Effects of Air Pollutants on Gene Expression in Plants

  • Akihiro Kubo


Air pollutants exert various effects on plants, which then show various responses to the pollutants (Alscher and Wellburn 1994; Yunus and Iqbal 1996). Among the effects and responses, those at the level of gene expression are rapidly becoming one of the best understood. For instance, several reviews on the effects of ozone (O3) on gene expression in plants (Kangasjärvi et al. 1994; Pell et al. 1994, 1997; Schraudner et al. 1996, 1997; Sandermann 1996; Sharma and Davis 1997) and one on the molecular effects of sulfur dioxide (SO2) in plants (Okpodu et al. 1996) have appeared. Overall, reports on this subject area relating to O3 outnumber those concerning other air pollutants. This chapter summarizes the effects of phytotoxic air pollutants on gene expression in higher plants, and discusses the application of this research field to environmental biotechnology.


Visible Injury Petroselinum Crispum Ozone Stress Acta Physiol Plant mRNA Degradation Rate 
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  1. Alscher RG, Wellburn AR (eds) (1994) Plant responses to the gaseous environment. Chapman & Hall, LondonGoogle Scholar
  2. Akkapeddi AS, Noormets A, Deo BK, et al (1999) Gene structure and expression of the aspen cytosolic copper/zinc-superoxide dismutase (PtSodCcl). Plant Sci 143: 151–162CrossRefGoogle Scholar
  3. Bahl A, Kahl G (1995) Air pollutant stress changes the steady-state transcript levels of three photosynthesis genes. Environ Pollut 88: 57–65PubMedCrossRefGoogle Scholar
  4. Bahl A, Loitsch SM, Kahl G (1995) Transcriptional activation of plant defence genes by short-term air pollutant stress. Environ Pollut 89: 221–227PubMedCrossRefGoogle Scholar
  5. Bauer S, Galliano H, Pfeiffer F, et al (1993) Isolation and characterization of a cDNA clone encoding a novel short-chain alcohol dehydrogenase from Norway spruce (Picea abies L. Karst). Plant Physiol 103: 1479–1480PubMedCrossRefGoogle Scholar
  6. Beuther E, Köster S, Loss P, et al (1988) Small RNAs originating from symptomless and damaged spruces (Picea spp.) I. Continuous observation of individual trees at three different locations in NRW. J Phytopathol 121: 289–302CrossRefGoogle Scholar
  7. Brendley BW, Pell EJ (1998) Ozone-induced changes in biosynthesis of Rubisco and associated compensation to stress in foliage of hybrid poplar. Tree Physiol 18: 81–90PubMedGoogle Scholar
  8. Brosché M, Strid Å (1999a) The mRNA-binding ribosomal protein S26 as a molecular marker in plants: molecular cloning, sequencing and differential gene expression during environmental stress. Biochim Biophys Acta 1445: 342–344PubMedGoogle Scholar
  9. Brosché M, Strid Å (1999b) Cloning, expression, and molecular characterization of a small pea gene family regulated by low levels of ultraviolet B radiation and other stresses. Plant Physiol 121: 479–487PubMedCrossRefGoogle Scholar
  10. Buschmann K, Etscheid M, Riesner D, et al (1998) Accumulation of a porin-like mRNA and a metallothionein-like mRNA in various clones of Norway spruce upon long-term treatment with ozone. Eur J For Pathol 28: 307–322CrossRefGoogle Scholar
  11. Chiron H, Drouet A, Lieutier F, et al (2000) Gene induction of stilbene biosynthesis in Scots pine in response to ozone treatment, wounding, and fungal infection. Plant Physiol 124: 865–872PubMedCrossRefGoogle Scholar
  12. Clayton H, Knight MR, Knight H, et al (1999) Dissection of the ozone-induced calcium signature. Plant J 17: 575–579PubMedCrossRefGoogle Scholar
  13. Conklin PL, Last RL (1995) Differential accumulation of antioxidant mRNAs in Arabidopsis thaliana exposed to ozone. Plant Physiol 109: 203–212PubMedCrossRefGoogle Scholar
  14. Dixon RA, Paiva NL (1995) Stress-induced phenylpropanoid metabolism. Plant Cell 7: 1085–1097PubMedCrossRefGoogle Scholar
  15. Eckardt NA, Pell EJ (1994) O3-induced degradation of Rubisco protein and loss of Rubisco mRNA in relation to leaf age in Solanum tuberosum L. New Phytol 127: 741–748CrossRefGoogle Scholar
  16. Eckey-Kaltenbach H, Ernst D, Heller W, et al (1994a) Biochemical plant responses to ozone IV. Cross-induction of defensive pathways in parsley (Petroselinum crispum L.) plants. Plant Physiol 104: 67–74PubMedGoogle Scholar
  17. Eckey-Kaltenbach H, Großkopf E, Sandermann H Jr, et al (1994b) Induction of pathogen defence genes in parsley (Petroselinum crispum L.) plants by ozone. Proc R Soc Edinburgh 102B: 63–74Google Scholar
  18. Eckey-Kaltenbach H, Kiefer E, Grosskopf E, et al (1997) Differential transcript induction of parsley pathogenesis-related proteins and of a small heat shock protein by ozone and heat shock. Plant Mol Biol 33: 343–350PubMedCrossRefGoogle Scholar
  19. Ernst D, Schraudner M, Langebartels C, et al (1992) Ozone-induced changes of mRNA levels of ß-1,3-glucanase, chitinase and ‘pathogenesis-related’ protein 1b in tobacco plants. Plant Mol Biol 20: 673–682PubMedCrossRefGoogle Scholar
  20. Ernst D, Bodemann A, Schmelzer E, et al (1996) ß-1,3-Glucanase mRNA is locally, but not systemically induced in Nicotiana tabacum L. cv. Bel W3 after ozone fumigation. J Plant Physiol 148: 215–221CrossRefGoogle Scholar
  21. Ernst D, Grimmig B, Heidenreich B, et al (1999) Ozone-induced genes: mechanisms and biotechnological applications. In: Smallwood MF, Calvert CM, Bowles DJ (eds) Plant responses to environmental stress. BIOS Scientific Publishers, Oxford, pp 33–41Google Scholar
  22. Etscheid M, Buschmann K, Köhler R, et al (1993) Differential screening in a cDNA-library from spruce for clones associated with forest decline reveals accumulation of ribulose- 1,5-bisphosphate carboxylase small subunit mRNA. J Phytopathol 137: 317–343CrossRefGoogle Scholar
  23. Etscheid M, Klümper S, Riesner D (1999) Accumulation of a metallothionein-like mRNA in Norway spruce under environmental stress. J Phytopathol 147: 207–213CrossRefGoogle Scholar
  24. Galliano H, Cabané M, Eckerskorn C, et al (1993) Molecular cloning, sequence analysis and elicitor-/ozone-induced accumulation of cinnamyl alcohol dehydrogenase from Norway spruce (Picea abies L.). Plant Mol Biol 23: 145–156PubMedCrossRefGoogle Scholar
  25. Glick RE, Schlagnhaufer CD, Arteca RN, et al (1995) Ozone-induced ethylene emission accelerates the loss of ribulose-1,5-bisphophate carboxylase/oxygenase and nuclear- encoded mRNAs in senescing potato leaves. Plant Physiol 109: 891–898PubMedGoogle Scholar
  26. Grimmig B, Schubert R, Fischer R, et al (1997) Ozone- and ethylene-induced regulation of a grapevine resveratrol synthase promoter in transgenic tobacco. Acta Physiol Plant 19: 467–474CrossRefGoogle Scholar
  27. Großkopf E, Wegener-Strake A, Sandermann H Jr, et al (1994) Ozone-induced metabolic changes in Scots pine: mRNA isolation and analysis of in vitro translated proteins. Can J For Res 24: 2030–2033CrossRefGoogle Scholar
  28. Hérouart D, Bowler C, Willekens H, et al (1993) Genetic engineering of oxidative stress resistance in higher plants. Philos Trans R Soc Lond B 342: 235–240Google Scholar
  29. Himelblau E, Mira H, Lin S-J, et al (1998) Identification of a functional homolog of the yeast copper homeostasis gent ATX1 from Arabidopsis. Plant Physiol 117: 1227–1234PubMedCrossRefGoogle Scholar
  30. Kangasjärvi J, Talvinen J, Utriainen M, et al (1994) Plant defence systems induced by ozone. Plant Cell Environ 17: 783–794CrossRefGoogle Scholar
  31. Karpinski S, Wingsle G, Karpinska B, et al (1992) Differential expression of CuZn- superoxide dismutases in Pinus sylvestris needles exposed to SO2 and NO2. Physiol Plant 85: 689–696CrossRefGoogle Scholar
  32. Kiiskinen M, Korhonen M, Kangasjärvi J (1997) Isolation and characterization of cDNA for a plant mitochondrial phosphate translocator (Mpt1): ozone stress induces Mpt1 mRNA accumulation in birch (Betula pendula Roth). Plant Mol Biol 35: 271–279PubMedCrossRefGoogle Scholar
  33. Kim K-Y, Huh G-H, Lee H-S, et al (1999) Molecular characterization of cDNAs for two anionic peroxidases from suspension cultures of sweet potato. Mol Gen Genet 261: 941–947PubMedCrossRefGoogle Scholar
  34. Kirtikara K, Talbot D (1996) Alteration in protein accumulation, gene expression and ascorbate-glutathione pathway in tomato (Lyeopersicon esculentum) under paraquat and ozone stress. J Plant Physiol 148: 752–760CrossRefGoogle Scholar
  35. Kliebenstein DJ, Monde R-A, Last RL (1998) Superoxide dismutase in Arabidopsis: an eclectic enzyme family with disparate regulation and protein localization. Plant Physiol 118: 637–650PubMedCrossRefGoogle Scholar
  36. Koch JR, Scherzer AJ, Eshita SM, et al (1998) Ozone sensitivity in hybrid poplar is correlated with a lack of defense-gene activation. Plant Physiol 118: 1243–1252CrossRefGoogle Scholar
  37. Köster S, Beuther E, Riesner D (1988) Small RNAs originating from symptomless and damaged spruces (Picea abies L., Karst.) II. Investigation of different trees from two differently exposed forest sections in the Hils area. J Phytopathol 121: 303–312CrossRefGoogle Scholar
  38. Kubo A, Saji H, Tanaka K, et al (1995) Expression of Arabidopsis cytosolic ascorbate peroxidase gene in response to ozone or sulfur dioxide. Plant Mol Biol 29: 479–489PubMedCrossRefGoogle Scholar
  39. Lee H, Jo J, Son D (1998) Molecular cloning and characterization of the gene encoding glutathione reductase in Brassica campestris. Biochim Biophys Acta 1395: 309–314PubMedGoogle Scholar
  40. Maccarrone M, Veldink GA, Vliegenthart JFG (1992) Thermal injury and ozone stress affect soybean lipoxygenases expression. FEBS Lett 309: 225–230PubMedCrossRefGoogle Scholar
  41. Maccarrone M, Veldink GA, Vliegenthart JFG, et al (1997) Ozone stress modulates amine oxidase and lipoxygenase expression in lentil (Lens culinaris) seedlings. FEBS Lett 408: 241–244PubMedCrossRefGoogle Scholar
  42. Madamanchi NR, Donahue JL, Cramer CL, et al (1994) Differential response of Cu,Zu superoxide dismutases in two pea cultivars during a short-term exposure to sulfur dioxide. Plant Mol Biol 26: 95–103PubMedCrossRefGoogle Scholar
  43. Miller JD, Arteca RN, Pell EJ (1999) Senescence-associated gene expression during ozone-induced leaf senescence in Arabidopsis. Plant Physiol 120: 1015–1023PubMedCrossRefGoogle Scholar
  44. No E-G, Flagler RB, Swize MA, et al (1997) cDNAs induced by ozone from Atriplex canescens (saltbush) and their response to sulfur dioxide and water-deficit. Physiol Plant 100: 137–146CrossRefGoogle Scholar
  45. Ohki T, Matsui H, Nagasaka A, et al (1999) Induction by ozone of ethylene production and an ACC oxidase cDNA in rice (Oryza sativa L.) leaves. Plant Growth Regul 28: 123–127CrossRefGoogle Scholar
  46. Okpodu CM, Alscher RG, Grabau EA, et al (1996) Physiological, biochemical and molecular effects of sulfur dioxide. J Plant Physiol 148: 309–316CrossRefGoogle Scholar
  47. Örvar BL, McPherson J, Ellis BE (1997) Pre-activating wounding response in tobacco prior to high-level ozone exposure prevents necrotic injury. Plant J 11: 203–212PubMedCrossRefGoogle Scholar
  48. Overmyer K, Tuominen H, Kettunen R, et al (2000) Ozone-sensitive Arabidopsis rcd1 mutant reveals opposite roles for ethylene and jasmonate signaling pathways in regulating superoxide-dependent cell death. Plant Cell 12: 1849–1862PubMedCrossRefGoogle Scholar
  49. Pääkkönen E, Seppänen S, Holopainen T, et al (1998) Induction of genes for the stress proteins PR-10 and PAL in relation to growth, visible injuries and stomatal conductance in birch (Betula pendula) clones exposed to ozone and/or drought. New Phytol 138: 295–305CrossRefGoogle Scholar
  50. Pell EJ, Eckardt NA, Glick RE (1994) Biochemical and molecular basis for impairment of photosynthetic potential. Photosynth Res 39: 453–462CrossRefGoogle Scholar
  51. Pell EJ, Schlagnhaufer CD, Arteca RN (1997) Ozone-induced oxidative stress: mechanisms of action and reaction. Physiol Plant 100: 264–273CrossRefGoogle Scholar
  52. Pino ME, Mudd JB, Bailey-Serres J (1995) Ozone-induced alterations in the accumulation of newly synthesized proteins in leaves of maize. Plant Physiol 108: 777–785PubMedGoogle Scholar
  53. Ramsay G (1998) DNA chips: state-of-the art. Nature Biotechnology 16: 40–44PubMedCrossRefGoogle Scholar
  54. Ranieri A, Tognini M, Tozzi C, et al (1997) Changes in the thylakoid protein pattern in sunflower plants as a result of ozone fumigation. J Plant Physiol 151: 227–234Google Scholar
  55. Rao MV, Davis KR (1999) Ozone-induced cell death occurs via two distinct mechanisms in Arabidopsis: the role of salicylic acid. Plant J 17: 603–614PubMedCrossRefGoogle Scholar
  56. Rao MV, Paliyath G, Ormrod DP (1995) Differential response of photosynthetic pigments, rubisco activity and rubisco protein of Arabidopsis thaliana exposed to UVB and ozone. Photochem Photobiol 62: 727–735CrossRefGoogle Scholar
  57. Rao MV, Lee H, Creelman RA, et al (2000) Jasmonic acid signaling modulates ozone-induced hypersensitive cell death. Plant Cell 12: 1633–1646PubMedCrossRefGoogle Scholar
  58. Reddy GN, Arteca RN, Dai Y-R, et al (1993) 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: 819–826CrossRefGoogle Scholar
  59. Richards KD, Schott EJ, Sharma YK, et al (1998) Aluminum induces oxidative stress genes in Arabidopsis thaliana. Plant Physiol 116: 409–418PubMedCrossRefGoogle Scholar
  60. Sandermann H Jr (1996) Ozone and plant health. Annu Rev Phytopathol 34: 347–366PubMedCrossRefGoogle Scholar
  61. Sandermann H Jr (2000) Ozone/biotic disease interactions: molecular biomarkers as a new experimental tool. Environ Pollut 108: 327–332PubMedCrossRefGoogle Scholar
  62. Sandermann H Jr, Ernst D, Heller W, et al (1998) Ozone: an abiotic elicitor of plant defence reactions. Trends Plant Sci 3: 47–50CrossRefGoogle Scholar
  63. Sävenstrand H, Brosché M, Ängehagen M, et al (2000) Molecular markers for ozone stress isolated by suppression subtractive hybridization: specificity of gene expression and identification of a novel stress-regulated gene. Plant Cell Environ 23: 689–700CrossRefGoogle Scholar
  64. Schlagnhaufer CD, Glick RE, Arteca RN, et al (1995) Molecular cloning of an ozone- induced 1-aminocyclopropane-l-carboxylate synthase cDNA and its relationship with a loss of rbcS in potato (Solanum tuberosum L.) plants. Plant Mol Biol 28: 93–103PubMedCrossRefGoogle Scholar
  65. Schlagnhaufer CD, Arteca RN, Pell EJ (1997) Sequential expression of two 1- aminocyclopropane-l-carboxylate synthase genes in response to biotic and abiotic stresses in potato (Solanum tuberosum L.) leaves. Plant Mol Biol 35: 683–688PubMedCrossRefGoogle Scholar
  66. Schmitt R, Sandermann H Jr (1990) Biochemical response of Norway spruce (Picea abies (L.) Karst.) towards 14-month exposure to ozone and acid mist: Part II—effects on protein biosynthesis. Environ Pollut 64: 367–373PubMedCrossRefGoogle Scholar
  67. Schneiderbauer A, Back E, Sandermann H Jr, et al (1995) Ozone induction of extension mRNA in Scots pine, Norway spruce and European beech. New Phytol 130: 225–230CrossRefGoogle Scholar
  68. Schraudner M, Ernst D, Langebartels C, et al (1992) Biochemical plant responses to ozone III. Activation of the defense-related proteins ß-1,3-glucanase and chitinase in tobacco leaves. Plant Physiol 99: 1321–1328PubMedCrossRefGoogle Scholar
  69. Schraudner M, Langebartels C, Sandermann H Jr (1996) Plant defence systems and ozone. Biochem Soc Trans 24: 456–461PubMedGoogle Scholar
  70. Schraudner M, Langebartels C, Sandermann H (1997) Changes in the biochemical status of plant cells induced by the environmental pollutant ozone. Physiol Plant 100: 274–280CrossRefGoogle Scholar
  71. Schraudner M, Moeder W, Wiese C, et al (1998) Ozone-induced oxidative burst in the ozone biomonitor plant, tobacco Bel W3. Plant J 16: 235–245CrossRefGoogle Scholar
  72. Schubert R, Fischer R, Hain R, et al (1997) An ozone-responsive region of the grapevine resveratrol synthase promoter differs from the basal pathogen-responsive sequence. Plant Mol Biol 34: 417–426PubMedCrossRefGoogle Scholar
  73. Sharma YK, Davis KR (1994) Ozone-induced expression of stress-related genes in Arabidopsis thaliana. Plant Physiol 105: 1089–1096PubMedGoogle Scholar
  74. Sharma YK, Davis KR (1995) Isolation of a novel Arabidopsis ozone-induced cDNA by differential display. Plant Mol Biol 29: 91–98PubMedCrossRefGoogle Scholar
  75. Sharma YK, Davis KR (1997) The effects of ozone on antioxidant responses in plants. Free Radical Biol Med 23: 480–488CrossRefGoogle Scholar
  76. Sharma YK, León J, Raskin I, et al (1996) 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: 5099–5104PubMedCrossRefGoogle Scholar
  77. Solecka D (1997) Role of phenylpropanoid compounds in plant responses to defferent stress factors. Acta Physiol Plant 19: 257–268CrossRefGoogle Scholar
  78. Torsethaugen G, Pitcher LH, Zilinskas BA, et al (1997) Overproduction of ascorbate peroxidase in the tobacco chloroplast does not provide protection against ozone. Plant Physiol 114: 529–537PubMedGoogle Scholar
  79. Tuomainen J, Pellinen R, Roy S, et al (1996). Ozone affects birch (Betula pendula Roth) phenylpropanoid, polyamine and active oxygen detoxifying pathways at biochemical and gene expression level. J Plant Physiol 148: 179–188CrossRefGoogle Scholar
  80. Tuomainen J, Betz C, Kangasjarvi J, et al (1997) Ozone induction of ethylene emission in tomato plants: regulation by differential accumulation of transcripts for the biosynthetic enzymes. Plant J 12: 1151–1162CrossRefGoogle Scholar
  81. Vahala J, Schlagnhaufer CD, Pell EJ (1998) Induction of an ACC synthase cDNA by ozone in light-grown Arabidopsis thaliana leaves. Physiol Plant 103: 45–50CrossRefGoogle Scholar
  82. Van Breusegem F, Slooten L, Stassart J-M, et al (1999) Overproduction of Arabidopsis thaliana FeSOD confers oxidative stress tolerance to transgenic maize. Plant Cell Physiol 40: 515–523PubMedGoogle Scholar
  83. Wegener A, Gimbel W, Werner T, et al (1997a) Molecular cloning of ozone-inducible protein from Pinus sylvestris L. with high sequence similarity to vertebrate 3-hydroxy-3- methylglutaryl-CoA-synthase. Biochim Biophys Acta 1350: 247–252PubMedGoogle Scholar
  84. Wegener A, Gimbel W, Werner T, et al (1997b) Sequence analysis and ozone-induced accumulation of polyubiquitin mRNA in Pinus sylvestris. Can J For Res 27: 945–948CrossRefGoogle Scholar
  85. Wiese CB, Pell EJ (1997) Influence of ozone on transgenic tobacco plants expressing reduced quantities of Rubisco. Plant Cell Environ 20: 1283–1291CrossRefGoogle Scholar
  86. Willekens H, Van Camp W, Van Montagu M, et al (1994) Ozone, sulfur dioxide, and ultraviolet B have similar effects on mRNA accumulation of antioxidant genes in Nicotiana plumbaginifolia L. Plant Physiol 106: 1007–1014PubMedGoogle Scholar
  87. Yunus M, Iqbal M (eds) (1996) Plant response to air pollution. Wiley, ChichesterGoogle Scholar
  88. Zinser C, Ernst D, Sandermann H Jr (1998) Induction of stilbene synthase and cinnamyl alcohol dehydrogenase mRNAs in Scots pine (Pinus sylvestris L.) seedlings. Planta 204: 169–176CrossRefGoogle Scholar

Copyright information

© Springer -Verlag Tokyo 2002

Authors and Affiliations

  • Akihiro Kubo
    • 1
  1. 1.Environmental Biology DivisionNational Institute for Environmental StudiesTsukuba, IbarakiJapan

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