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Environmental Science and Pollution Research

, Volume 22, Issue 9, pp 6535–6545 | Cite as

Temporal dynamics of the cellular events in tobacco leaves exposed in São Paulo, Brazil, indicate oxidative stress by ozone

  • Andrea Nunes Vaz PedrosoEmail author
  • Edenise Segala Alves
Research Article

Abstract

Nicotiana tabacum ‘Bel-W3’ is widely used as an ozone bioindicator species, showing typical necrosis preceded by microscopic markers of oxidative stress. This study aimed to follow the development of symptoms in tobacco exposed in São Paulo highlighting the temporal dynamics of the cellular events. Leaves with and without necrosis were processed according to standard techniques for anatomical analyses. Leaves from the site with higher SUM00 presented thinner palisade parenchyma, fewer layers of spongy parenchyma, higher stomatal density, clusters of vessel elements in the midrib, erosion of cuticular waxes and stomatal damage. The sequence of microscopic events from the third day of exposure were condensation of the cytoplasm in parenchyma tissue, sinuosity of anticlinal walls, pectinaceous cell wall protrusions, chromatin condensation and changes in chlorophyll autofluorescence. On the 14th day of exposure, these events finally led to cell death in the palisade parenchyma and necrosis on the leaf. The markers observed indicated oxidative stress caused by ozone.

Keywords

Oxidative stress Ozone Tobacco ‘Bel-W3’ 

Notes

Acknowledgments

The authors are grateful to the Post-Graduation Program of the Instituto de Botânica, Coordenação de Aperfeiçoamento de Pessoal de Nível Superior (CAPES) for the scholarship of A.N.V. Pedroso and Fundação de Amparo à Pesquisa do Estado de São Paulo (FAPESP) (Grant 05/51169-9) for the financial support. E.S. Alves also thank the Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq) for the support (Grants 304617/2012-1). Thanks also to S. Sant‘Anna in providing raw data of necrosis (experiment I).

References

  1. Adams T, Lintilhac M (1993) Fluorescence microscopy of fresh tissue as a rapid technique for assessing early injury to mesophyll. Biotech Histochem 68:3–7CrossRefGoogle Scholar
  2. Alves ES (1995) The effects of the pollution on wood of Cecropia glazioui (Cecropiaceae). IAWA J 16:69–80CrossRefGoogle Scholar
  3. Alves ES, Giusti PM, Domingos M, Saldiva PHN, Guimarães ET, Lobo DJA (2001) Estudo anatômico foliar do clone híbrido 4430 de Tradescantia: alterações decorrentes da poluição aérea urbana. Braz J Bot 24:567–576CrossRefGoogle Scholar
  4. Alves ES, Tresmondi F, Longui EL (2008) Análise estrutural de folhas de Eugenia uniflora L. (Myrtaceae) coletadas em ambientes rural e urbano, SP, Brasil. Acta Bot Bras 22:241–248CrossRefGoogle Scholar
  5. Alves ES, Moura BB, Pedroso ANV, Tresmondi F, Domingos M (2011) The efficiency of tobacco Bel-W3 and native species for ozone biomonitoring in subtropical climate, as revealed by histo-cytochemical techniques. Environ Pollut 159:3309–3315CrossRefGoogle Scholar
  6. Ashmore MR (2005) Assessing the future global impacts of ozone on vegetation. Plant Cell Environ 28:949–964CrossRefGoogle Scholar
  7. Baas P, Ewers FW, Davis SD, Wheeler EA (2004) Evolution of xylem physiology. In: Hewsley AR, Poole I (eds) The evolution of plant physiology. Elsevier, London, pp 273–295CrossRefGoogle Scholar
  8. Bray EA, Bailey-Serres J, Weretilnyk E (2000) Responses to abiotic stresses. In: Buchanan BB, Gruissen W, Jones RL (eds) Biochemistry & molecular biology of plants. American Society of Plant Physiologists, New York, pp 1158–1203Google Scholar
  9. Bussotti F, Agati G, Desotgiu R, Matteini P, Tani C (2005) Ozone foliar symptoms in woody plant species assessed with ultrastructural and fluorescence analysis. New Phytol 166:941–955CrossRefGoogle Scholar
  10. Calatayud V, Sanz MJ, Calvo E, Cerveró J, Ansel W, Klumpp A (2007) Ozone biomonitoring with Bel-W3 tobacco plants in the city of Valencia (Spain). Water Air Soil Pollut 283–291Google Scholar
  11. Cetesb (2011) Relatório de qualidade do ar do Estado de São Paulo de 2012. Companhia de Tecnologia de Saneamento Ambiental, Série Relatórios, São Paulo http://www.cetesb.sp.gov.br/ar/qualidade-do-ar/31-publicacoes-e-relatorios
  12. Dias APL, Dafré M, Rinaldi MCS, Domingos M (2011) How the redox state of tobacco ‘Bel-W3’ is modified in response to ozone and other environmental factors in a sub-tropical area? Environ Pollut 159:458–465CrossRefGoogle Scholar
  13. Esposito MP, Ferreira ML, Sant’Anna SMR, Domingos M, Souza SR (2009) Relationship between leaf antioxidants and ozone injury in Nicotiana tabacum ‘Bel-W3’ under environmental conditions in São Paulo, SE—Brazil. Atmos Environ 43:619–623CrossRefGoogle Scholar
  14. Evans LS, Adamski JH II, Renfro JR (1996) Relationships between cellular injury, visible injury of leaves, and ozone exposure levels for several dicotyledonous plant species at Great Smoky Mountains National Park. Environ Exp Bot 36:229–237CrossRefGoogle Scholar
  15. Faoro F, Iriti M (2009) Plant cell death and cellular alterations induced by ozone: key studies in Mediterranean conditions. Environ Pollut 157:1470–1477CrossRefGoogle Scholar
  16. Ferdinand JA, Fredericksen TS, Kouterick KB, Skelly JM (2000) Leaf morphology and ozone sensitivity of two open pollinated genotypes of black cherry (Prunus serotina) seedlings. Environ Pollut 108:297–302CrossRefGoogle Scholar
  17. Fink S (1999) Pathological and regenerative plant anatomy. Gebrüder Borntraeger Berlin, StuttgarttGoogle Scholar
  18. Fuhrer J (2009) Ozone risk for crops and pastures in present and future climates. Naturwissenschaften 96:173–194CrossRefGoogle Scholar
  19. Fujino T, Itoh T (1998) Changes in pectin structure during epidermal cell elongation in pea (Pisum sativum) and its implications for cell wall architecture. Plant Cell Physiol 39:1315–1323CrossRefGoogle Scholar
  20. Gerosa G, Marzuoli R, Bussotti F, Pancrazi M, Ballarin-Denti A (2003) Ozone sensitivity of Fagus sylvatica and Fraxinus excelsior young trees in relation to leaf structure and foliar ozone uptake. Environ Pollut 125:91–98CrossRefGoogle Scholar
  21. Giacomo B, Forino LMC, Tagliasacchi AM, Bernardi R, Durante M (2010) Ozone damage and tolerance in leaves of two poplar genotypes. Caryologia 63:422–434CrossRefGoogle Scholar
  22. Gostin IN (2009) Air pollution effects on the leaf structure of some Fabaceae species. Not Bot Hortic Agrobot Cluj 37:57–63Google Scholar
  23. Gravano E, Giulietti V, Desotgiu R, Bussotti F, Grossoni P, Gerosa G, Tani C (2003) Foliar response of an Ailanthus altissima clone in two sites with different levels of ozone pollution. Environ Pollut 121:137–146CrossRefGoogle Scholar
  24. Gravano E, Bussotti F, Strasser RJ, Schaub M, Novak K, Skelly J, Tani C (2004) Ozone symptoms in leaves of woody plants in open-top chambers: ultrastructural and physiological characteristics. Physiol Plant 121:620–633CrossRefGoogle Scholar
  25. Grulke NE, Neufeld HS, Davison AW, Roberts M, Chappelka AH (2007) Stomatal behavior of ozone-sensitive and -insensitive coneflowers (Rudbeckia laciniata var. Digitata) in Great Smoky Mountains National Park. New Phytol 173:100–109CrossRefGoogle Scholar
  26. Guidi L, Mali C, Ciompi S, Lorenzini G, Soldatini GF (1997) The use of chlorophyll fluorescence and leaf gas exchange as methods for studying the different responses to ozone of two bean cultivars. J Exp Bot 48:173–179CrossRefGoogle Scholar
  27. Günthardt-Goerg MS, Vollenweider P (2007) Linking stress with macroscopic and microscopic leaf response in trees: new diagnostic perspectives. Environ Pollut 147:467–488CrossRefGoogle Scholar
  28. Günthardt-Goerg MS, McQuattie CJ, Scheidegger C, Rhiner C, Matyssek R (1997) Ozone-induced cytochemical and ultrastructural changes in leaf mesophyll cell walls. Can J For Res 27:453.463Google Scholar
  29. Heath MC (1994) Possible mechanisms for the inhibition of photosynthesis by ozone. Photosynth Res 39:439–451CrossRefGoogle Scholar
  30. Heggestad HE (1991) Origin of Bel-W3, Bel-C and Bel-B tobacco varieties and their use as indicators of ozone. Environ Pollut 74:264–291CrossRefGoogle Scholar
  31. Hollaway MJ, Arnold SR, Challinor AJ, Emberson LD (2012) Intercontinental trans-boundary contributions to ozone-induced crop yield losses in the Northern Hemisphere. Biogeosciences 9:271–292CrossRefGoogle Scholar
  32. Karnosky DF, Skelly JM, Percy KE, Chappelka AH (2007) Perspectives regarding 50 years of research on effects of tropospheric ozone air pollution on US forests. Environ Pollut 147:489–506CrossRefGoogle Scholar
  33. Klumpp A, Ansel W, Klumpp G, Vergne P, Sifakis N, Sanz MJ, Rasmussen S, RoPoulsen H, Ribas A, Peñuelas J, Kambezidis H, He S, Garrec JP, Calatayud V (2006) Ozone pollution and ozone biomonitoring in European cities Part II. Ozone-induced plant injury and its relationship with descriptors of ozone pollution. Atmos Environ 40:7437–7448CrossRefGoogle Scholar
  34. Kraus JE, Arduin M (1997) Manual básico de métodos em morfologia vegetal. Editora da Universidade Rural do Rio de. Janeiro, Rio de JaneiroGoogle Scholar
  35. Krupa S, McGrath MT, Andersen CP, Booker FL, Burkey KO, Chappelka AH, Chevone BI, Pell EJ, Zilinskas BA (2001) Ambient ozone and plant health. Plant Dis 85:4–12CrossRefGoogle Scholar
  36. Lake JA, Quick WP, Beerling DJ, Woodward EL (2001) Signals from mature to new leaves. Nature 411:154CrossRefGoogle Scholar
  37. Lawson T, Craigon J, Black CR, Colls JJ, Landon G, Weyers JDB (2002) Impact of elevated CO2 and O3 on gas exchange parameters and epidermal characteristics in potato (Solanum tuberosum L.). J Exp Bot 53:737–746CrossRefGoogle Scholar
  38. Loreto F, Mannozzi M, Maris C, Nascetti P, Ferranti F, Pasqualini S (2001) Ozone quenching properties of isoprene and its antioxidant role in leaves. Plant Physiol 126:993–1000CrossRefGoogle Scholar
  39. Masuch G, Franz JT, Kicinski HG, Kettrup A (1992) Histological and biochemical differences of slightly and severely injured spruce needles of two stands in Northrhine Westphalia. Environ Exp Bot 32:163–182CrossRefGoogle Scholar
  40. Mittler R (2002) Oxidative stress, antioxidants and stress tolerance. Trends Plant Sci 7:405–410CrossRefGoogle Scholar
  41. Miyazawa SI, Livingston NJ, Turpin DH (2006) Stomatal development in new leaves is related to the stomatal conductance of mature leaves in poplar (Populus trichocarpa x P. deltoides). J Exp Bot 57:373–380CrossRefGoogle Scholar
  42. Moura BB, Souza SR, Alves ES (2011) Structural responses of Ipomoea nil (L.) Roth ‘Scarlet O’Hara’ (Convolvulaceae) exposed to ozone. Acta Bot Bras 25:122–129Google Scholar
  43. Moura BB, Souza SR, Alves ES (2014) Response of Brazilian native trees to acute ozone dose. Environ Sci Pollut Res 21:4220–4227CrossRefGoogle Scholar
  44. O’Brien TP, McCully ME (1965) Polychromatic staining of plant cell walls by toluidine blue. Protoplasma 59:368–373CrossRefGoogle Scholar
  45. Oksanen E, Sober J, Karnosky DF (2001) Impacts of elevated CO2 and/or O3 on leaf ultrastructure of aspen (Populus tremuloides) and birch (Betula papyrifera) in the Aspen FACE experiment. Environ Pollut 115:437–446CrossRefGoogle Scholar
  46. Orlando JP, Alvim DS, Yamazaki A, Corrêa SM, Gatti LV (2010) Ozone precursors for the São Paulo metropolitan area. Sci Total Environ 408:1612–1620CrossRefGoogle Scholar
  47. Pääkkönen E, Metsärinne S, Holopainen T, Kärenlampi L (1995) The ozone sensitivity of birch (Betula pendula) in relation to the developmental stage of leaves. New Phytol 132:145–154CrossRefGoogle Scholar
  48. Pääkkönen E, Holopainen T, Kärenlampi L (1997) Differences in growth, leaf senescence and injure, and stomatal density in birch (Betula pendula Roth) in relation to ambient levels of ozone in Finland. Environ Pollut 96:117–127CrossRefGoogle Scholar
  49. Paoletti E (2006) Impact of ozone on Mediterranean forests: a review. Environ Pollut 144:463–474CrossRefGoogle Scholar
  50. Paoletti E, Contran N, Bernasconi P, Günthardt-Goerg M, Vollenweider P (2009) Structural and physiological responses to ozone in Manna ash (Fraxinus ornus L.) leaves of seedlings and mature trees under controlled and ambient conditions. Sci Total Environ 407:1631–1643CrossRefGoogle Scholar
  51. Pasqualini S, Piccioni C, Reale L, Ederli L, Torre GD, Ferranti F (2003) Ozone induced cell death in tobacco cultivar Bel W3 plants. The role of programmed cell death in lesion formation. Plant Physiol 133:1122–1134CrossRefGoogle Scholar
  52. Pedroso ANV, Alves ES (2008) Anatomia foliar comparativa das cultivares de Nicotiana tabacum L. (Solanaceae) sensível e tolerante ao ozônio. Acta Bot Bras 22:21–28CrossRefGoogle Scholar
  53. Pell EJ, Schlagnhaufer CD, Arteca RN (1997) Ozone-induced oxidative stress: mechanisms of action and reaction. Physiol Plant 100:264–273CrossRefGoogle Scholar
  54. Rashidi F, Jalili A, Kafaki SB, Sagheb-Talebi K, Hodgson J (2012) Anatomical responses of leaves of Black Locust (Robinia pseudoacacia L.) to urban pollutant gases and climatic factors. Trees 26:363–375CrossRefGoogle Scholar
  55. Reig-Armiñana J, Calatayud V, Cerveró J, Garcia-Breijo FJ, Ibars A, Sanz MJ (2004) Effects of ozone on the foliar histology of the mastic plant (Pistacia lentiscus L.). Environ Pollut 132:321–331CrossRefGoogle Scholar
  56. Resende MLV, Salgado SML, Chaves ZM (2003) Espécies ativas de oxigênio na resposta de defesa de plantas a patógenos. Fitopatol Bras 28:123–130CrossRefGoogle Scholar
  57. Richter HG (1981) Anatomia des sekundaren xylems und der Rinde der Lauraceae. Sonderbande des Naturn. Vereins Hamburg 5. Paul Parey, Hamburg.Google Scholar
  58. Riikonen J, Percy KE, Kivimäenpää M, Kubiske ME, Nelson ND, Vapaavuori E, Karnosky DF (2010) Leaf size and surface characteristics of Betula papyrifera exposed to elevated CO2 and O3. Environ Pollut 158:1029–1035CrossRefGoogle Scholar
  59. Sant’Anna SMR, Esposito MP, Domingos M, Souza SR (2008) Suitability of Nicotiana tabacum ‘Bel W3’ for biomonitoring ozone in São Paulo, Brazil. Environ Pollut 151:389–394CrossRefGoogle Scholar
  60. Shephred T, Griffiths SW (2006) The effects of stress on plant cuticular waxes. New Phytol 171:469–499CrossRefGoogle Scholar
  61. Soda C, Bussotti F, Grossoni P, Barnes J, Mori B, Tani C (2000) Impacts of urban levels of ozone on Pinus halepensis foliage. Environ Exp Bot 44:69–82CrossRefGoogle Scholar
  62. Strittmatter CGD (1973) Nueva tecnica de diafanizacion. Bol Soc Argent Bot 15:126–129Google Scholar
  63. Tresmondi T, Alves ES (2011) Structural changes in Psidium guajava ‘Paluma’ leaves exposed to tropospheric ozone. Acta Bot Bras 25:542–548CrossRefGoogle Scholar
  64. Uhl D, Mosbrugger (1999) Leaf venation density as a climate and environmental proxy: a critical review and new data. Palaeogeogr Palaeoclimatol Palaeoecol 149:15–26CrossRefGoogle Scholar
  65. Ullah K, Wahid A, Ahmad SS, Shamsi SRA (2012) Ozone biomonitoring in Pakistan using tobacco cultivar Bel-W3. Pak J Bot 44:717–723Google Scholar
  66. VDI - Verein Deutscher Ingenieure (2003) Biological measuring techniques for the determination and evaluation of effects of air pollutants on plants (bioindication). Determination and evaluation of the phytotoxic effects of photooxidants. Method of the standardized tobacco exposure. VDI 3957/6. VDI/DIN Handbuch Reinhaltung der Luft, Vol. 1a, Beuth, Berlin.Google Scholar
  67. Vergé X, Chapuis A, Delpoux M (2002) Bioindicator reliability: the example of Bel W3 tobacco (Nicotiana tabacum L.). Environ Pollut 85:337–349CrossRefGoogle Scholar
  68. Vollenweider P, Ottiger M, Günthardt-Goerg MS (2003) Validation of leaf ozone symptoms in natural vegetation using microscopical methods. Environ Pollut 124:101–118CrossRefGoogle Scholar
  69. Vollenweider P, Fenn ME, Menard T, Günthardt-Goerg M, Bytnerowicz A (2013) Structural injury underlying mottling in ponderosa pine needles exposed to ambient ozone concentrations in the San Bernardino mountains near Los Angeles, California. Trees 27:895–911CrossRefGoogle Scholar
  70. Zimmermann MH (1983) Xylem structure and ascent sap. Springer - Verlag, Berlin, Heidelberg New York,Tokyo.Google Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2015

Authors and Affiliations

  • Andrea Nunes Vaz Pedroso
    • 1
    Email author
  • Edenise Segala Alves
    • 1
  1. 1.Instituto de Botânica, Núcleo de Pesquisa em AnatomiaSão PauloBrazil

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