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Expression of tobacco class II catalase gene activates the endogenous homologous gene and is associated with disease resistance in transgenic potato plants

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Abstract

We have previously shown that healthy potato plants respond poorly to salicylic acid (SA) for activating disease resistance against the late blight fungal pathogen Phytophthora infestans. However, SA is essential for the establishment of potato systemic acquired resistance (SAR) against P. infestans after treatment with the fungal elicitor arachidonic acid (AA). To understand the molecular mechanisms through which AA induces SA-dependent SAR in potato, we have recently studied the expression of potato class II catalase (Cat2St) in comparison with its tobacco homologue, Cat2Nt, which has previously been shown to bind SA. In the present study, we show that tobacco Cat2Nt is expressed at high levels and accounts for almost half of total SA-binding activity detected in tobacco leaves. In contrast, potato Cat2St is not expressed in healthy leaves, which is associated with the low SA responsiveness of potato plants for activation of disease resistance mechanisms. Upon treatment with AA, expression of potato Cat2St is induced not only in AA-treated leaves, but also in the upper untreated parts of the plants, concomitant with the establishment of SA -dependent SAR to P. infestans. Moreover, expression of the tobacco Cat2Nt gene in transgenic potato plants leads to constitutive expression of the endogenous potato Cat2St gene and is associated with enhanced resistance to P. infestans. These results collectively indicate that plant SA-binding class II catalases may play an important role in the development of disease resistance, possibly by serving as biological targets of SA.

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References

  1. An G: Development of plant promoter expression vectors and their use for analysis of differential activity of nopaline synthase promoters in transformed tobacco cells. Plant Physiol 81: 86–91(1986).

    Google Scholar 

  2. Anderson MD, Chen Z, Klessig DF: Possible involvement of lipid peroxidation in SA-mediated induction of PR-1 gene expression. Phytochemistry 47: 555–566(1998).

    Google Scholar 

  3. Bi Y-M, Kenton P, Mur L, Darby R, Draper J: Hydrogen peroxide does not function downstream of salicylic acid in the induction of PR protein expression. Plant J 8: 235–245(1995).

    Article  PubMed  Google Scholar 

  4. Bilha B, Kadish D, Levy Y. Cohen Y: Infectivity to potato, sporangial germination, and respiration of isolates of Phytophthora infestans from metalaxy-sensitive and metalaxyresistant populations. Phytopathology 79: 823–836( 1989).

    Google Scholar 

  5. Bradley DJ, Kjellbom P, Lamb C: Elicitor-and woundinduced oxidative cross-linking of a proline-rich plant cell wall protein: a novel, rapid defense response. Cell 70: 21–30 (1992).

    Google Scholar 

  6. Burnett WV: Northern blotting of RNA denatured in glyoxal without buffer recirculation. BioTechniques 22: 668–671 (1997).

    PubMed  Google Scholar 

  7. Cao H, Glazebrook J, Clarke JD, Volko S, Dong X: The Arabidopsis NPR 1 gene that controls systemic acquired resistance encodes a novel protein containing ankyrin repeats. Cell 88: 57–63(1997).

    PubMed  Google Scholar 

  8. Chamnongpol S, Willekens H, Langebartels C, Van Montagu M, Inzé D, Van Camp W: Transgenic tobacco with a reduced catalase activity develop necrotic lesions and have constitutive pathogenesis-related gene expression under high light. Plant J 10: 491–503(1996).

    Google Scholar 

  9. Chen Z, Klessig DF: Identification of a soluble salicylic acidbinding protein that may function in the signal transduction in the plant disease resistance response. Proc Natl Acad Sci USA 88: 8179–8183(1991).

    PubMed  Google Scholar 

  10. Chen Z, Lyer S, Caplan A, Klessig DF, Fan B: Differential accumulation of salicylic acid and salicylic acid-sensitive catalase in different rice tissues. Plant Physiol 114: 193–201 (1997).

    PubMed  Google Scholar 

  11. Chen Z, Ricigliano JW, Klessig DF: Purification and characterization of a soluble salicylic acid-binding protein from tobacco. Proc Natl Acad Sci USA 90: 9533–9537(1993).

    PubMed  Google Scholar 

  12. Chen Z, Silva H, Klessig DF: Active oxygen species in the induction of plant systemic acquired resistance by salicylic acid. Science 262: 1883–1886(1993).

    PubMed  Google Scholar 

  13. Conrath U, Chen Z, Ricigliano JW, Klessig DF: Two inducers of plant defence responses, 2,6-dichloroisonicotinic acid and salicylic acid, inhibit catalase activity in tobacco. Proc Natl Acad Sci USA 92: 7143–7147(1995).

    PubMed  Google Scholar 

  14. Coquoz JL, Buchala AJ, Meuwly PH, Metraix JP: Arachidonic acid induces local but not systemic synthesis of salicylic acid and confers systemic resistance to potato plants to Phytophthora infestans and Alternaria solani. Phytopathology 85: 1219–1224(1995).

    Google Scholar 

  15. Dellaporta SL, Wood J, Hicks JB: A plant DNA minipreparation: version II. Plant Mol Biol Rep 1: 19–21(1983).

    Google Scholar 

  16. Drory A, Woodson WR: Molecular cloning and nucleotide sequence of a cDNA encoding catalase from tomato. Plant Physiol 100: 1605–1606(1992).

    Google Scholar 

  17. Du H, Klessig DF: Identification of a soluble, high affinity salicylic acid-binding protein in tobacco. Plant Physiol 113: 1319–1327(1997).

    PubMed  Google Scholar 

  18. Durner J, Klessig DF: Inhibition of ascorbate peroxidase by salicylic acid and 2,6-dichloroisonicotinic acid, two inducers of plant defense responses. Proc Natl Acad Sci USA 92: 11312–11316(1995).

    PubMed  Google Scholar 

  19. Durner J, Klessig DF: Salicylic acid is a modulator of tobacco and mammalian catalases. J Biol Chem 27: 28492–28501 (1996).

    Google Scholar 

  20. Enyedi A, Yalpani N, Silverman P, Rasin I: Localization, conjugation and function of salicylic acid in tobacco during the hypersensitive reaction to tobacco mosaic virus. Proc Natl Acad Sci USA 89: 2480–2484(1992).

    Google Scholar 

  21. Faith M, Merten A, Hahn M, Jeblick W, Kaiss H: Competence for elicitation of H2O2 in hypocotyls of cucumer is induced by breaching the cuticle and is enhanced by salicylic acid. Plant Physiol 110: 347–354(1996).

    PubMed  Google Scholar 

  22. Halliwell B, Gutteridge JMC: Free Radicals in Biology and Medicine. Oxford University Press, Oxford, UK (1989).

    Google Scholar 

  23. Kaiss H, Jeblick W: Pretreatment of parsley suspension cultures with salicylic acid enhances spontaneous and elicited production of H2O2. Plant Physiol 108: 1171–1178(1995).

    PubMed  Google Scholar 

  24. Kaiss H, Jeblick W: Influence of salicylic acid on the induction of competence for H2O2 elicitation. Plant Physiol 111: 755–763(1996).

    PubMed  Google Scholar 

  25. Kawano T, Sahashi N, Takahashi K, Uozumi N, Muto S: Salicylic acid induces extracellular superoxide generation followed by an increase in cytosolic calcium ion in tobacco suspension culture: the earliest events in salicylic acid signal transduction. Plant Cell Physiol 39: 721–730(1998).

    Google Scholar 

  26. Leon J, Lawton MA, Raskin I: Hydrogen peroxide stimulates salicylic acid biosynthesis in tobacco. Plant Physiol 108: 1673–1678( 1995).

    PubMed  Google Scholar 

  27. Levine A, Tenhaken R, Dixon R, Lamb C: H2O2 from the oxidative burst orchestrates the plant hypersensitive disease resistance response. Cell 79: 583–593(1994).

    Article  PubMed  Google Scholar 

  28. Liu D., Raghothama KG, Hasegawa P, Bressan RA: Osmotin overexpression in potato delays development of disease symptoms. Proc Natl Acad Sci USA 91: 1881–1892(1994).

    Google Scholar 

  29. Logemann J, Schell J, Willmitzer L: Improved method for the isolation of RNA from plant tissues. Anal Biochem 163: 16–20 (1987).

    PubMed  Google Scholar 

  30. Malamy J, Carr J.P, Klessig DF, Raskin I: Salicylic acid: a likely endogenous signal in the resistance response of tobacco to viral infection. Science 250: 1002–1004(1990).

    Google Scholar 

  31. Malamy J, Hennig J, Klessig DF: Temperature-dependent induction of salicylic acid and its conjugates during the resistance response to tobacco mosaic virus infection. Plant Cell 4: 359–366(1992).

    Google Scholar 

  32. Metraix JP, Signer H, Ryals JA, Ward E, Wyss-Benz M, Gaidin J, Raschdorf K, Schmid E, Blum W, Inveradi B: Increase in salicylic acid at the onset of systemic acquired resistance in cucumber. Science 250: 1004–1006(1990).

    Google Scholar 

  33. Mur LA, Naylor G, Warner SAJ, Sugars JM, White RF, Draper J: Salicylic acid potentiates defense gene expression in leaf tissue exhibiting acquired resistance to pathogen attack. Plant J 9: 559–571(1996).

    Google Scholar 

  34. Neuenschwander U., Vernooij B., Friedrich L., Uknes S., Kessmann H, Ryals J: Is hydrogen peroxide a second messenger of salicylic acid in systemic acquired resistance. Plant J 8: 227–233(1995).

    Article  Google Scholar 

  35. Niebel A., Heungens K., Barthels N., Inzé D., Van Montagu M, Gheysen G: Characterization of a pathogen-induced potato catalase and its systemic expression upon nematode and bacterial infection. Mol Plant-Microbe Interact 8: 371–378 (1995).

    PubMed  Google Scholar 

  36. Raskin I, Skubatz H, Tang W, Meeuse BJD: Salicylic acid levels in thermogenic and nonthermogenic plants. Ann Bot 66: 369–373(1990).

    Google Scholar 

  37. Rasmussen JB, Hammerschmidt R, Zook MN: Systemic induction of salicylic acid accumulation in cucumber after inoculation with Psedomonas syringae pv. syringae. Plant Physiol 97: 1342–1347(1991).

    Google Scholar 

  38. Ruffer M, Steipe B, Zenk MH: Evidence against specific binding of salicylic acid to plant catalase. FEBS Lett 377: 175–180 (1995).

    PubMed  Google Scholar 

  39. Ryals JA, Neuenschwander UH, Willits MG, Molina A, Steiner HY, Hunt MD: Systemic acquired resistance. Plant Cell 8: 1809–1819(1996).

    Article  PubMed  Google Scholar 

  40. Ryals J, Weymann K, Lawton K, Friedrich L, Ellis D, Steiner HY, Johnson J, Delaney TP, Jesse T, Vos P, Uknes S: The Arabidopsis thaliana NIM1 protein shows homology to the mammalian transcription factor inhibitor IκB. Plant Cell 9: 425–439(1997).

    PubMed  Google Scholar 

  41. Shah J., Tsui F, Klessig DF: Characterization of a salicylic acid-insensitive mutant (sai1) of Arabidopsis thaliana identi-fied in a selective screening utilizing the SA-inducible expression of the tms2 gene. Mol Plant-Microbe Interact 10: 69–76 (1997).

    PubMed  Google Scholar 

  42. Shirasu K, Nakajima H, Rajasekhar VY, Dixon RA, Lamb C: Salicylic acid potentiates an agonist-dependent gain control that amplifies pathogen signals in the activation of defense mechanisms. Plant Cell 9: 261–270(1996).

    Google Scholar 

  43. Takahashi H, Chen Z, Du H, Liu Y, Klessig D.F: Development of necrosis and activation of disease resistance in transgenic tobacco plants with severely reduced catalase levels. Plant J 11: 993–1005(1997).

    PubMed  Google Scholar 

  44. Timmermans MCP, Maliga P, Veira J, Messing, J: The pFF plasmids: cassettes utilising CaMV sequences for expression of foreign genes in plants. J Biotechnol 14: 333–344(1990).

    PubMed  Google Scholar 

  45. Tooley PW, Swelgard JA, Fry WE: Fitness and virulence of Phytophthora infestans isolates from sexual and asexual populations. Phytopathology 76: 1209–1212(1980).

    Google Scholar 

  46. Uknes S, Winter A, Delaney T, Vernooij B, Morse A, Friedrich L, Potter S, Slusarenko A, Ward E, Ryals J: Biological in duction of systemic acquired resistance in Arabidopsis. Mol Plant-Microbe Interact 6: 680–685(1993).

    PubMed  Google Scholar 

  47. Vernooij B, Friedrich L, Morse A, Reist R, Koldttz-Jawhar R, Ward E, Uknes S, Kessmann H, Ryals J: Salicylic acid is not the translocated signal responsible for inducing systemic acquired resistance but is required in signal transduction. Plant Cell 6: 959–969(1994).

    Article  PubMed  Google Scholar 

  48. Wendehenne D, Durner J, Chen Z, Klessig DF: Benzothiadiazole, an inducer of plant defenses, inhibits catalases and ascorbate peroxidase. Phytochemistry 47: 651–657(1998).

    Google Scholar 

  49. Wenzler HC, Mignery G, May G, Park WD: A rapid and efficient transformation method for the production of large numbers of transgenic potato plants. Plant Sci 63: 79–85 (1989).

    Article  Google Scholar 

  50. Weyman K, Hunt M, Uknes S, Neuenschwander U, Lawton K, Steiner H, Ryals J: Suppression and restoration of lesion formation in Arabidopsis Isd mutants. Plant Cell 7: 2013–2022 (1995).

    PubMed  Google Scholar 

  51. Willekens H, Villarroel, Van Camp W, Van Montagu M, Inzé D: Molecular identification of catalases from Nicotinana plumbaginfolia (L). FEBS Lett 352: 79–83(1994).

    PubMed  Google Scholar 

  52. Willekens H, Langebartels C, Tire C, Van Montagu M, Inzé D, Van Camp W: Differential expression of catalase genes in Nicotinana plumbagiifolia. Proc Natl Acad Sci USA 91: 10450–10454(1994).

    Google Scholar 

  53. Wu G, Shortt BJ, Lawrence EB, Levine EB, Fitzsimmons KC, Shah DM: Disease resistance conferred by expression of a gene encoding H2O2-generating glucose oxidase in transgenic potato plants. Plant Cell 7: 1357–1368(1995).

    PubMed  Google Scholar 

  54. Yu D, Liu Fan B, Klessig DF, Chen Z: Is the high basal level of salicylic acid important for disease resistance in potato? Plant Physiol 115: 343–349(1997).

    PubMed  Google Scholar 

  55. Zhu B, Chen THH, Li PH: Analysis of late-blight disease resistance and freezing tolerance in transgenic potato plants expressing sense and antisense genes for an osmotin-like protein. Planta 198: 70–77(1996).

    PubMed  Google Scholar 

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Authors and Affiliations

  1. Department of Microbiology, Molecular Biology and Biochemistry, University of Idaho, Moscow, ID, 83844-3052, USA

    Diqiu Yu, Zhixin Xie, Chunhong Chen, Baofang Fan & Zhixiang Chen

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  1. Diqiu Yu
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Yu, D., Xie, Z., Chen, C. et al. Expression of tobacco class II catalase gene activates the endogenous homologous gene and is associated with disease resistance in transgenic potato plants. Plant Mol Biol 39, 477–488 (1999). https://doi.org/10.1023/A:1006180708533

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