP, Beintema JJ, Fedoreyeva LI, Yakovlev GI: High sequence similarity between a ribonuclease from ginseng calluses and fungus-elicited proteins from parsley indicates that intracellular pathogenesis-related proteins are ribonucleases. Planta 193: 470–472 (1994).

    Google Scholar 

  32. Morgan RW, Christman W, Jacobson FS, Storz G, Ames BN: Hydrogen peroxide-inducible proteins in Salmonella typhimurium overlap with heat shock and other stress proteins. Proc Natl Acad Sci USA 83: 8059–8063 (1986).

    Google Scholar 

  33. Powell R, Neilan J, Gannon F: Plaque dot assay. Nucl Acids Res 14: 1541 (1986).

    Google Scholar 

  34. Reddy GN, Arteca RN, Dai Y-R, Flores HE, Negm FB, Pell EJ: Changes in ethylene and polyamines in relation to mRNA levels of the large and small subunits of ribulose bisphosphate carboxylase/oxygenase in ozone-stressed potato foliage. Plant Cell Environ 16: 819–826 (1993).

    Google Scholar 

  35. Rosemann D, Heller W, Sandermann H: Biochemical plant responses to ozone. II. Induction of stilbene biosynthesis in Scots pine (Pinus sylvestris L.) seedlings. Plant Physiol 97: 1280–1286 (1991).

    Google Scholar 

  36. Sambrook J, Fritsch EF, Maniatis T: Molecular Cloning: A Laboratory Manual. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY (1989)

    Google Scholar 

  37. Sandermann H, Ernst D, Heller W, Langebartels C: Biochemical markers for stress detection and ecophysiology. In: Schulze ED, Mooney HA (eds) Design and Execution of Experiments on CO2 Enrichment, pp. 45–51, Ecosystem Research Report 6 of the Commission of the European Communities. Guyot, Brussels (1993).

  38. Sanger F, Nicklen S, Coulsen AR: DNA sequencing with chain-terminating inhibitors. Proc Natl Acad Sci USA 74: 5463–5467 (1977).

    Google Scholar 

  39. Schlagnhaufer CD, Glick RE, Arteca RN, Pell EJ: Molecular cloning of an ozone-induced 1-aminocyclopropane-1-carboxylate synthase cDNA and its relationship with loss of rbcS in poato (Solanum tuberosum L.) Plant Mol Biol 28: 93–103 (1995).

    Google Scholar 

  40. Schneiderbauer A, Back E, Sandermann H, Ernst D: Ozone induction of extensin mRNA in Scots pine, Norway spruce and European beech. New Phytol 130: 225–230 (1995).

    Google Scholar 

  41. Schraudner M, Ernst D, Langebartels C, Sandermann H: Biochemical plant responses to ozone. III. Activation of the defense-related proteins β-1,3-glucanase and chitinase in tobacco leaves. Plant Physiol 99: 1321–1328 (1992).

    Google Scholar 

  42. Schwacke R, Hager A: Fungal elicitors induce a transient release of active oxygen species from cultured spruce cells that is dependent on Ca2+ and protein-kinase activity. Planta 187: 136–141 (1992).

    Google Scholar 

  43. Sharma YK, Davis KR: Ozone-induced expression of stress-related genes in Arabidopsis thaliana. Plant Physiol 105: 1089–1096 (1994).

    Google Scholar 

  44. Sharma YK, Davis KR: Isolation of a novel Arabidopsis ozone-induced cDNA by differential display. Plant Mol Biol 29: 91–98 (1995).

    Google Scholar 

  45. Sharma YK, Léon J, Raskin L, Davis KR: Ozone-induced responses in Arabidopsis thaliana: the role of salicylic acid in the accumulation of defense-related transcripts and induced resistance. Proc Natl Acad Sci USA 93: 5099–5104 (1996).

    Google Scholar 

  46. Somssich IE, Schmelzer E, Bollmann J, Hahlbrock K: Rapid activation by fungal elicitor of genes encoding ‘pathogenesis-related’ proteins in cultured parsley cells. Proc Natl Acad Sci USA 83: 2472–2430 (1986).

    Google Scholar 

  47. Somssich IE, Schmelzer E, Kawalleck P, Hahlbrock K: Gene structure and in situ transcript localization of pathogenesis-related protein 1 in parsley. Mol Gen Genet 213: 93–98 (1988).

    Google Scholar 

  48. Somssich IE, Bollmann J, Hahlbrock K, Kombrink E, Schulz W: Differential early activation of defense-related genes in elicitor-treated parsley cells. Plant Mol Biol 12: 227–234 (1989).

    Google Scholar 

  49. Treshow M, Anderson FK: Plant Stress from Air Pollution. John Wiley, New York (1989).

    Google Scholar 

  50. Tuomainen J, Pellinen R, Roy S, Kiiskinen M, Eloranta T, Kadalainen R, Kangasjärvi J: Ozone affects birch (Betula pendula Roth) phenylpropanoid, polyamine and active oxygen detoxifying pathways at biochemical and gene expression level. J Plant Physiol 148: I79–188 (1996).

    Google Scholar 

  51. Van Berkel J, Salamini F, Gebhardt C: Transcripts accumulation during cold storage of potato (Solanum tuberosum L.) tubers are sequence related to stress-responsive genes. Plant Physiol 104: 445–452 (1994).

    Google Scholar 

  52. Van Loon LC, Pierpoint WS, Boller Th, Conejero V: Recommendations for naming plant pathogenesis-related proteins. Plant Mol Biol Rep 12: 245–264 (1994).

    Google Scholar 

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

    Google Scholar 

  54. Willekens H, Van Camp W, Van Montagu M, lnzé D, Langebartels C, Sandermann H: Ozone, sulfur dioxide, and ultraviolet B have similar effects on mRNA accumulation of antioxidant genes in Nicotiana plumbaginifolia (L.). Plant Physiol 106: 1007–1014 (1994).

    Google Scholar 

  55. Yalpani N, Enyedi AR, Léon J, Raskin I: Ultraviolet light and ozone stimulate accumulation of salicylic acid, pathogenesis-related proteins and virus resistance in tobacco. Planta 193: 372–376 (1994).

    Google Scholar 

  56. Zarsky V, Garrido D, Eller N, Tupy J, Vicente O, Schöffl F, Heberle-Bors E: The expression of a small heat shock gene is activated during induction of tobacco pollen embryogenesis by starvation. Plant Cell Environ 18: 139–147 (1995).

    Google Scholar 

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Eckey-Kaltenbach, H., Kiefer, E., Grosskopf, E. et al. Differential transcript induction of parsley pathogenesis-related proteins and of a small heat shock protein by ozone and heat shock. Plant Mol Biol 33, 343–350 (1997). https://doi.org/10.1023/A:1005786317975

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