biologia plantarum

International journal on Plant Life established by Bohumil Nìmec in 1959

Biologia plantarum 57:514-524, 2013 | DOI: 10.1007/s10535-013-0315-3

Cell death induced by ozone stress in the leaves of Populus deltoides × maximowiczii

G. Bartoli1,*, L. M. C. Forino1, A. M. Tagliasacchi1, M. Durante2
1 Department of Biology, University of Pisa, Pisa, Italy
2 Department of Agriculture, Food and Environment, University of Pisa, Pisa, Italy

When exposed to an acute ozone stress, cell death occurred in leaves of the O3 sensitive Populus deltoides × maximowiczii clone Eridano. After treatment (5 h fumigation and 24 h recovery), the damaged areas covered more than 50 % of the leaf surface. At cellular level, these lesions were preceded by some apoptotic hallmarks and by biochemical and physiological alterations evoked by the apoplastic O3 dissociation. The cell death pattern was highly localized and involved an increase of membrane permeability, externalization of phosphatidylserine, DNA fragmentation, callose accumulation, polyphenol production, and a biphasic oxidative burst accompanied by NO overproduction. These results indicate a process of programmed cell death that could have the biological significance of limiting the spreading the oxidative burst triggered by ozone dissociation in apoplastic environment. Moreover, materials derived from cell dismantling could be remobilized toward developing structures which can conclude their ontogenetic program after the stress.

Keywords: hypersensitive response; phosphatidylserine; oxidative burst; nitric oxide; TUNEL assay; DNA-laddering assay; DNA smear
Subjects: cell death; ozone; hypersensitive reaction; oxidative burst; nitric oxide; TUNEL assay; DNA-laddering; DNA smear; leaf injury; hydrogen peroxide; poplar

Received: July 31, 2012; Accepted: January 9, 2013; Published: September 1, 2013  Show citation

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Bartoli, G., Forino, L.M.C., Tagliasacchi, A.M., & Durante, M. (2013). Cell death induced by ozone stress in the leaves of Populus deltoides × maximowiczii. Biologia plantarum, 57(3), 514-524. doi: 10.1007/s10535-013-0315-3
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    References

    1. Ahlfors, R., Brosché, M., Kangasjärvi, J.: Ozone and nitric oxide interaction in Arabidopsis thaliana. A role for ethylene? - Plant Signal. Behavior 4: 878-879, 2009a. Go to original source...
    2. Ahlfors, R., Brosché, M., Kollist, H., Kangasjärvi, J.: Nitric oxide modulates ozone-induced cell death, hormone biosynthesis and gene expression in Arabidopsis thaliana. - Plant J. 58: 1-12, 2009b. Go to original source...
    3. Bartoli, G., Forino, L.M.C., Tagliasacchi, A.M., Bernardi, R., Durante, M.: Ozone damage and tolerance in leaves of two poplar genotypes. - Caryologia 63: 422-434, 2010. Go to original source...
    4. Bartoli, G., Forino, L.M.C., Tagliasacchi, A.M., Bernardi, R., Durante, M.: Ozone induces a HR-like response in the O3 - sensitive Populus deltoides × maximowiczii Eridano clone. - In: Proceedings of the 1st Annual Congress of Italian Society of Plant Biollogy. Pp. 52. SIBV, Verona 2009.
    5. Bernardi, R., Nali, C., Ginestri, P., Pugliesi, C., Lorenzini, G., Durante, M.: Antioxidant enzyme isoforms on gels in two poplar clones differing in sensitivity after exposure to ozone. - Biol. Plant. 48: 41-48, 2004. Go to original source...
    6. Bethke, P.C., Lonsdale, J.E., Fath, A., Jones, R.L.: Hormonally regulated programmed cell death in barley aleurone cells. - Plant Cell 11: 1033-1045, 1999. Go to original source...
    7. Bird, A.P., Southern, E.M.: Use of restriction enzymes to study eukaryotic DNA methylation: I The methylation pattern in ribosomal DNA from Xenopus. - J. mol. Biol. 118: 27-47, 1978. Go to original source...
    8. Cohen, G.M., Sun, X., Fearnhead, H., Macfarlane, M., Brown, D.J., Snowden, R.T., Dinsdale, D.: Formation of large molecular weight fragments of DNA is a key committed step of apoptosis in thymocytes. - J. Immunol. 153: 507-16, 1994. Go to original source...
    9. Delledonne, M., Zeier, J., Marocco, A., Lamb, C.: Signal interactions between nitric oxide and reactive oxygen intermediates in the plant hypersensitive disease resistance response. - Proc. nat. Acad. Sci. USA 98: 13454-13459, 2001. Go to original source...
    10. De Pinto, M.C., Tommasi, F., De Gara, L.: Changes in the antioxidant systems as part of the signalling pathway responsible for the programmed cell death activated by nitric oxide and reactive oxygen species in tobacco BY-2 cells. - Plant Physiol. 130: 698-708, 2002. Go to original source...
    11. Dizengremel, P., Le Thiec, D., Hasenfratz-Sauder, M.P., Vaultier, M.N., Bagard, M., Jolivet, Y.: Metabolicdependent changes in plant cell redox power after ozone exposure. - Plant Biol. 11: 35-42, 2009. Go to original source...
    12. Diara, C., Castagna, A., Baldan, B., Mensuali Sodi, A., Sahr, T., Langebartels, C., Sebastiani, L., Ranieri, A.: Differences in the kinetics and scale of signaling molecule production modulate the ozone sensitivity of hybrid poplar clones: the roles of H2O2, ethylene and salicylic acid. - New Phytol. 168: 351-364, 2005. Go to original source...
    13. Di Baccio, D., Castagna, A., Paoletti, E., Sebastiani, L., Ranieri, A.: Could the differences in O3 sensitivity between two poplar clones be related to a difference in antioxidant defence and secondary metabolic response to O3 influx? - Tree Physiol. 28: 1761-1772, 2008. Go to original source...
    14. Di Baccio, D., Ederli, L., Marabottini, R., Badiani, M., Francini, A., Nali, C., Antonelli, M., Santangelo, E., Sebastiani, L., Pasqualini, S.: Similar foliar lesions but opposite hormonal patterns in a tomato mutant impaired in ethylene perception and its near isogenic wild type challenged with ozone. - Environ. exp. Bot. 75: 286-297, 2012. Go to original source...
    15. Doyle, J.J., Doyle, J.L.: Isolation of plant DNA from fresh tissue. - Focus 12: 13-15, 1990.
    16. Draper, J.: Salicylate, superoxide synthesis and cell suicide in plant defence. - Trends Plant Sci. 2: 162-165, 1997. Go to original source...
    17. Durante, M., Geri, C., Bonatti, S., Parenti, R.: Non-random alkylation of DNA sequences induced in vivo by chemical mutagens. - Carcinogenesis 10: 1357-1361, 1989. Go to original source...
    18. Fan, T., Xing, T.: Heat shock induces programmed cell death in wheat lesions. - Biol. Plant. 48: 389-394, 2004. Go to original source...
    19. Faoro, F., Iriti, M.: Cell death behind invisible symptoms: early diagnosis of ozone injury. - Biol. Plant. 49: 585-592, 2005. Go to original source...
    20. Faoro, F., Iriti M.: Plant cell death and cellular alterations induced by ozone: key studies in Mediterranean conditions. - Environ. Pollut. 157: 1470-1477, 2009. Go to original source...
    21. Fincher, G.B., Stone, B.A.: Metabolism of noncellulosic polysaccharides. - In: Loewus, F.A. (ed.): Encyclopedia of Plant Phisyology, New Series. Vol. 13. Pp. 68-132. Springer-Verlag, Berlin 1981. Go to original source...
    22. Fiscus, E.L., Booker, F.L., Burkey, K.O.: Crop responses to ozone: uptake, modes of action, carbon assimilation and partitioning. - Plant Cell Environ. 28: 997-1011, 2005. Go to original source...
    23. Gadjev, I., Stone, J.M., Gechev, T.S.: Programmed cell death in plants: new insights into redox regulation and the role of hydrogen peroxide. - Int. Rev. cell. mol. Biol. 270: 87-144, 2008. Go to original source...
    24. Garces, H., Durzan, D., Pedroso, M.C.: Mechanical stress elicits nitric oxide formation and DNA fragmentation in Arabidopsis thaliana. - Ann. Bot. 87: 567-574, 2001. Go to original source...
    25. Gechev, T.S., Van Breusegem, F., Stone, J.M., Denev, I., Laloi, C.: Reactive oxygen species as signals that modulate plant stress responses and programmed cell death. - Bioassays 28: 1091-1101, 2006. Go to original source...
    26. Gilchrist, D.G.: Programmed cell death in plant disease: the purpose and promise of cellular suicide. - Annu. Rev. Phytopathol. 36: 393-414, 1998. Go to original source...
    27. Gravano, E., Giulietti, V., Desotgiu, R., Bussotti, F., Grossoni, P., Gerosa, G., Tani, C.: Foliar response of an Ailanthus altissima clone in two sites with different levels of ozonepollution. - Environ. Pollut. 121: 137-146, 2003. Go to original source...
    28. Greenberg, J.T.: Programmed cell death: a way of life for plants. - Proc. nat. Acad. Sci. USA 93: 12094-12097, 1996. Go to original source...
    29. Gunawardena, A., Greenwood, J.S., Dengler, N.: Programmed cell death remodels lace plant leaf shape during development. - Plant Cell 16: 60-73, 2004. Go to original source...
    30. Günthardt-Goerg, M.S., Vollenweider, P.: Linking stress with macroscopic and microscopic leaf response in trees: new diagnostic perspectives. - Environ. Pollut. 147: 467-488, 2007. Go to original source...
    31. Guo, J., Li, X.F., Qi, D.M., Chen, S.Y., Li, Z.Q., Nijs, I., Li, Y.G., Liu, G.S.: Effects of ozone on wild type and transgenic tobacco. - Biol. Plant. 53: 670-676, 2009. Go to original source...
    32. Havel, L., Durzan, D.J.: Apoptosis in plants. - Bot. Acta 109: 268-277, 1996. Go to original source...
    33. Havel, L., Durzan, D.J.: Programmed cell death in plants development. - In: Strnad, M., Peè, P., Beck, E. (ed.): Advances in Regulation of Plant Growth and Development. Pp 203-212. Peres, Prague 1999.
    34. Heath, R.L.: Modification of the biochemical pathways of plants induced by ozone: what are the varied routes to change? - Environ. Pollut. 155: 453-463, 2008. Go to original source...
    35. Jensen W.A. (ed): Botanical Histochemistry. - W. Freeman & Co., San Francisco 1962.
    36. Kangasjärvi, J., Jaspers, P., Kollist, H.: Signalling and cell death in ozone exposed plants. - Plant Cell Environ. 28: 1021-1036, 2005. Go to original source...
    37. Koch, J.R., Creelman, R.A., Eshita, S.M., Seskar, M., Mullet, J.E., Davis, K.R.: Ozone sensitivity in hybrid poplar correlates with insensitivity to both salicylic acid and jasmonic acid. the role of programmed cell death in lesion formation. - Plant Physiol. 123: 487-496, 2000. Go to original source...
    38. Ko³odziejek, I., Kozio³-Lipiñska, J., Wa³eza, M., Korczyñski, J., Mostowska, A.: Aspects of programmed cell death during early senescence of barley leaves: possible role of nitric oxide. - Protoplasma 232: 97-108, 2007. Go to original source...
    39. Laloi, C., Apel, K., Danon, A.: Reactive oxygen signalling: the latest news. - Curr. Opin. Plant Biol. 7: 323-328, 2004. Go to original source...
    40. Lam, E.: Controlled cell death, plant survival and development. - Nat. Rev. mol. cell. Biol. 5: 305-315, 2004. Go to original source...
    41. Lamb, C., Dixon, R. A.: The oxidative burst in plant disease resistance. - Annu. Rev. Plant Physiol. Plant mol. Biol. 48: 251-275, 1997. Go to original source...
    42. Lenochová, Z., Soukup, A., Votrubová, O.: Aerenchyma formation in maize roots. - Biol. Plant. 53: 263-270, 2009. Go to original source...
    43. Lei, M., Podell, E.R., Baumann, P., Cech, T.R.: DNA self-recognition in the structure of Pot1 bound to telomeric single-stranded DNA. - Nature 426:198-203, 2003. Go to original source...
    44. Ljubeŝiæ, N., Britvec, M.: Tropospheric ozone-induced structural changes in leaf mesophyll cell walls in grapevine plants. - Biologia 61: 85-90, 2006.
    45. Lombardi, L., Ceccarelli, N., Picciarelli, P., Lorenzi, R.: DNA degradation during programmed cell death of Phaseolus coccineus. - Plant Physiol. Biochem. 45: 221-227, 2007. Go to original source...
    46. Mahalingam, R., Shah, N., Scrymgeour, A., Fedorof, N.: Temporal evolution of the Arabidopsis oxidative stress response. - Plant Mol. Biol. 57: 709-730, 2005. Go to original source...
    47. Mittler, R., Lam, E.: Pathogen-induced programmed cell death in tobacco. - Plant mol. Biol. 34: 209-221, 1997. Go to original source...
    48. Moldau, H., Padu, E., Bichele, I.: Quantification of ozone decay and requirement for ascorbate in Phaseolus vulgaris L. mesophyll cell walls. - Phyton 37: 175-180, 1997.
    49. Nali, C., Guidi, L., Filippi, F., Soldatini, G.F., Lorenzini, G.: Photosynthesis of two poplar clones contrasting in O3 sensitivity. - Trees 12: 196-200, 1998. Go to original source...
    50. Neill, S.J., Desikan, R., Clarke, A., Hurst, R.D., Hancock, J.T.: Hydrogen peroxide and nitric oxide as signalling molecules in plants. - J. exp. Bot. 53: 1237-1247, 2002. Go to original source...
    51. Nikula, S., Percy, K., Oksanen, E., Holopainen, T., Manninen, S.: Effects of elevated ozone on growth and foliar traits of European and hybrid aspen. - Boreal Environ. Res. 14: 29-47, 2009.
    52. O'Brien, T., Mc Cully, M.E. (ed.): The Study of Plant Structure. Principles and Selected Methods. - Termacarphi, Melbourne 1981.
    53. O'Brien, I.E.W., Reutelingsperger, C.P., Holdaway, K.M.: The use of Annexin V and TUNEL to monitor the progression of apoptosis in plants. - Cytometry 29: 28-33, 1997. Go to original source...
    54. O'Brien, I.E.W., Baguley, B.C., Murray B.G., Morris B.A.M., Ferguson I.B.: Early stages of the apoptotic pathway in plant cells are reversible. - Plant J. 13: 803-814, 1998. Go to original source...
    55. Overmyer, K., Brosché, M., Pellinen, R., Kuittinen, T., Tuominen, H., Ahlfors, R., Keinänen, M., Saarma, M., Scheel, D., Kangasjärvi, J.: Ozone-induced programmed cell death in the Arabidopsis radical-induced cell death 1 mutant. - Plant Physiol. 137: 1092-1104, 2005. Go to original source...
    56. Pääkkönen, E., Holopainen, T., Karenlampi H.: Variation in ozone sensitivity among clones of Betula pendula and Betula pubescens. - Environ. Pollut. 95: 37-44, 1997. Go to original source...
    57. Pachauri, R.K., Reisinger, A. (ed): Climate Change 2007: Synthesis Report. Contribution of Working Groups I, II and III to the Fourth Assessment Report of the Intergovernmental Panel on Climate Change. - IPCC, Geneva 2007.
    58. Paolacci, A.R., D'Ovidio, R., Marabottini, R., Nali, C., Lorenzini, G., Abenavoli, M.R., Badiani, M.: Ozone induces a differential accumulation of phenyalanine ammonia-lyase, chalcone synthase and chalcone isomerase RNA transcripts in sensitive and resistant bean cultivars. - Aust. J. Plant Physiol. 28: 425-428, 2001. Go to original source...
    59. Pasqualini, S., Piccioni, C., Reale, L., Ederli, L., Della Torre, G., Ferranti, F.: Ozone-induced cell death in tobacco cultivar Bel W3 plants. The role of programmed cell death in lesion formation. - Plant Physiol. 133: 1122-1134, 2003. Go to original source...
    60. Pedroso, M.C., Magalhaes, J.R., Durzan, D.J.: A nitric oxide burst precedes apoptosis in angiosperm and gymnosperm foliar tissues. - J. exp. Bot. 51: 1027-1036, 2000. Go to original source...
    61. Pennell, R.I., Lamb C.: Programmed cell death in plants. - Plant Cell 9:1157-1168, 1997. Go to original source...
    62. Qiao, W., Fan, L.M.: Nitric oxide signalling in plant responses to abiotic stresses. - J. integr. Plant Biol. 50: 1238-1246, 2008. Go to original source...
    63. Richet, N., Afif, D., Tozo, K., Pollet, B., Maillard, P., Huber, F., Priault, P., Banvoy, J., Gross, P., Dizengremel, P., Lapierre, C., Perré, P., Cabané, M.: Elevated CO2 and/or ozone modify lignification in the wood of poplars (Populus tremula × alba). - J. exp. Bot. 63: 4291-4301, 2012. Go to original source...
    64. Rizzo, M., Bernardi, R., Salvini, M., Nali, C., Lorenzini, G., Durante, M.: Identification of differentially expressed genes induced by ozone stress in sensitive and tolerant poplar hybrids. - J. Plant Physiol. 164: 945-949, 2007. Go to original source...
    65. Schraudner, M., Moeder, W., Wiese, C., Van Camp, W., Inzè, D., Langebartels, C., Sandermann, H. Jr.: Ozone-induced oxidative burst in the ozone biomonitor plant, tobacco Bel W3. - Plant J. 16: 235-245, 1998. Go to original source...
    66. Singer, J., Roberts-Ems, J., Riggs, A.D.: Methylation of mouse liver DNA studied by means of the restriction enzymes msp I and hpa II. - Science 203: 1019-1021, 1979. Go to original source...
    67. Strohm, M., Eiblmeier, M., Langebartels, C., Jouanin, L., Polle, A., Sandermann, H., Rennenberg, H.: Responses of transgenic poplar (Populus tremula × P. alba) overexpressing glutathione synthetase or glutathione reductase to acute ozone stress: visible injury and leaf gas exchange. - J. exp. Bot. 50: 365-374, 1999. Go to original source...
    68. Tamaoki, M.: The role of phytohormone signaling in ozoneinduced cell death in plants. - Plant Signal. Behavior 3: 166-174, 2008. Go to original source...
    69. Taylor, G.: Populus: Arabidopsis for forestry. Do we need a model tree? - Ann. Bot. 90: 681-689, 2002. Go to original source...
    70. Vingarzan, R.: A review of surface O3 background levels and trends. - Atmos. Environ. 38: 3431-3442, 2004. Go to original source...
    71. Vollenweider, P., Ottiger, M., Günthardt-Goerg, M.S.: Validation of leaf ozone symptoms in natural vegetation using microscopical methods. - Environ. Pollut. 124: 101-118, 2003. Go to original source...
    72. Wang, Y., Lin, J.S., Wang, G.X.: Role of calcium in nitric oxide-induced programmed cell death in tobacco protoplasts. - Biol. Plant. 54: 471-476, 2010. Go to original source...
    73. Wohlgemuth, H., Mittelstrass, K., Kschieschan, S., Bender, J., Weigel, H.J., Overmyer, K., Kangasjärvi, J., Sandermann, H., Langebartels, C.: Activation of an oxidative burst is a general feature of sensitive plants exposed to the air pollutant ozone. - Plant Cell Environ. 25: 717-726, 2002. Go to original source...
    74. Xie, Q.E., Liu, I.D., Yu, S.X., Wang, R.F., Fan, Z.X., Wang, Y.G., Shen, F.F.: Detection of DNA ladder during cotyledon senescence in cotton. - Biol. Plant. 52: 654-659, 2008. Go to original source...
    75. Xu, C.J., Chen, K.S., Ferguson, I.B.: Programmed cell death feature in apple suspension cells under low oxygen culture. - J. Zhejiang Univ. Sci. 5: 137-143, 2004. Go to original source...
    76. Xu, P., Roossinck, M. J.: Cucumber mosaic virus D satellite RNA-induced programmed cell death in tomato. - Plant Cell 12:1079-92, 2000. Go to original source...

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