The Role of Volatile Organic Compounds in Plant Resistance to Abiotic Stresses: Responses and Mechanisms

  • Malcolm PossellEmail author
  • Francesco Loreto
Part of the Tree Physiology book series (TREE, volume 5)


Why plants constitutively emit certain volatile organic compounds is a question that has attracted numerous researchers since the discovery of emissions. A number of hypotheses exist regarding the role of constitutive volatile organic compounds and many of these highlight the role of these compounds in enhancing plant tolerance to certain abiotic stresses. As practically any stress can modify constitutive emissions and also elicit production of novel compounds (induced emissions), this chapter provides a review of the hypotheses with particular foci on the key environmental stresses – heat and drought. Furthermore, we discuss how changes in the atmospheric CO2 concentration over past and future geologic epochs are likely to affect the role of volatile organic compounds as an adaptation to abiotic stresses.


Heat Stress Secondary Organic Aerosol Isoprene Emission Methyl Vinyl Ketone Methyl Vinyl Ketone 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.


  1. Adushkin VV, Kudryavtsev VP (2010) Global methane flux into the atmosphere and its seasonal variations. Izv Phys Solid Earth 46:350–357Google Scholar
  2. Affek HP, Yakir D (2002) Protection by isoprene against singlet oxygen in leaves. Plant Phys 129:269–277Google Scholar
  3. Almeras E, Stolz S, Vollenweider S, Reymond P, Mene-Saffrane L, Farmer EE (2003) Reactive electrophile species activate defense gene expression in Arabidopsis. Plant J 34:205–216PubMedGoogle Scholar
  4. Apel K, Hirt H (2004) Reactive oxygen species: metabolism, oxidative stress, and signal transduction. Annu Rev Plant Biol 55:373–399PubMedGoogle Scholar
  5. Arneth A, Niinemets Ü (2010) Induced BVOCs: how to bug our models? Trends Plant Sci 15(3):118–125PubMedGoogle Scholar
  6. Arneth A, Monson RK, Schurgers G, Niinemets Ü, Palmer PI (2008) Why are estimates of global terrestrial isoprene emissions so similar (and why is this not so for monoterpenes)? Atmos Chem Phys 8:4605–4620Google Scholar
  7. Asada K (2006) Production and scavenging of reactive oxygen species in chloroplasts and their functions. Plant Physiol 141:391–396PubMedGoogle Scholar
  8. Asensio D, Owen SM, Llusià J, Peñuelas J (2008) The distribution of volatile isoprenoids in the soil horizons around Pinus halepensis trees. Soil Biol Biochem 40:2937–2947Google Scholar
  9. Ashworth K, Boissard C, Folberth G, Lathière J, Schurgers G (2013) Global modeling of volatile organic compound emissions. In: Niinemets Ü, Monson RK (eds) Biology, controls and models of tree volatile organic compound emissions, vol 5, Tree physiology. Springer, Berlin, pp –Google Scholar
  10. Beauchamp J, Wisthaler A, Hansel A, Kleist E, Miebach M, Niinemets Ü, Schurr U, Wildt J (2005) Ozone induced emissions of biogenic VOC from tobacco: relations between ozone uptake and emission of LOX products. Plant Cell Environ 28:1334–1343Google Scholar
  11. Behnke K, Ehlting B, Teuber M, Bauerfeind M, Louis S, Hänsch R, Polle A, Bohlmann J, Schnitzler J-P (2007) Transgenic, non-isoprene emitting poplars don’t like it hot. Plant J 51:485–499PubMedGoogle Scholar
  12. Behnke K, Loivamäki M, Zimmer I, Rennenberg H, Schnitzler J-P, Louis S (2010) Isoprene emission protects photosynthesis in sunfleck exposed grey poplar. Photosynth Res 104:5–17PubMedGoogle Scholar
  13. Beligni MV, Lamattina L (2002) Nitric oxide interferes with plant photo-oxidative stress by detoxifying reactive oxygen species. Plant Cell Environ 25:737–748Google Scholar
  14. Ben Taarit M, Msaada K, Hosni K, Hammami M, Kchouk ME, Marzouk B (2009) Plant growth, essential oil yield and composition of sage (Salvia officinalis L.) fruits cultivated under salt stress conditions. Ind Crop Prod 30(3):333–337. doi: 10.1016/j.indcrop.2009.06.001 Google Scholar
  15. Bertin N, Staudt M (1996) Effect of water stress on monoterpene emissions from young potted holm oak (Quercus ilex L) trees. Oecologia 107:456–462Google Scholar
  16. Boy M, Karl T, Turnipseed A, Mauldin RL, Kosciuch E, Greenberg J, Rathbone J, Smith J, Held A, Barsanti K, Wehner B, Bauer S, Wiedensohler A, Bonn B, Kulmala M, Guenther A (2008) New particle formation in the front range of the Colorado Rocky Mountains. Atmos Chem Phys 8:1577–1590Google Scholar
  17. Brilli F, Barta C, Fortunati A, Lerdau M, Loreto F, Centritto M (2007) Response of isoprene emission and carbon metabolism to drought in white poplar (Populus alba) saplings. New Phytol 175:244–254PubMedGoogle Scholar
  18. Brilli F, Hörtnagl L, Bamberger I, Schnitzhofer R, Ruuskanen TM, Hansel A, Loreto F, Wohlfahrt G (2012) Qualitative and quantitative characterization of volatile organic compound emissions from cut grass. Environ Sci Technol 46:3859–3865PubMedGoogle Scholar
  19. Bruhn D, Møller IM, Mikkelsen TN, Ambus P (2012) Terrestrial plant methane production and emission. Physiol Plant 144:201–209PubMedGoogle Scholar
  20. Calfapietra C, Pallozzi E, Lusini I, Velikova V (2013) Modification of BVOC emissions by changes in atmospheric [CO2] and air pollution. In: Niinemets Ü, Monson RK (eds) Biology, controls and models of tree volatile organic compound emissions, vol 5, Tree physiology. Springer, Berlin, pp –Google Scholar
  21. Capitani D, Brilli F, Mannina L, Proietti N, Loreto F (2009) In situ investigation of leaf water status by portable unilateral nuclear magnetic resonance. Plant Physiol 149:1638–1647PubMedGoogle Scholar
  22. Centritto M, Brilli F, Fodale R, Loreto F (2011) Different sensitivity of isoprene emission, respiration and photosynthesis to high growth temperature coupled with drought stress in black poplar (Populus nigra) saplings. Tree Physiol 31:275–286PubMedGoogle Scholar
  23. Claeys M, Graham B, Vas G, Wang W, Vermeylen R, Pashynska V, Cafmeyer J, Guyon P, Andreae MO, Artaxo P, Maenhaut W (2004) Formation of secondary organic aerosols through photooxidation of isoprene. Science 303:1173–1176PubMedGoogle Scholar
  24. Copolovici L, Niinemets Ü (2010) Flooding induced emissions of volatile signaling compounds in three tree species with differing waterlogging tolerance. Plant Cell Environ 33:1582–1594PubMedGoogle Scholar
  25. Copolovici LO, Filella I, Llusià J, Niinemets Ü, Peñuelas J (2005) The capacity for thermal protection of photosynthetic electron transport varies for different monoterpenes in Quercus ilex. Plant Physiol 139(1):485–496. doi: 10.1104/pp. 105.065995PubMedGoogle Scholar
  26. Copolovici L, Kännaste A, Pazouki L, Niinemets Ü (2012) Emissions of green leaf volatiles and terpenoids from Solanum lycopersicum are quantitatively related to the severity of cold and heat shock treatments. J Plant Physiol 169:664–672PubMedGoogle Scholar
  27. Cowling SA, Sage RF (1998) Interactive effects of low atmospheric CO2 and elevated temperature on growth, photosynthesis and respiration in Phaseolus vulgaris. Plant Cell Environ 21:427–435Google Scholar
  28. Darbah JNT, Sharkey TD, Calfapietra C, Karnosky DF (2010) Differential response of aspen and birch trees to heat stress under elevated carbon dioxide. Environ Pollut 158:1008–1014PubMedGoogle Scholar
  29. Delfine S, Csiky O, Seufert G, Loreto F (2000) Fumigation with exogenous monoterpenes of a non-isoprenoid-emitting oak (Quercus suber): monoterpene acquisition, translocation, and effect on the photosynthetic properties at high temperatures. New Phytol 146:27–36Google Scholar
  30. Denman KL, Brasseur G, Chidthaisong A, Ciais P, Cox PM, Dickinson RE, Hauglustaine D, Heinze C, Holland E, Jacob D, Lohmann U, Ramachandran S, da Silva Dias PL, Wofsy SC, Zhang X (2007) Couplings between changes in the climate system and biogeochemistry. In: Solomon S, Qin D, Manning M, Chen Z, Marquis M, Averyt KB, Tignor M, Miller HL (eds) Climate Change 2007: the physical science basis. Contribution of working group I to the fourth assessment report of the Intergovernmental Panel on Climate Change. Cambridge University Press, CambridgeGoogle Scholar
  31. Dudareva N, Negre F, Nagegowda DA, Orlova I (2006) Plant volatiles: recent advances and future perspectives. CRC Crit Rev Plant Sci 25:417–440Google Scholar
  32. Fall R (2003) Abundant oxygenates in the atmosphere: a biochemical perspective. Chem Rev 103:4941–4951PubMedGoogle Scholar
  33. Fares S, Mereu S, Scarascia Mugnozza G, Vitale M, Manes F, Frattoni M, Ciccioli P, Gerosa G, Loreto F (2009) The ACCENT-VOCBAS field campaign on biosphere-atmosphere interactions in a Mediterranean ecosystem of Castelporziano (Rome): site characteristics, climatic and meteorological conditions, and eco-physiology of vegetation. Biogeosciences 6:1043–1058Google Scholar
  34. Fehsenfeld F, Calvert J, Fall R, Goldan P, Guenther AB, Hewitt CN, Lamb B, Liu S, Trainer M (1992) Emissions of volatile organic compounds from vegetation and the implications for atmospheric chemistry. Global Biogeochem Cycles 6:389–430Google Scholar
  35. Feussner I, Wasternack C (2002) The lipoxygenase pathway. Annu Rev Plant Biol 53:275–297PubMedGoogle Scholar
  36. Filella I, Peñuelas J, Seco R (2009) Short-chained oxygenated VOC emissions in Pinus halepensis in response to changes in water availability. Acta Physiol Plant 31:311–318Google Scholar
  37. Fineschi S, Loreto F, Staudt M, Peñuelas J (2013) Diversification of volatile isoprenoid emissions from trees: evolutionary and ecological perspectives. In: Niinemets Ü, Monson RK (eds) Biology, controls and models of tree volatile organic compound emissions, vol 5, Tree physiology. Springer, Berlin, pp –Google Scholar
  38. Flexas J, Bota J, Loreto F, Cornic G, Sharkey TD (2004) Diffusive and metabolic limitations to photosynthesis under drought and salinity in C3 plants. Plant Biol 6:269–279PubMedGoogle Scholar
  39. Fortunati A, Barta C, Brilli F, Centritto M, Zimmer I, Schnitzler J-P, Loreto F (2008) Isoprene emission is not temperature-dependent during and after severe drought-stress: a physiological and biochemical analysis. Plant J 55:687–697PubMedGoogle Scholar
  40. Fuentes JD, Lerdau M, Atkinson R, Baldocchi D, Bottenheim JW, Ciccioli P, Lamb B, Geron C, Gu L, Guenther A, Sharkey TD, Stockwell W (2000) Biogenic hydrocarbons in the atmospheric boundary layer: a review. Bull Am Met Soc 81:1537–1575Google Scholar
  41. Ghirardo A, Koch K, Taipale R, Zimmer I, Schnitzler J-P, Rinne J (2010) Determination of de novo and pool emissions of terpenes from four common boreal/alpine trees by 13CO2 labelling and PTR-MS analysis. Plant Cell Environ 33:781–792PubMedGoogle Scholar
  42. Gould KS, Lamotte O, Klinguer A, Pugin A, Wendehenne D (2003) Nitric oxide production in tobacco leaf cells: a generalized stress response? Plant Cell Environ 26:1851–1862Google Scholar
  43. Grace J, Rayment M (2000) Respiration in the balance. Nature 404:819–820PubMedGoogle Scholar
  44. Grote R, Monson RK, Niinemets Ü (2013) Leaf-level models of constitutive and stress-driven volatile organic compound emissions. In: Niinemets Ü, Monson RK (eds) Biology, controls and models of tree volatile organic compound emissions, vol 5, Tree physiology. Springer, Berlin, pp –Google Scholar
  45. Guenther A (2013) Upscaling biogenic volatile compound emissions from leaves to landscapes. In: Niinemets Ü, Monson RK (eds) Biology, controls and models of tree volatile organic compound emissions, vol 5, Tree physiology. Springer, Berlin, pp –Google Scholar
  46. Guenther A, Hewitt CN, Erickson D, Fall R, Geron C, Graedel T, Harley P, Klinger L, Lerdau M, McKay WA, Pierce T, Scholes B, Steinbrecher R, Tallamraju R, Taylor J, Zimmerman P (1995) A global-model of natural volatile organic-compound emissions. J Geophys Res Atmos 100:8873–8892Google Scholar
  47. Guidolotti G, Calfapietra C, Loreto F (2011) The relationship between isoprene emission, CO2 assimilation and water use efficiency across a range of poplar genotypes. Physiol Plant 142:297–304PubMedGoogle Scholar
  48. Hamilton JF, Lewis AC, Carey TJ, Wenger JC, Garcia EBI, Munoz A (2009) Reactive oxidation products promote secondary organic aerosol formation from green leaf volatiles. Atmos Chem Phys 9:3815–3823Google Scholar
  49. Hanson DT, Swanson S, Graham LE, Sharkey TD (1999) Evolutionary significance of isoprene emission from mosses. Am J Bot 86:634–639PubMedGoogle Scholar
  50. Hao LQ, Yli-Pirila P, Tiitta P, Romakkaniemi S, Vaattovaara P, Kajos MK, Rinne J, Heijari J, Kortelainen A, Miettinen P, Kroll JH, Holopainen JK, Smith JN, Joutsensaari J, Kulmala M, Worsnop DR, Laaksonen A (2009) New particle formation from the oxidation of direct emissions of pine seedlings. Atmos Chem Phys 9:8121–8137Google Scholar
  51. Harley PC (2013) The roles of stomatal conductance and compound volatility in controlling the emission of volatile organic compounds from leaves. In: Niinemets Ü, Monson RK (eds) Biology, controls and models of tree volatile organic compound emissions, vol 5, Tree physiology. Springer, Berlin, pp –Google Scholar
  52. Harley P, Greenberg J, Niinemets Ü, Guenther A (2007) Environmental controls over methanol emission from leaves. Biogeosciences 4:1083–1099Google Scholar
  53. Hastings A, Byers JE, Crooks JA, Cuddington K, Jones CG, Lambrinos JG, Talley TS, Wilson WG (2007) Ecosystem engineering in space and time. Ecol Lett 10:153–164PubMedGoogle Scholar
  54. Holopainen JK (2011) Can forest trees compensate for stress-generated growth losses by induced production of volatile compounds? Tree Physiol 31:1356–1377PubMedGoogle Scholar
  55. Holopainen JK, Nerg A-M, Blande JD (2013) Multitrophic signalling in polluted atmospheres. In: Niinemets Ü, Monson RK (eds) Biology, controls and models of tree volatile organic compound emissions, vol 5, Tree physiology. Springer, Berlin, pp –Google Scholar
  56. Ibrahim MA, Mäenpää M, Hassinen V, Kontunen-Soppela S, Malec L, Rousi M, Pietikainen L, Tervahauta A, Kärenlampi S, Holopainen JK, Oksanen EJ (2010) Elevation of night-time temperature increases terpenoid emissions from Betula pendula and Populus tremula. J Exp Bot 61:1583–1595PubMedGoogle Scholar
  57. Jardine KJ, Monson RK, Abrell L, Saleska SR, Arneth A, Jardine A, Ishida FY, Maria A, Serrano Y, Artaxo P, Karl T, Fares S, Goldstein A, Loreto F, Huxman T (2011) Within-plant isoprene oxidation confirmed by direct emissions of oxidation products methyl vinyl ketone and methacrolein. Glob Change Biol 18:973–984Google Scholar
  58. Jelali N, Dhifi W, Chahed T, Marzouk B (2011) Salinity effects on growth, essential oil yield and composition and phenolic compounds content of marjoram (Origanum majorana L.) leaves. J Food Biochem 35(5):1443–1450. doi: 10.1111/j.1745-4514.2010.00465.x Google Scholar
  59. Joutsensaari J, Loivamäki M, Vuorinen T, Miettinen P, Nerg A-M, Holopainen JK, Laaksonen A (2005) Nanoparticle formation by ozonolysis of inducible plant volatiles. Atmos Chem Phys 5:1489–1495Google Scholar
  60. Keppler F, Hamilton JTG, McRoberts WC, Vigano I, Brass M, Rockmann T (2008) Methoxyl groups of plant pectin as a precursor of atmospheric methane: evidence from deuterium labelling studies. New Phytol 178:808–814PubMedGoogle Scholar
  61. Kesselmeier J, Staudt M (1999) Biogenic volatile organic compounds (VOC): An overview on emission, physiology and ecology. J Atmos Chem 33:23–88Google Scholar
  62. Kiendler-Scharr A, Zhang Q, Hohaus T, Kleist E, Mensah A, Mentel TF, Spindler C, Uerlings R, Tillmann R, Wildt J (2009) Aerosol mass spectrometric features of biogenic SOA: observations from a plant chamber and in rural atmospheric environments. Environ Sci Technol 43:8166–8172PubMedGoogle Scholar
  63. Knudsen JT, Gershenzon J (2006) The chemical diversity of floral scent. In: Dudareva N, Pichersky E (eds) Biology of floral scent. Taylor & Francis, New York, pp 27–52Google Scholar
  64. Knudsen JT, Tollsten L, Bergstrom LG (1993) Floral scents – a checklist of volatile compounds isolated by headspace techniques. Phytochemistry 33:253–280Google Scholar
  65. Kreuzwieser J, Rennenberg H (2013) Flooding-driven emissions from trees. In: Niinemets Ü, Monson RK (eds) Biology, controls and models of tree volatile organic compound emissions, vol 5, Tree physiology. Springer, Berlin, pp –Google Scholar
  66. Kreuzwieser J, Scheerer U, Rennenberg H (1999) Metabolic origin of acetaldehyde emitted by poplar (Populus tremula x P. alba) trees. J. Exp. Bot. 50:757–765Google Scholar
  67. Kulmala M, Nieminen T, Chellapermal R, Makkonen R, Bäck J, Kerminen V-M (2013) Climate feedbacks linking the increasing atmospheric CO2 concentration, BVOC emissions, aerosols and clouds in forest ecosystems. In: Niinemets Ü, Monson RK (eds) Biology, controls and models of tree volatile organic compound emissions, vol 5, Tree physiology. Springer, Berlin, pp –Google Scholar
  68. Lamattina L, Garcia-Mata C, Graziano M, Pagnussat G (2003) Nitric oxide: the versatility of an extensive signal molecule. Annu Rev Plant Biol 54:109–136PubMedGoogle Scholar
  69. Laothawornkitkul J, Paul ND, Vickers CE, Possell M, Taylor JE, Mullineaux PM, Hewitt CN (2008) Isoprene emissions influence herbivore feeding decisions. Plant Cell Environ 31:1410–1415PubMedGoogle Scholar
  70. Lerdau M (2007) A positive feedback with negative consequences. Science 316:212–213PubMedGoogle Scholar
  71. Li Z, Sharkey TD (2013a) Metabolic profiling of the methylerythritol phosphate pathway reveals the source of post-illumination isoprene burst from leaves. Plant Cell Environ 36:429–437. doi: 10.1111/j.1365-3040.2012.02584.x Google Scholar
  72. Li Z, Sharkey TD (2013b) Molecular and pathway controls on biogenic volatile organic compound emissions. In: Niinemets Ü, Monson RK (eds) Biology, controls and models of tree volatile organic compound emissions, vol 5, Tree physiology. Springer, Berlin, pp –Google Scholar
  73. Lichtenthaler HK (2010) Biosynthesis and emission of isoprene, methylbutenol and other volatile plant isoprenoids. In: Herrman A (ed) The chemistry and biology of volatiles. Wiley, Chichester, pp 11–47Google Scholar
  74. Lin ZF, Zhong SL, Grierson D (2009) Recent advances in ethylene research. J. Exp. Bot. 60:3311–3336Google Scholar
  75. Llusià J, Peñuelas J, Alessio GA, Estiarte M (2006) Seasonal contrasting changes of foliar concentrations of terpenes and other volatile organic compound in four dominant species of a Mediterranean shrubland submitted to a field experimental drought and warming. Physiol Plant 127(4):632–649. doi: 10.1111/j.1399-3054.2006.00693.x Google Scholar
  76. Llusià J, Peñuelas J, Alessio GA, Estiarte M (2008) Contrasting species-specific, compound-specific, seasonal, and interannual responses of foliar isoprenoid emissions to experimental drought in a Mediterranean shrubland. Int J Plant Sci 169(5):637–645. doi: 10.1086/533603 Google Scholar
  77. Logan BA, Anchordoquy TJ, Monson RK, Pan RS (1999) The effect of isoprene on the properties of spinach thylakoids and phosphatidylcholine liposomes. Plant Biol 1(6):602–606. doi: 10.1055/s-2007-978561 Google Scholar
  78. Loreto F (2002) Distribution of isoprenoid emitters in the Quercus genus around the world: chemo-taxonomical implications and evolutionary considerations based on the ecological function of the trait. Perspect Plant Ecol Evol Syst 5:185–192Google Scholar
  79. Loreto F, Delfine S (2000) Emission of isoprene from salt-stressed Eucalyptus globulus leaves. Plant Physiol 123:1605–1610PubMedGoogle Scholar
  80. Loreto F, Schnitzler J-P (2010) Abiotic stresses and induced BVOCs. Trends Plant Sci 15:154–166PubMedGoogle Scholar
  81. Loreto F, Velikova V (2001) Isoprene produced by leaves protects the photosynthetic apparatus against ozone damage, quenches ozone products, and reduces lipid peroxidation of cellular membranes. Plant Physiol 127:1781–1787PubMedGoogle Scholar
  82. Loreto F, Forster A, Durr M, Csiky O, Seufert G (1998) On the monoterpene emission under heat stress and on the increased thermotolerance of leaves of Quercus ilex L. fumigated with selected monoterpenes. Plant Cell Environ 21:101–107Google Scholar
  83. Loreto F, Pinelli P, Brancaleoni E, Ciccioli P (2004a) 13C labelling reveals chloroplastic and extrachloroplastic pools of dimethylallyl pyrophosphate and their contribution to isoprene formation. Plant Physiol 135:1903–1907PubMedGoogle Scholar
  84. Loreto F, Pinelli P, Manes F, Kollist H (2004b) Impact of ozone on monoterpene emissions and evidence for an isoprene-like antioxidant action of monoterpenes emitted by Quercus ilex leaves. Tree Physiol 24:361–367PubMedGoogle Scholar
  85. Loreto F, Barta C, Brilli F, Nogues I (2006) On the induction of volatile organic compound emissions by plants as consequence of wounding or fluctuations of light and temperature. Plant Cell Environ 29:1820–1828PubMedGoogle Scholar
  86. Magel E, Mayrhofer S, Müller A, Zimmer I, Hampp R, Schnitzler J-P (2006) Photosynthesis and substrate supply for isoprene biosynthesis in poplar leaves. Atmos Environ 40:S138–S151Google Scholar
  87. Mayrhofer S, Teuber M, Zimmer I, Louis S, Fischbach RJ, Schnitzler RP (2005) Diurnal and seasonal variation of isoprene biosynthesis-related genes in grey poplar leaves. Plant Physiol 139:474–484PubMedGoogle Scholar
  88. Mentel TF, Wildt J, Kiendler-Scharr A, Kleist E, Tillmann R, Dal Maso M, Fisseha R, Hohaus T, Spahn H, Uerlings R, Wegener R, Griffiths PT, Dinar E, Rudich Y, Wahner A (2009) Photochemical production of aerosols from real plant emissions. Atmos Chem Phys 9:4387–4406Google Scholar
  89. Mittler R (2006) Abiotic stress, the field environment and stress combination. Trends Plant Sci 11:15–19PubMedGoogle Scholar
  90. Mongelard G, Seemann M, Boisson AM, Rohmer M, Bligny R, Rivasseau C (2011) Measurement of carbon flux through the MEP pathway for isoprenoid synthesis by 31P-NMR spectroscopy after specific inhibition of 2-C-methyl-D-erythritol 2,4-cyclodiphosphate reductase. Effect of light and temperature. Plant Cell Environ 34(8):1241–1247. doi: 10.1111/j.1365-3040.2011.02322.x PubMedGoogle Scholar
  91. Monson RK (2013) Metabolic and gene expression controls on the production of biogenic volatile organic compounds. In: Niinemets Ü, Monson RK (eds) Biology, controls and models of tree volatile organic compound emissions, vol 5, Tree physiology. Springer, Berlin, pp –Google Scholar
  92. Monson RK, Jones RT, Rosenstiel TN, Schnitzler J-P (2013) Why only some plants emit isoprene. Plant Cell Environ 36:503–516. doi: 10.1111/pce.12015 PubMedGoogle Scholar
  93. Niinemets Ü (2010a) Mild versus severe stress and BVOCs: thresholds, priming and consequences. Trends Plant Sci 15:145–153PubMedGoogle Scholar
  94. Niinemets Ü (2010b) Responses of forest trees to single and multiple environmental stresses from seedlings to mature plants: past stress history, stress interactions, tolerance and acclimation. For Ecol Manage 260:1623–1639Google Scholar
  95. Niinemets Ü, Reichstein M (2003) Controls on the emission of plant volatiles through stomata: sensitivity or insensitivity of the emission rates to stomatal closure explained. J Geophys Res Atmos 108:4208. doi: 4210.1029/2002JD002620Google Scholar
  96. Niinemets Ü, Reichstein M, Staudt M, Seufert G, Tenhunen JD (2002) Stomatal constraints may affect emission of oxygenated monoterpenoids from the foliage of Pinus pinea. Plant Physiol 130:1371–1385PubMedGoogle Scholar
  97. Niinemets Ü, Loreto F, Reichstein M (2004) Physiological and physico-chemical controls on foliar volatile organic compound emissions. Trends Plant Sci 9:180–186PubMedGoogle Scholar
  98. Niinemets Ü, Monson RK, Arneth A, Ciccioli P, Kesselmeier J, Kuhn U, Noe SM, Peñuelas J, Staudt M (2010a) The leaf-level emission factor of volatile isoprenoids: caveats, model algorithms, response shapes and scaling. Biogeosciences 7:1809–1832Google Scholar
  99. Niinemets Ü, Arneth A, Kuhn U, Monson RK, Peñuelas J, Staudt M (2010b) The emission factor of volatile isoprenoids: stress, acclimation, and developmental responses. Biogeosciences 7:2203–2223Google Scholar
  100. O’Dowd CD, Aalto P, Hameri K, Kulmala M, Hoffmann T (2002) Aerosol formation – atmospheric particles from organic vapours. Nature 416:497–498PubMedGoogle Scholar
  101. Ormeño E, Mevy JP, Vila B, Bousquet-Melou A, Greff S, Bonin G, Fernandez C (2007) Water deficit stress induces different monoterpene and sesquiterpene emission changes in Mediterranean species. Relationship between terpene emissions and plant water potential. Chemosphere 67:276–284PubMedGoogle Scholar
  102. Ourisson G, Nakatani Y (1994) The terpenoid theory of the origin of cellular life: the evolution of terpenoids to cholesterol. Chem Biol 1:11–23PubMedGoogle Scholar
  103. Pegoraro E, Rey A, Greenberg J, Harley P, Grace J, Malhi Y, Guenther A (2004) Effect of drought on isoprene emission rates from leaves of Quercus virginiana Mill. Atmos Environ 38:6149–6156Google Scholar
  104. Peñuelas J, Llusià J (2003) BVOCs: plant defense against climate warming? Trends Plant Sci 8:105–109PubMedGoogle Scholar
  105. Peñuelas J, Staudt M (2010) BVOCs and global change. Trends Plant Sci 15:133–144PubMedGoogle Scholar
  106. Peñuelas J, Filella I, Seco R, Llusià J (2009) Increase in isoprene and monoterpene emissions after re-watering of droughted Quercus ilex seedlings. Biol Plant 53:351–354Google Scholar
  107. Petron G, Harley P, Greenberg J, Guenther A (2001) Seasonal temperature variations influence isoprene emission. Geophys Res Lett 28:1707–1710Google Scholar
  108. Pinto DM, Blande JD, Nykanen R, Dong W-X, Nerg A-M, Holopainen JK (2007) Ozone degrades common herbivore-induced plant volatiles: Does this affect herbivore prey location by predators and parasitoids? J Chem Ecol 33:683–694PubMedGoogle Scholar
  109. Possell M, Hewitt CN (2011) Isoprene emissions from plants are mediated by atmospheric CO2 concentrations. Global Change Biol 17:1595–1610Google Scholar
  110. Possell M, Heath J, Nicholas Hewitt C, Ayres E, Kerstiens G (2004) Interactive effects of elevated CO2 and soil fertility on isoprene emissions from Quercus robur. Global Change Biol 10:1835–1843Google Scholar
  111. Possell M, Ryan A, Vickers CE, Mullineaux PM, Hewitt CN (2010) Effects of fosmidomycin on plant photosynthesis as measured by gas exchange and chlorophyll fluorescence. Photosynth Res 104:49–59PubMedGoogle Scholar
  112. Rajabi Memari H, Pazouki L, Niinemets Ü (2013) The biochemistry and molecular biology of volatile messengers in trees. In: Niinemets Ü, Monson RK (eds) Biology, controls and models of tree volatile organic compound emissions, vol 5, Tree physiology. Springer, Berlin, pp –Google Scholar
  113. Ramanathan V, Ramana MV, Roberts G, Kim D, Corrigan C, Chung C, Winker D (2007) Warming trends in Asia amplified by brown cloud solar absorption. Nature 448:575–578PubMedGoogle Scholar
  114. Rasulov B, Copolovici L, Laisk A, Niinemets Ü (2009a) Postillumination isoprene emission: in vivo measurements of dimethylallyldiphosphate pool size and isoprene synthase kinetics in aspen leaves. Plant Physiol 149(3):1609–1618. doi: 10.1104/pp. 108.133512PubMedGoogle Scholar
  115. Rasulov B, Hüve K, Välbe M, Laisk A, Niinemets Ü (2009b) Evidence that light, carbon dioxide and oxygen dependencies of leaf isoprene emission are driven by energy status in hybrid aspen. Plant Physiol 151:448–460PubMedGoogle Scholar
  116. Rasulov B, Hüve K, Bichele I, Laisk A, Niinemets Ü (2010) Temperature response of isoprene emission in vivo reflects a combined effect of substrate limitations and isoprene synthase activity: a kinetic analysis. Plant Physiol 154:1558–1570PubMedGoogle Scholar
  117. Rivasseau C, Seemann M, Boisson AM, Streb P, Gout E, Douce R, Rohmer M, Bligny R (2009) Accumulation of 2-C-methyl-D-erythritol 2,4-cyclodiphosphate in illuminated plant leaves at supraoptimal temperatures reveals a bottleneck of the prokaryotic methylerythritol 4-phosphate pathway of isoprenoid biosynthesis. Plant Cell Environ 32(1):82–92. doi: 10.1111/j.1365-3040.2008.01903.x PubMedGoogle Scholar
  118. Roderick ML, Farquhar GD, Berry SL, Noble IR (2001) On the direct effect of clouds and atmospheric particles on the productivity and structure of vegetation. Oecologia 129:21–30Google Scholar
  119. Rosenkranz M, Schnitzler J-P (2013) Genetic engineering of BVOC emissions from trees. In: Niinemets Ü, Monson RK (eds) Biology, controls and models of tree volatile organic compound emissions, vol 5, Tree physiology. Springer, Berlin, pp –Google Scholar
  120. Rosenstiel TN, Ebbets AL, Khatri WC, Fall R, Monson RK (2004) Induction of poplar leaf nitrate reductase: a test of extrachloroplastic control of isoprene emission rate. Plant Biol 6:12–21PubMedGoogle Scholar
  121. Santos LS, Dalmazio I, Eberlin MN, Claeys M, Augusti R (2006) Mimicking the atmospheric OH-radical-mediated photooxidation of isoprene: formation of cloud-condensation nuclei polyols monitored by electrospray ionization mass spectrometry. Rapid Commun Mass Spectrom 20:2104–2108PubMedGoogle Scholar
  122. Sasaki K, Saito T, Laemsae M, Oksman-Caldentey K-M, Suzuki M, Ohyama K, Muranaka T, Ohara K, Yazaki K (2007) Plants utilize isoprene emission as a thermotolerance mechanism. Plant Cell Physiol 48:1254–1262PubMedGoogle Scholar
  123. Schade GW, Goldstein AH (2001) Fluxes of oxygenated volatile organic compounds from a ponderosa pine plantation. J Geophys Res Atmos 106:3111–3123Google Scholar
  124. Schnitzler J-P, Graus M, Kreuzwieser J, Heizmann U, Rennenberg H, Wisthaler A, Hansel A (2004) Contribution of different carbon sources to isoprene biosynthesis in poplar leaves. Plant Physiol 135:152–160PubMedGoogle Scholar
  125. Scholefield PA, Doick KJ, Herbert BMJ, Hewitt CNS, Schnitzler J-P, Pinelli P, Loreto F (2004) Impact of rising CO2 on emissions of volatile organic compounds: isoprene emission from Phragmites australis growing at elevated CO2 in a natural carbon dioxide spring. Plant Cell Environ 27:393–401Google Scholar
  126. Sharkey TD, Loreto F (1993) Water-stress, temperature, and light effects on the capacity for isoprene emission and photosynthesis of kudzu leaves. Oecologia 95:328–333Google Scholar
  127. Sharkey TD, Singsaas EL (1995) Why plants emit isoprene. Nature 374:769Google Scholar
  128. Sharkey TD, Yeh SS (2001) Isoprene emission from plants. Annu Rev Plant Physiol Plant Mol Biol 52:407–436PubMedGoogle Scholar
  129. Sharkey TD, Singsaas EL, Vanderveer PJ, Geron C (1996) Field measurements of isoprene emission from trees in response to temperature and light. Tree Physiol 16:649–654PubMedGoogle Scholar
  130. Sharkey TD, Singsaas EL, Lerdau MT, Geron CD (1999) Weather effects on isoprene emission capacity and applications in emissions algorithms. Ecol Appl 9:1132–1137Google Scholar
  131. Sharkey TD, Chen XY, Yeh S (2001) Isoprene increases thermotolerance of fosmidomycin-fed leaves. Plant Physiol 125:2001–2006PubMedGoogle Scholar
  132. Sharkey TD, Wiberley AE, Donohue AR (2008) Isoprene emission from plants: why and how. Ann Bot 101:5–18PubMedGoogle Scholar
  133. Šimpraga M, Verbeeck H, Demarcke M, Joó E, Pokorska O, Amelynck C, Schoon N, Dewulf J, Van Langenhove H, Heinesch B, Aubinet M, Laffineur Q, Müller JF, Steppe K (2011) Clear link between drought stress, photosynthesis and biogenic volatile organic compounds in Fagus sylvatica L. Atmos Environ 45:5254–5259Google Scholar
  134. Singh HB, Salas LJ, Chatfield RB, Czech E, Fried A, Walega J, Evans MJ, Field BD, Jacob DJ, Blake D, Heikes B, Talbot R, Sachse G, Crawford JH, Avery MA, Sandholm S, Fuelberg H (2004) Analysis of the atmospheric distribution, sources, and sinks of oxygenated volatile organic chemicals based on measurements over the Pacific during TRACE-P. J Geophys Res-Atmos 109: D15S07. doi: 10.1029/2003JD003883
  135. Singsaas EL, Sharkey TD (1998) The regulation of isoprene emission responses to rapid leaf temperature fluctuations. Plant Cell Environ 21:1181–1188Google Scholar
  136. Singsaas EL, Sharkey TD (2000) The effects of high temperature on isoprene synthesis in oak leaves. Plant Cell Environ 23:751–757Google Scholar
  137. Singsaas EL, Lerdau M, Winter K, Sharkey TD (1997) Isoprene increases thermotolerance of isoprene-emitting species. Plant Physiol 115(4):1413–1420PubMedGoogle Scholar
  138. Singsaas EL, Laporte MM, Shi JZ, Monson RK, Bowling DR, Johnson K, Lerdau M, Jasentuliytana A, Sharkey TD (1999) Kinetics of leaf temperature fluctuation affect isoprene emission from red oak (Quercus rubra) leaves. Tree Physiol 19:917–924PubMedGoogle Scholar
  139. Siwko ME, Marrink SJ, de Vries AH, Kozubek A, Uiterkamp AJMS, Mark AE (2007) Does isoprene protect plant membranes from thermal shock? A molecular dynamics study. Biochim Biophys Acta-Biomembr 1768:198–206Google Scholar
  140. Spracklen DV, Bonn B, Carslaw KS (2008) Boreal forests, aerosols and the impacts on clouds and climate. Philos Trans R Soc A-Math Phys Eng Sci 366:4613–4626Google Scholar
  141. Staudt M, Bertin N (1998) Light and temperature dependence of the emission of cyclic and acyclic monoterpenes from holm oak (Quercus ilex L.) leaves. Plant Cell Environ 21:385–395Google Scholar
  142. Staudt M, Rambal S, Joffre R, Kesselmeier J (2002) Impact of drought on seasonal monoterpene emissions from Quercus ilex in southern France. J Geophys Res-Atmos 107: 4602. doi: 10.1029/2001JD002043
  143. Sun Z, Niinemets Ü, Hüve K, Noe SM, Rasulov B, Copolovici L, Vislap V (2012) Enhanced isoprene emission capacity and altered light responsiveness in aspen grown under elevated atmospheric CO2 concentration. Glob Change Biol 18:3423–3440Google Scholar
  144. Teuber M, Zimmer I, Kreuzwieser J, Ache P, Polle A, Rennenberg H, Schnitzler J-P (2008) VOC emissions of grey poplar leaves as affected by salt stress and different N sources. Plant Biol 10:86–96PubMedGoogle Scholar
  145. Tholl D, Boland W, Hansel A, Loreto F, Rose USR, Schnitzler J-P (2006) Practical approaches to plant volatile analysis. Plant J 45:540–560PubMedGoogle Scholar
  146. Tingey DT, Evans RC, Bates EH, Gumpertz ML (1987) Isoprene emissions and photosynthesis in three ferns – the influence of light and temperature. Physiol Plant 69:609–616Google Scholar
  147. Tunved P, Hansson HC, Kerminen VM, Strom J, Dal Maso M, Lihavainen H, Viisanen Y, Aalto PP, Komppula M, Kulmala M (2006) High natural aerosol loading over boreal forests. Science 312:261–263PubMedGoogle Scholar
  148. Velikova V, Loreto F (2005) On the relationship between isoprene emission and thermotolerance in Phragmites australis leaves exposed to high temperatures and during the recovery from a heat stress. Plant Cell Environ 28:318–327Google Scholar
  149. Velikova V, Edreva A, Loreto F (2004) Endogenous isoprene protects Phragmites australis leaves against singlet oxygen. Physiol Plant 122:219–225Google Scholar
  150. Velikova V, Tsonev T, Pinelli P, Alessio GA, Loreto F (2005a) Localized ozone fumigation system for studying ozone effects on photosynthesis, respiration, electron transport rate and isoprene emission in field-grown Mediterranean oak species. Tree Physiol 25:1523–1532PubMedGoogle Scholar
  151. Velikova V, Pinelli P, Pasqualini S, Reale L, Ferranti F, Loreto F (2005b) Isoprene decreases the concentration of nitric oxide in leaves exposed to elevated ozone. New Phytol 166:419–426PubMedGoogle Scholar
  152. Velikova V, Loreto F, Tsonev T, Brilli F, Edreva A (2006) Isoprene prevents the negative consequences of high temperature stress in Platanus orientalis leaves. Funct Plant Biol 33:931–940Google Scholar
  153. Velikova V, Fares S, Loreto F (2008) Isoprene and nitric oxide reduce damages in leaves exposed to oxidative stress. Plant Cell Environ 31:1882–1894PubMedGoogle Scholar
  154. Velikova V, Várkonyi Z, Szabó M, Maslenkova L, Nogues I, Kovács L, Peeva V, Busheva M, Garab G, Sharkey TD, Loreto F (2011) Increased thermostability of thylakoid membranes in isoprene-emitting leaves probed with three biophysical techniques. Plant Physiol 157:905–916PubMedGoogle Scholar
  155. Velikova V, Sharkey TD, Loreto F (2012) Stabilization of thylakoid membranes in isoprene-emitting plants reduces formation of reactive oxygen species. Plant Signal Behav 7:139–141PubMedGoogle Scholar
  156. Vickers CE, Gershenzon J, Lerdau MT, Loreto F (2009a) A unified mechanism of action for volatile isoprenoids in plant abiotic stress. Nat Chem Biol 5:283–291PubMedGoogle Scholar
  157. Vickers CE, Possell M, Cojocariu CI, Velikova VB, Laothawornkitkul J, Ryan A, Mullineaux PM, Hewitt CN (2009b) Isoprene synthesis protects transgenic tobacco plants from oxidative stress. Plant Cell Environ 32:520–531PubMedGoogle Scholar
  158. Vickers CE, Possell M, Hewitt CN, Mullineaux PM (2010) Genetic structure and regulation of isoprene synthase in poplar (Populus spp.). Plant Mol Biol 73:547–558PubMedGoogle Scholar
  159. Vickers CE, Possell M, Laothawornkitkul J, Ryan AC, Hewitt CN, Mullineaux PM (2011) Isoprene synthesis in plants: lessons from a transgenic tobacco model. Plant Cell Environ 34:1043–1053PubMedGoogle Scholar
  160. Virtanen A, Joutsensaari J, Koop T, Kannosto J, Yli-Pirila P, Leskinen J, Mäkela JM, Holopainen JK, Pöschl U, Kulmala M, Worsnop DR, Laaksonen A (2010) An amorphous solid state of biogenic secondary organic aerosol particles. Nature 467:824–827PubMedGoogle Scholar
  161. Visser EJW, Voesenek L, Vartapetian BB, Jackson MB (2003) Flooding and plant growth. Ann Bot 91(2):107–109. doi: 10.1093/aob/mcg014 Google Scholar
  162. Way DA, Schnitzler J-P, Monson RK, Jackson RB (2011) Enhanced isoprene-related tolerance of heat- and light-stressed photosynthesis at low, but not high, CO2 concentrations. Oecologia 166:273–282PubMedGoogle Scholar
  163. Went FW (1960) Blue hazes in the atmosphere. Nature 187:641–643Google Scholar
  164. Wiberley AE, Linskey AR, Falbel TG, Sharkey TD (2005) Development of the capacity for isoprene emission in kudzu. Plant Cell Environ 28:898–905Google Scholar
  165. Wiedinmyer C, Guenther A, Harley P, Hewitt CN, Geron C, Artaxo P, Steinbrecher R, Rasmussen R (2004) Global organic emissions from vegetation. In: Granier C, Artaxo P, Reeves CE (eds) Emission of atmospheric trace compounds. Kluwers Academic Publishers, Dordrecht, pp 115–170Google Scholar
  166. Wilson ID, Neill SJ, Hancock JT (2008) Nitric oxide synthesis and signaling in plants. Plant Cell Environ 31:622–631PubMedGoogle Scholar
  167. Yordanova RY, Christov KN, Popova LP (2004) Antioxidative enzymes in barley plants subjected to soil flooding. Environ Exp Bot 51(2):93–101. doi: 10.1016/s0098-8472(03)00063-7 Google Scholar
  168. Zhang R, Cruz JA, Kramer DM, Magallanes-Lundback ME, Dellapenna D, Sharkey TD (2009) Moderate heat stress reduces the pH component of the transthylakoid proton motive force in light-adapted, intact tobacco leaves. Plant Cell Environ 32:1538–1547PubMedGoogle Scholar

Copyright information

© Springer Science+Business Media Dordrecht 2013

Authors and Affiliations

  1. 1.Faculty of Agriculture and EnvironmentUniversity of SydneySydneyAustralia
  2. 2.Istituto per la Protezione delle Piante (IPP), Consiglio Nazionale delle Ricerche (CNR)Sesto FiorentinoItaly

Personalised recommendations