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Journal of Chemical Ecology

, Volume 36, Issue 1, pp 22–34 | Cite as

Plant Volatile Organic Compounds (VOCs) in Ozone (O3) Polluted Atmospheres: The Ecological Effects

  • Delia M. Pinto
  • James D. Blande
  • Silvia R. Souza
  • Anne-Marja Nerg
  • Jarmo K. Holopainen
Review Article

Abstract

Tropospheric ozone (O3) is an important secondary air pollutant formed as a result of photochemical reactions between primary pollutants, such as nitrogen oxides (NOx), and volatile organic compounds (VOCs). O3 concentrations in the lower atmosphere (troposphere) are predicted to continue increasing as a result of anthropogenic activity, which will impact strongly on wild and cultivated plants. O3 affects photosynthesis and induces the development of visible foliar injuries, which are the result of genetically controlled programmed cell death. It also activates many plant defense responses, including the emission of phytogenic VOCs. Plant emitted VOCs play a role in many eco-physiological functions. Besides protecting the plant from abiotic stresses (high temperatures and oxidative stress) and biotic stressors (competing plants, micro- and macroorganisms), they drive multitrophic interactions between plants, herbivores and their natural enemies e.g., predators and parasitoids as well as interactions between plants (plant-to-plant communication). In addition, VOCs have an important role in atmospheric chemistry. They are O3 precursors, but at the same time are readily oxidized by O3, thus resulting in a series of new compounds that include secondary organic aerosols (SOAs). Here, we review the effects of O3 on plants and their VOC emissions. We also review the state of current knowledge on the effects of ozone on ecological interactions based on VOC signaling, and propose further research directions.

Keywords

Ozone Volatile organic compounds Trophic interactions Infochemicals 

Notes

Acknowledgements

We thank Prof. Elina Oksanen and two anonymous reviewers for critical review and valuable comments on this review. The authors acknowledge the financial support of the Academy of Finland decisions number 128404 (J.D.B), 111543 and 105209 (J.K.H.), the Finnish Graduate School in Environmental Science and Technology (EnSTe), the Rikala Foundation (Rikalan puutarhasäätiö) (D.M.P) and Fundação do Amparo à Pesquisa do Estado de São Paulo (FAPESP) (Processes 08/03208-3) (S.R.S).

References

  1. Agrell, J., Kopper, B., McDonald, E. P., and Lindroth, R. L. 2005. CO2 and O3 effects on host plant preferences of the forest tent caterpillar (Malacosoma disstria). Glob. Change Biol. 11:588–599.CrossRefGoogle Scholar
  2. Arimura, G., Ozawa, R., Shimoda, T., Nishioka, T., Boland, W., and Takabayashi, J. 2000. Herbivory-induced volatiles elicit defense genes in lima bean leaves. Nature 406:512–515.PubMedCrossRefGoogle Scholar
  3. Arimura, G., Ozawa, R., Horiuchi, J., Nishioka, T., and Takabayashi, J. 2001. Plant–plant interactions mediated by volatiles emitted from plants infested by spider mites. Biochem. System. Ecol. 29:1049–1061.CrossRefGoogle Scholar
  4. Arimura, G., Kost, C., and Boland, W. 2005. Herbivore-induced, indirect plant defenses. Biochim. Biophys. Acta 1734:91–111.PubMedGoogle Scholar
  5. Arimura, G., Köpke, S., Kunert, M., Volpe, V., David, A., Brand, P., Dabrowska, P., Maffei, M. E., and Boland, W. 2008. Effect of feeding Spodoptera littoralis on Lima Beaan leaves: IV. Diurnal and nocturnal damage differentially initiate plant volatile emissions. Plant Physiol. 146:965–973.PubMedCrossRefGoogle Scholar
  6. Aschmann, S. M., Arey, J., and Atkinson, R. 2002. OH radical formation from the gas-phase reactions of O3 with a series of terpenes. Atmos. Environ. 36:4347–4355.CrossRefGoogle Scholar
  7. Ashmore, M. R. 2005. Assessing the future global impacts of ozone on vegetation. Plant Cell Environ. 28:949–964.CrossRefGoogle Scholar
  8. Atkinson, R., and Arey, J. 2003. Gas-phase tropospheric chemistry of biogenic volatile organic compounds: a review. Atmos. Environ. 37:S197–S219.CrossRefGoogle Scholar
  9. Awmack, C. S., Harrington, R., and Lindroth, R. L. 2004. Aphid individual performance may not predict population responses to elevated CO2 or O3. Glob. Change Biol. 10:1414–1423.CrossRefGoogle Scholar
  10. Baier, M., Kandlbinder, A., Golldack, D., and Dietz, K.-J. 2005. Oxidative stress and ozone: perception, signalling and response. Plant Cell Environ. 28:1012–1020.CrossRefGoogle Scholar
  11. Baird, C. and Michael, C. 2005. Environmental Chemistry, 3rd edn, p. 650. Freeman, New YorkGoogle Scholar
  12. Baldwin, I. T. and Schultz, J. C. 1983. Rapid changes in tree leaf chemistry induced by damage—evidence for communication between plants. Science 221:277–279.PubMedCrossRefGoogle Scholar
  13. Baldwin, I. T., Kessler, A., and Halitschke, R. 2002. Volatile signaling in plant–plant–herbivore interactions: what is real? Curr. Op. Plant Biol. 5:351–354.CrossRefGoogle Scholar
  14. Beauchamp, J., Wisthaler, A., Hansel, A., Kleist, E., Miebach, M., Niinemets, U., Schurr, U., and Wildt, J. 2005. Ozone induced emissions of biogenic VOC from tobacco: relationships between ozone uptake and emission of LOX products. Plant Cell Environ. 28:1334–1343.CrossRefGoogle Scholar
  15. Black, V. J., Stewart, C. A., Roberts, J. A., and Black, C. R. 2007. Ozone affects gas exchange, growth and reproductive development in Brassica campestris (Wisconsin Fast Plants). New Phytol. 176:150–163.PubMedCrossRefGoogle Scholar
  16. Blande, J. D., Tiiva, P., Oksanen, E., and Holopainen, J. K. 2007. Emission of herbivore-induced volatile terpenoids from two hybrid aspen (Populus tremula × tremuloides) clones under ambient and elevated ozone concentrations in the field. Glob. Change Biol. 13:2538–2550.CrossRefGoogle Scholar
  17. Bonn, B. and Moortgat, G. K. 2003. Sesquiterpene ozonolysis: origin of atmospheric new particle formation from biogenic hydrocarbons. Geophys. Res. Lett. 30, Art. 1585, doi: 10.1029/2003GL017000.
  18. Calfapietra, C., Mugnozza, G. S., Karnosky, D. F., Loreto, F., and Sharkey, T. D. 2008. Isoprene emission rates under elevated CO2 and O3 in two field-grown aspen clones differing in their sensitivity to O3. New Phytol. 179:55–61.PubMedCrossRefGoogle Scholar
  19. Calogirou, A., Larsen, B. R., Brussol, C., Duane, M., and Kotzias, D. 1996. Decomposition of terpenes by ozone during sampling on Tenax. Anal. Chem. 68:1499–1506.CrossRefGoogle Scholar
  20. Calogirou, A., Larsen, B. R., and Kotzias, D. 1999. Gas-phase terpene oxidation products: a review. Atmos. Environ. 33:1423–1439.CrossRefGoogle Scholar
  21. Cannon, W. N. 1990. Olfactory response of eastern spruce budworm larvae to red spruce needles exposed to acid-rain and elevated levels of ozone. J. Chem. Ecol. 16:3255–3261.CrossRefGoogle Scholar
  22. Cape, J. N. 2008. Interactions of forests with secondary air pollutants: Some challenges for future research. Environ. Pollut. 155:391–397.PubMedCrossRefGoogle Scholar
  23. Claeys, M., Graham, B., Vas, G., Wang, W., Vermeylen, R., Pashynska, V., Cafmeyer, J., Guyon, P., Andreae, M. O., Artaxo, P., and Maenhaut, W. 2004. Formation of secondary organic aerosols through photooxidation of isoprene. Science 303:1173–1176.PubMedCrossRefGoogle Scholar
  24. De Boer, J. G. and Dicke, M. 2004. The role of methyl salicylate in prey searching behavior of the predatory mite Phytoseiulus persimilis. J. Chem. Ecol. 30:255–271.PubMedCrossRefGoogle Scholar
  25. Dicke, M. 1999. Evolution of induced indirect defense of plants, pp. 62–88, in R. Tollrian and C. D. Harvell (eds.). The Ecology and Evolution of Inducible Defenses. Princeton University Press, Princeton.Google Scholar
  26. Dicke, M., van Beek, T. A., Posthumus, M. A., Bendom, N., van Bokhoven, H., and de Groot, A. E. 1990. Isolation and identification of volatile kairomone that affects acarine predator–prey interactions. Involvement of host plant in its production. J. Chem. Ecol. 16:381–396.CrossRefGoogle Scholar
  27. Dizengremel, P., Le Thiec, D., Bagard, M., and Jolivet, Y. 2008. Ozone risk assessment for plants: central role of metabolism-dependent changes in reducing power. Environ. Pollut. 156:11–15.PubMedCrossRefGoogle Scholar
  28. Dudareva, N., Negre, F., Nagegowda, D. A., and Orlova, I. 2006. Plant volatiles: recent advances and future perspectives. Crit. Rev. Plant Sci. 25:417–440.CrossRefGoogle Scholar
  29. Farag, M. A. and Paré, P. W. 2002. C-6-green leaf volatiles trigger local and systemic VOC emissions in tomato. Phytochemistry 61:545–554.PubMedCrossRefGoogle Scholar
  30. Farmer, E. E. and Ryan, C. A. 1990. Interplant communication—airborne methyl jasmonate induces synthesis of proteinase-inhibitors in plant leaves. Proc. Nat. Acad. Sci. USA 87:7713–7716.PubMedCrossRefGoogle Scholar
  31. Finlayson-Pitts, B. J. and Pitts, J. N. Jr. 2000. Chemistry of the Upper and Lower Atmosphere Theory, Experiments and Applications, 1st edn, p. 969. Academic, San Diego.Google Scholar
  32. Fowler, S. V. and Lawton, J. H. 1985. Rapidly induced defences and talking trees—the devil’s advocate position. Am. Nat. 126:181–195.CrossRefGoogle Scholar
  33. Frati, F., Chamberlain, K., Birkett, M., Dufour, S., Mayon, P., Woodcock, C., Wadhams, L., Pickett, J., Salerno, G., Conti, E., and Bin, F. 2009. Vicia faba—Lygus rugulipennis interactions: induced plant volatiles and sex pheromone enhancement. J. Chem. Ecol. 35:201–208.PubMedCrossRefGoogle Scholar
  34. Frost, C. J., Appel, H. M., Carlson, J. E., de Moraes, C. M., Mescher, M. C., and Schultz, J. C. 2007. Within-plant signalling via volatiles overcomes vascular constraints on systemic signalling and primes responses against herbivores. Ecol. Lett. 10:490–498.PubMedCrossRefGoogle Scholar
  35. Frost, C. J., Mescher, M. C., Dervinis, C., Davis, J. M., Carlson, J. E., and de Moraes, C. M. 2008. Priming defense genes and metabolites in hybrid poplar by the green volatile cis-3-hexenyl acetate. New Phytol. 180:722-734.PubMedCrossRefGoogle Scholar
  36. Fruekilde, P., Hjorth, J., Jensen, N. R., Kotzias, D., and Larsen, B. 1998. Ozonolysis at vegetation surfaces: a source of acetone, 4-oxopentanal, 6-methyl-5-hepten-2-one, and geranyl acetone in the troposphere. Atmos. Environ. 32:1893–1902.CrossRefGoogle Scholar
  37. Fuentes, J. D., Lerdau, M., Atkinson, R., Baldocchi, D., Bottenheim, J. W., Ciccioli, P., Lamb, B., Geron, C., Gu, L., Guenther, A., Sharkey, T. D., and Stockwell, W. 2000. Biogenic hydrocarbons in the atmospheric boundary layer: a review. Bull. Am. Meteorol. Soc. 81:1537–1575.CrossRefGoogle Scholar
  38. Gate, I. M., McNeill, S., and Ashmore, M. R. 1995. Effects of air pollution on the searching behaviour of an insect parasitoid. Water Air Soil Pollut. 85:1425–1430.CrossRefGoogle Scholar
  39. Godard, K. A., White, R., and Bohlmann, J. 2008. Monoterpene-induced molecular responses in Arabidopsis thaliana. Phytochemistry 69: 1838–1849.PubMedCrossRefGoogle Scholar
  40. Gouinguené, S. P. and Turlings, T. C. J. 2002. The effects of abiotic factors on induced volatile emissions in corn plants. Plant Physiol. 129:1296–1307.PubMedCrossRefGoogle Scholar
  41. Grantz, D. A., Gunn, S., and Vu, H.-B. 2006. O3 impacts on plant development: a meta-analysis of root/shoot allocation and growth. Plant Cell Environ. 29:1193–1209.PubMedCrossRefGoogle Scholar
  42. Guenther, A. 1999. Modeling biogenic volatile organic compounds emissions to the atmosphere, pp. 97–118, in C. N. Hewitt (ed.). Reactive Hydrocarbon in the Atmosphere. Academic, San Diego.CrossRefGoogle Scholar
  43. Guerrieri, E., Poppy, G. M., Powell, W., Rao, R., and Pennacchio, F. 2002. Plant-to-plant communication mediating in-flight orientation of Aphidius ervi. J. Chem. Ecol. 28:1703–1715.PubMedCrossRefGoogle Scholar
  44. Hartikainen, K., Nerg, A.-M., Kivimäenpää, M., Kontunen-Soppela, S., Mäenpää, M., Oksanen, E., Rousi, M., and Holopainen, T. 2009. Emissions of volatile organic compounds and leaf structural characteristics of European aspen (Populus tremula) grown under elevated ozone and temperature. Tree Physiol. doi: 10.1093/treephys/tpp033 PubMedGoogle Scholar
  45. Heath, R. L. 2008. Modification of the biochemical pathways of plants induced by ozone: what are the varied routs to change? Environ. Pollut. 155:453–463.PubMedCrossRefGoogle Scholar
  46. Heiden, A. C., Hoffmann, T., Kahl, J., Kley, D., Klockow, D., Langebartels, C., Mehlhorn, H., Sandermann, H., Schraudner, M., Schuh, G., and Wildt, J. 1999. Emission of volatile organic compounds from ozone-exposed plants. Ecol. Appl. 9:1160–1167.CrossRefGoogle Scholar
  47. Heiden, A. C., Kobel, K., Langebartels, C., Schuh-Thomas, G., and Wildt, J. 2003. Emissions of oxygenated volatile organic compounds from plants—part I: emissions from lipoxygenase activity. J. Atmos. Chem. 45:143–172.CrossRefGoogle Scholar
  48. Heil, M. and Silva Bueno, J. C. 2007. Within-plant signaling by volatiles leads to induction and priming of an indirect plant defense in nature. Proc. Nat. Acad. Sci. USA 104:5467–5472.PubMedCrossRefGoogle Scholar
  49. Hewitt, C. N., Owen, S., Boissard, C., and Csiky, O. 1994. Biogenic emissions in the Mediterranean area report on BEMA field campaign at Castelporziano, May 1994. BEMA-Project (Biogenic Emissions in the Mediterranean Area). European Comission, EUR 16293 EN, pp. 137–150.Google Scholar
  50. Himanen, S. J., Nerg, A.-M., Nissinen, A., Pinto, D. M., Stewart, C. N. Jr., Poppy, G. M., and Holopainen, J. K. 2009. Effects of elevated carbon dioxide and ozone on volatile terpenoid emissions and multitrophic communication of transgenic insecticidal oilseed rape (Brassica napus). New Phytol. 181:174–186.PubMedCrossRefGoogle Scholar
  51. Hoffmann, T., Odum, J. R., Bowman, F., Collins, D., Klockow, D, Flagan, R. C., and Seinfeld, J. H. 1997. Formation of organic aerosols from the oxidation of biogenic hydrocarbons. J. Atmos. Chem. 26:189–222.CrossRefGoogle Scholar
  52. Holopainen, J. K. 2004. Multiple functions of inducible plant volatiles. Trends Plant Sci. 9:529–533.PubMedCrossRefGoogle Scholar
  53. Holton, M. K., Lindroth, R. L., and Nordheim, E. V. 2003. Foliar quality influences tree-herbivore-parasitoid interactions: effects of elevated CO2, O3, and plant genotype. Oecologia 137:233–244.PubMedCrossRefGoogle Scholar
  54. IPCC (Intergovernmental Panel on Climate Change) 2007. 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. Available at: http://www.ipcc.ch/pdf/assessmentreport/ar4/syr/ar4_syr.pdf (accessed 7 October 2009).
  55. Jackson, D. M., Heagle, A. S., and Eckel, R. V. W. 1999. Ovipositional response of tobacco hornworm moths (Lepidoptera: Sphingidae) to tobacco plants grown under elevated levels of ozone. Environ. Entomol. 28:566–571.Google Scholar
  56. Jones, C. G. and Coleman, J. S. 1988. Plant stress and insect behavior—cottonwood, ozone and the feeding and oviposition preference of a beetle. Oecologia 76:51–56.Google Scholar
  57. Kai, Y., Matsumura, H., and Izui, K. 2003. Phosphoenolpyruvate carboxylase: three-dimensional structure and molecular mechanisms. Arch. Biochem. Biophys. 414:170–179.PubMedCrossRefGoogle Scholar
  58. Kangasjärvi, J., Jaspers, P., and Kollist, H. 2005. Signalling and cell death in ozone-exposed plants. Plant Cell Environ. 28:1021–1036.CrossRefGoogle Scholar
  59. Karban, R. and Baldwin, I. T. 1997. Induced Responses to Herbivory, 1st edn, p. 319. University of Chicago Press, Chicago.Google Scholar
  60. Karban, R., Maron, J., Felton, G. W., Ervin, G., and Eichenseer, H. 2003. Herbivore damage to sagebrush induces resistance in wild tobacco: evidence for eavesdropping between plants. Oikos 100:325–332.CrossRefGoogle Scholar
  61. Kempema, L., Cui, X., Holzer, F. M., and Walling, L. L. 2007. Arabidopsis transcriptome changes in response to phloem-feeding silverleaf whitefly nymphs. Similarities and distinctions in responses to aphids. Plant Physiol. 143:849–865.PubMedCrossRefGoogle Scholar
  62. Kesselmeier, J. and Staudt, M. 1999. Biogenic volatile organic compounds (VOC): an overview on emission, physiology and ecology. J. Atmos. Chem. 33:23–88.CrossRefGoogle Scholar
  63. Kopper, B. J. and Lindroth, R. L. 2003. Effects of elevated carbon dioxide and ozone on the phytochemistry of aspen and performance of an herbivore. Oecologia 134:95–103.PubMedCrossRefGoogle Scholar
  64. Kost, C. and Heil, M. 2005. Increased availability of extrafloral nectar reduces herbivory in Lima bean plants (Phaseolus lunatus, Fabaceae). Basic Appl. Ecol. 6:237–248.CrossRefGoogle Scholar
  65. Kurpius, M. R. and GOLDSTEIN, A. H. 2003. Gas-phase chemistry dominates O3 loss to a forest, implying a source of aerosols and hydroxyl radicals to the atmosphere. Geophys. Res. Lett. 30, Article Number: 1371.Google Scholar
  66. Laothawornkitkul, J., Taylor, J. E., Paul, N. D., and Hewitt, C. N. 2009. Biogenic volatile organic compounds in the Earth system. New Phytol. 183:27–51.PubMedCrossRefGoogle Scholar
  67. Lee, A., Goldstein, A. H., Keywood, M. D., Gao, S., Varutbangkul, V., Bahreini, R., Ng, N. L., Flagan, R. C., and Seinfeld, J. H. 2006. Gas-phase products and secondary aerosol yields from the ozonolysis of ten different terpenes. J. Geophys. Res. 111, D07302. doi: 10.1029/2005JD006437.CrossRefGoogle Scholar
  68. Leitao, L., Bethenod, O., and Biolley, J. P. 2007. The impact of ozone on juvenile maize (Zea mays L.) plant photosynthesis: effects on vegetative biomass, pigmentation, and carboxylases (PEPc and Rubisco). Plant Biol. 9:478–488.PubMedCrossRefGoogle Scholar
  69. Lerdau, M. and Slobodkin, L. 2002. Trace gas emissions and species-dependent ecosystem services. Trends Ecol. Evol. 17:309–312.CrossRefGoogle Scholar
  70. Li, S., Matthews, J., and Sinha, A. 2009 Atmospheric hydroxyl radical production from electronically excited NO2 and H2O. Science 319:1657–1659.CrossRefGoogle Scholar
  71. Llusià, J., Peñuelas, J., and Gimeno, B. S. 2002. Seasonal and species-specific response of VOC emissions by Mediterranean woody plant to elevated ozone concentrations. Atmos. Environ. 36:3931–3938.CrossRefGoogle Scholar
  72. Long, S. P. and Naidu, S. L. 2002. Effects of oxidants at the biochemical, cell, and physiological levels, with particular reference to ozone, pp. 69–88, in J. N. B. Bell and M. Treshow (eds.). Air Pollution and Plant Life. Wiley, London.Google Scholar
  73. Loreto, F., Mannozzi, M., Maris, C., Nascetti, P., Ferranti, F., and Pasqualini, S. 2001. Ozone quenching properties of isoprene and its antioxidant role in leaves. Plant Physiol. 126:993–1000.PubMedCrossRefGoogle Scholar
  74. Loreto, F., Pinelli, P., Manes, F., and Kollist, H. 2004. Impact of ozone on monoterpene emissions and evidence for an isoprene-like antioxidant action of monoterpenes emitted by Quercus ilex leaves. Tree Physiol. 24:361–367.PubMedGoogle Scholar
  75. McFrederick, Q. S., Kathilankal, J. C., and Fuentes, J. D. 2008. Air pollution modifies floral scent trails. Atmos. Environ. 42:2336–2348.CrossRefGoogle Scholar
  76. McFrederick, Q. S, Fuentes, J. D., Roulston, T., Kathilankal, J. C., and Lerdau, M. 2009. Effects of air pollution on biogenic volatiles and ecological interactions. Oecologia 160:411–420.PubMedCrossRefGoogle Scholar
  77. Mirabella, R., Rauwerda, H., Struys, E. A., Jakobs, C., Triantaphylidès, C., Haring, M. A., and Schuurink, R. C. 2008. The Arabidopsis her1 mutant implicates GABA in (E)-2-hexenal responsiveness. Plant J. 53:197–213.PubMedCrossRefGoogle Scholar
  78. Müller, C. and Riederer, M. 2005. Plant surface properties in chemical ecology. J. Chem. Ecol. 31:2621–2651.PubMedCrossRefGoogle Scholar
  79. Nishida, N., Tamotsu, S., Nagata, N., Saito, C., and Sakai, A., 2005. Allelopathic effects of volatile monoterpenoids produced by Salvia leucophylla: inhibition of cell proliferation and DNA synthesis in the root apical meristem of Brassica campestris seedlings. J. Chem. Ecol. 31:1187–1203.PubMedCrossRefGoogle Scholar
  80. O’Donnell, P. J., Calvert, C., Atzorn, R., Wasternack, C., Leyser, H. M. O., and Bowles, D. J. 1996. Ethylene as a signal mediating the wound response of tomato plants. Science 274:1914–1917.PubMedCrossRefGoogle Scholar
  81. Overmyer, K., Kollist, H., Tuominen, H., Betz, C., Langebartels, C., Wingsle, G., Kangasjärvi, S., Brader, G., Mullineaux, P. and Kangasjärvi, J. 2008. Complex phenotypic profiles leading to ozone sensitivity in Arabidopsis thaliana mutants. Plant Cell Environ. 31:1237–1249.PubMedCrossRefGoogle Scholar
  82. Paré, P. W. and Tumlinson, J. H. 1997. De novo biosynthesis of volatiles induced by insect herbivory in cotton plants. Plant Physiol. 114:1161–1167.PubMedGoogle Scholar
  83. Peñuelas, J. and Llusià, J. 2003. BVOCs: plant defense against climate warming? Trends Plant Sci. 8:105–109.PubMedCrossRefGoogle Scholar
  84. Peñuelas, J., Llusià, J., and Gimeno, B. S. 1999. Effects of ozone concentrations on biogenic volatile organic compounds emission in the Mediterranean region. Environ. Pollut. 105:17–23.CrossRefGoogle Scholar
  85. Percy, K. E., Jensen, K. F., and McQuattie, C. J. 1992. Effects of ozone and acidic fog on red spruce needle epicuticular wax production, chemical composition, cuticular membrane ultrastructure and needle wettability. New Phytol. 122:71–80.CrossRefGoogle Scholar
  86. Percy, K. E., Awmack, C. S., Lindroth, R. L., Kubiske, M. E., Kopper, B. J., Isebrands, J. G., Pregitzer, K. S., Hendrey, G. R., Dickson, R. E., Zak, D. R., Oksanen, E., Sober, J., Harrington, R., and Karnosky, D. F. 2002. Altered performance of forest pests under atmospheres enriched by CO2 and O3. Nature 420:403–407.PubMedCrossRefGoogle Scholar
  87. Pieterse, C. M. J., Ton, J., and van Loon, L. C. 2001. Cross-talk between plant defense signalling pathways: boost or burden. Ag. Biotech. Net 3 ABN 068.Google Scholar
  88. Pinto, D. M., Blande, J. D., Nykänen, R., Dong, W. X., Nerg, A.-M., and Holopainen, J. K. 2007a. Ozone degrades common herbivore-induced plant volatiles: does this affect herbivore prey location by predators and parasitoids? J. Chem. Ecol. 33:683–694.PubMedCrossRefGoogle Scholar
  89. Pinto, D. M., Nerg, A.-M., and Holopainen, J. K. 2007b. The role of ozone reactive compounds, terpenes and green leaf volatiles (GLVs), in the orientation of Cotesia plutellae. J. Chem. Ecol. 33:2218–2228.PubMedCrossRefGoogle Scholar
  90. Pinto, D. M., Tiiva, P., Miettinen, P., Joutsensaari, J., Kokkola, H., Nerg, A.-M., Laaksonen, A., and Holopainen, J. K. 2007c. The effects of increasing atmospheric ozone on biogenic monoterpene profiles and the formation of secondary aerosols. Atmos. Environ. 41:4877–4887.CrossRefGoogle Scholar
  91. Pinto, D. M., Himanen, S. J., Nissinen, A., Nerg, A.-M., and Holopainen, J. K. 2008. Host location behavior of Cotesia plutellae Kurdjumov (Hymenoptera: Braconidae) in ambient and moderately elevated ozone in field conditions. Environ. Pollut. 156:227–231.PubMedCrossRefGoogle Scholar
  92. Preston, C. A., Laue, G., and Baldwin, I. T. 2001. Methyl jasmonate is blowing in the wind, but can it act as a plant–plant airborne signal? Biochem. System. Ecol. 29:1007–1023.CrossRefGoogle Scholar
  93. Rao, M. V., Koch, J. R., and Davis, K. R. 2000. Ozone: a tool for probing programmed cell death in plants. Plant Mol. Biol. 44:345–358.PubMedCrossRefGoogle Scholar
  94. Rasmann, S., Kollner, T. G., Degenhardt, J., Hiltpold, I., Toepfer, S., Kuhlmann, U., Gershenzon, J., and Turlings, T. C. J. 2005. Recruitment of entomopathogenic nematodes by insect-damaged maize roots. Nature 434:732–737.PubMedCrossRefGoogle Scholar
  95. Riikonen, J., Kets, K., Darbah, J., Oksanen, E., Sober, A., Vapaavuori, E., Kubiske, M. E., Nelson, N., and Karnosky, D. F. 2008. Carbon gain and bud physiology in Populus tremuloides and Betula papyrifera grown under long-term exposure to elevated concentrations of CO2 and O3. Tree Physiol. 28:243–254.PubMedGoogle Scholar
  96. Romagni, J. G., Allen, S. N., and Dayan, F. E. 2000. Allelopathic effects of volatile cineoles on two weedy plant species. J. Chem. Ecol. 26:303–313.CrossRefGoogle Scholar
  97. Ruther, J. and Kleier, S. 2005. Plant–plant signalling: Ethylene synergizes volatile emission in Zea mays induced by exposure to (Z)-3-hexen-1-ol. J. Chem. Ecol. 31:2217–2222.PubMedCrossRefGoogle Scholar
  98. Sant’Anna, S. M. R., Esposito, M. P., Domingos, M., and Souza, S. R. 2008. Suitability of Nicotiana tabacum ‘Bel W3’ for biomonitoring ozone in Sao Paulo, Brazil. Environ. Pollut. 151:389–394.PubMedCrossRefGoogle Scholar
  99. Schoonhoven, L. M., van Loon, J. J. A., and Dicke, M. 2006. Insect–Plant Biology. Oxford University Press, UK.Google Scholar
  100. Seinfeld, J. H. and Pandis, S. N. 2006. Atmospheric Chemistry and Physics: From Air Pollution to Climate Change, 2nd edn, p. 1232. Wiley-Interscience, USAGoogle Scholar
  101. Sharkey, T. D., Wiberley, A. E., Donohue, A. R. 2008. Isoprene emission from plants: why and how. Annal. Bot. 101:5–18.PubMedCrossRefGoogle Scholar
  102. Shulaev, V., Silverman, P., and Raskin, I. 1997. Airborne signalling by methyl salicylate in plant pathogen resistance. Nature 385:718–721.CrossRefGoogle Scholar
  103. Sitch, S., Cox, P. M., Collins, W. J., and Huntingford, C. 2007. Indirect radiative forcing of climate change through ozone effects on the land–carbon sink. Nature 448:791–794PubMedCrossRefGoogle Scholar
  104. Souza, S. R., Vasconcellos, P. C., and Carvalho, L. R. 1999. Low-molecular weight carboxylic acids in an urban atmosphere: winter measurements in São Paulo City, Brazil. Atmos. Environ. 33:2563–2574.CrossRefGoogle Scholar
  105. The Royal Society. 2008. Ground-level ozone in the 21st century: future trends, impacts and policy implications. Science Policy, Report 15/08, http://royalsociety.org/displaypagedoc.asp?id=31506.
  106. Ton, J., D’Alessandro, M., Jourdie, V., Jakab, G., Karlen, D., Held, M., Mauch-Mani, B., and Turlings, T. C. J. 2007. Priming by airborne signals boosts direct and indirect resistance in maize. Plant J. 49:16–26.PubMedCrossRefGoogle Scholar
  107. Wennberg, O. P. and Dabdub, D. 2009. Rethinking ozone production. Science 319:1624–1625CrossRefGoogle Scholar
  108. Valkama, E., Koricheva, J., and Oksanen, E. 2007. Effects of elevated O3, alone and in combination with elevated CO2, on tree leaf chemistry and insect herbivore performance: a meta-analysis. Glob. Change Biol. 13:184–201CrossRefGoogle Scholar
  109. van Reken, T. M., Greenberg, J. P., Harley, P. C., Guenther, A. B., and Smith, J. N. 2006. Direct measurement of particle formation and growth from the oxidation of biogenic emissions. Atmos. Chem. Phys. 6:4403–4413.CrossRefGoogle Scholar
  110. Vingarzan, R. 2004. A review of surface ozone background levels and trends. Atmos. Environ. 38:3431–3442.CrossRefGoogle Scholar
  111. Vuorinen, T., Nerg, A.-M., and Holopainen, J. K. 2004a. Ozone exposure triggers the emission of herbivore-induced plant volatiles, but does not disturb tritrophic signalling. Environ. Pollut. 131:305–311.PubMedCrossRefGoogle Scholar
  112. Vuorinen, T., Nerg, A.-M., Ibrahim, M. A., Reddy, G. V. P., and Holopainen, J. K. 2004b. Emission of Plutella xylostella-induced compounds from cabbages grown at elevated CO2 and orientation behavior of the natural enemies. Plant Physiol. 135:1984–1992.PubMedCrossRefGoogle Scholar
  113. Vuorinen, T., Nerg, A.-M., Vapaavuori, E., and Holopainen, J. K. 2005. Emission of volatile organic compounds from two silver birch (Betula pendula Roth) clones grown under ambient and elevated CO2 and different O3 concentrations. Atmos. Environ. 39:1185–1197.CrossRefGoogle Scholar
  114. Yan, Z. G., and Wang, C. Z. 2006. Wound-induced green leaf volatiles cause the release of acetylated derivatives and a terpenoid in maize. Phytochemistry 67:34–42.PubMedCrossRefGoogle Scholar
  115. Yu, J., Cocker III, D. R., Griffin, R. J., Flagan, R. C., and Seinfeld, J. H. 1999. Gas-phase ozone oxidation of monoterpenes: gaseous and particulate products. J. Atmos. Chem. 34:207–258.CrossRefGoogle Scholar
  116. Yuan, J. S., Himanen, S., Holopainen, J. K., Chen, F., and Stewart, C. N. Jr. 2009. Smelling global climate change: mitigation of function for plant volatile organic compounds. Trends Ecol. Evol. 24:323–331.PubMedCrossRefGoogle Scholar
  117. Zhu, J. W., and Park, K. C. 2005. Methyl salicylate, a soybean aphid-induced plant volatile attractive to the predator Coccinella septempunctata. J. Chem. Ecol. 31:1733–1746.PubMedCrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media, LLC 2010

Authors and Affiliations

  • Delia M. Pinto
    • 1
  • James D. Blande
    • 2
  • Silvia R. Souza
    • 3
  • Anne-Marja Nerg
    • 2
  • Jarmo K. Holopainen
    • 2
  1. 1.Plant Production Research/Plant Protection UnitMTT Agrifood Research FinlandJokioinenFinland
  2. 2.Department of Environmental ScienceUniversity of KuopioKuopioFinland
  3. 3.Department of EcologyBotanic InstituteSão PauloBrazil

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