What Are Plant-Released Biogenic Volatiles and How They Participate in Landscape- to Global-Level Processes?

  • Ülo NiinemetsEmail author


Plants face a multitude of abiotic and biotic stresses with varying severity throughout their life, and these stresses can result in varying changes to the ecosystem services provided by the plants. Climate change involves modification of several environmental drivers, and it is predicted to increase the frequency and severity of various abiotic and biotic stresses, including rising temperatures, increasingly uneven distribution of precipitation, and more frequent outbreaks of herbivore and pathogen attacks. As any stress reduces plant CO2 fixation, enhanced stress frequency and severity are expected to lead to faster rise of atmospheric CO2 concentration, thereby further exacerbating climate change. On the other hand, plants can importantly modify their own life environment by release of volatile organic compounds (BVOC). The plant-generated volatiles modify the oxidative status of the ambient atmosphere by enhancing the rate of ozone formation in atmospheres polluted by mono-nitrogen oxides (NOx). From this perspective, plant emissions can be considered as ecosystem “disservice.” Plant-emitted volatiles also importantly participate in aerosol and cloud formation in both polluted and non-polluted atmospheres, thereby reducing solar radiation penetration and ambient temperature. Plant-facilitated cooling can partly counteract global warming, and thus, plant emissions provide an important global regulatory ecosystem service. Apart from constitutive volatile emissions that are present in only some species and are expected to decrease under stress, especially under severe stress, all plants respond to stresses by inducing BVOC emissions that serve as signal molecules eliciting stress response pathways and leading to plant acclimation. These induced BVOC emissions, the plant “talk,” also contribute to atmospheric processes and can potentially reduce the stress severity, and, accordingly, stress-driven reductions in CO2 uptake. Thus, the stress responses and acclimation of vegetation to future environmental stresses can importantly modify the speed and magnitude of climate change.


Constitutive Emissions Climate Change Induced Emissions Global Feedbacks Plant-Biosphere Relationships Stress Terpenoids Volatile Organic Compounds 



I thank Prof. Josep Peñuelas (Global Ecology Unit CREAF-CSIC-UAB, Barcelona, Catalonia) and Dr. Trevor F. Keenan (Earth and Environmental Sciences, Lawrence Berkeley National Lab, USA) for insightful comments on the MS. My work on plant volatiles has been supported by the Estonian Ministry of Science and Education (institutional grant IUT-8-3) and the European Commission through the European Research Council (advanced grant 322603, SIP-VOL+) and the European Regional Development Fund (Centre of Excellence EcolChange, TK 131).


  1. Achotegui-Castells A, Danti R, Llusià J, Della Rocca G, Barberini S, Peñuelas J (2015) Strong induction of minor terpenes in Italian cypress, Cupressus sempervirens, in response to infection by the fungus Seiridium cardinale. J Chem Ecol 41:224–243PubMedCrossRefGoogle Scholar
  2. Altieri M, Nicholls C (2004) Biodiversity and pest management in agroecosystems, 2nd edn. Food Products Press, New YorkGoogle Scholar
  3. Andreou A, Feussner I (2009) Lipoxygenases – structure and reaction mechanism. Phytochemistry 70:1504–1510PubMedCrossRefGoogle Scholar
  4. Arneth A, Niinemets Ü (2010) Induced BVOCs: how to bug our models? Trends Plant Sci 15:118–125PubMedCrossRefGoogle Scholar
  5. Arneth A, Monson RK, Schurgers G, Niinemets Ü, Palmer PI (2008) Why are estimates of global isoprene emissions so similar (and why is this not so for monoterpenes)? Atmos Chem Phys 8:4605–4620CrossRefGoogle Scholar
  6. Arneth A, Unger N, Kulmala M, Andreae MO (2009) Clean the air, heat the planet? Science 326:672–673PubMedCrossRefGoogle Scholar
  7. 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, Tree physiology, vol 5. Springer, Berlin, pp 451–487CrossRefGoogle Scholar
  8. Atkinson R, Arey J (2003) Gas-phase tropospheric chemistry of biogenic volatile organic compounds: a review. Atmos Environ 37:197–219CrossRefGoogle Scholar
  9. 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 28:1334–1343CrossRefGoogle Scholar
  10. Blanch J-S, Peñuelas J, Llusià J (2007) Sensitivity of terpene emissions to drought and fertilization in terpene-storing Pinus halepensis and non-storing Quercus ilex. Physiol Plant 131:211–225PubMedGoogle Scholar
  11. Blanch J-S, Peñuelas J, Sardans J, Llusià J (2009) Drought, warming and soil fertilization effects on leaf volatile terpene concentrations in Pinus halepensis and Quercus ilex. Acta Physiol Plant 31:207–218CrossRefGoogle Scholar
  12. Blanch J-S, Llusià J, Niinemets Ü, Noe SM, Peñuelas J (2011) Instantaneous and historical temperature effects on α-pinene emissions in Pinus halepensis and Quercus ilex. J Environ Biol 32:1–6PubMedGoogle Scholar
  13. Blande JD, Tiiva P, Oksanen E, Holopainen JK (2007) Emission of herbivore-induced volatile terpenoids from two hybrid aspen (Populus tremula x tremuloides) clones under ambient and elevated ozone concentrations in the field. Glob Chang Biol 13:2538–2550CrossRefGoogle Scholar
  14. Blande JD, Holopainen JK, Niinemets Ü (2014) Plant volatiles in polluted atmospheres: stress responses and signal degradation. Plant Cell Environ 37:1892–1904PubMedPubMedCentralCrossRefGoogle Scholar
  15. Bracho Nunez A, Knothe N, Liberato MAR, Schebeske G, Ciccioli P, Piedade MTF, Kesselmeier J (2009) Flooding effects on plant physiology and VOC emissions from Amazonian tree species from two different flooding environments: Varzea and Igapo. Geophys Res Abstr 11:EGU2009–EGU1497Google Scholar
  16. 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, Tree physiology, vol 5. Springer, Berlin, pp 253–284CrossRefGoogle Scholar
  17. Calogirou A, Larsen BR, Brussol C, Duane M, Kotzias D (1996) Decomposition of terpenes by ozone during sampling on Tenax. Anal Chem 68:1499–1506PubMedCrossRefGoogle Scholar
  18. Cescatti A, Niinemets Ü (2004) Sunlight capture. Leaf to landscape. In: Smith WK, Vogelmann TC, Chritchley C (eds) Photosynthetic adaptation. Chloroplast to landscape, Ecological studies, vol 178. Springer, Berlin, pp 42–85Google Scholar
  19. Chakraborty S (2013) Migrate or evolve: options for plant pathogens under climate change. Glob Chang Biol 19:1985–2000PubMedCrossRefGoogle Scholar
  20. Chameides WL, Fehsenfeld F, Rodgers MO, Cardelino C, Martinez J, Parrish D, Lonneman W, Lawson DR, Rasmussen RA, Zimmerman P, Greenberg J, Middleton P, Wang T (1992) Ozone precursor relationships in the ambient atmosphere. J Geophys Res 97:6037–6055CrossRefGoogle Scholar
  21. Chen X, Hopke PK (2009) A chamber study of secondary organic aerosol formation by linalool ozonolysis. Atmos Environ 43:3935–3940CrossRefGoogle Scholar
  22. Chen F, Tholl D, Bohlmann J, Pichersky E (2011) The family of terpene synthases in plants: a mid-size family of genes for specialized metabolism that is highly diversified throughout the kingdom. Plant J 66:212–229PubMedCrossRefGoogle Scholar
  23. Christianson DW (2008) Unearthing the roots of the terpenome. Curr Opin Chem Biol 12:141–150PubMedPubMedCentralCrossRefGoogle Scholar
  24. Cooter EJ, Rea A, Bruins R, Schwede D, Dennis R (2013) The role of the atmosphere in the provision of ecosystem services. Sci Total Environ 448:197–208PubMedCrossRefGoogle Scholar
  25. Copolovici LO, Niinemets Ü (2005) Temperature dependencies of Henry’s law constants and octanol/water partition coefficients for key plant volatile monoterpenoids. Chemosphere 61:1390–1400PubMedCrossRefGoogle Scholar
  26. Copolovici L, Niinemets Ü (2016) Environmental impacts on plant volatile emission. In: Blande J, Glinwood R (eds) Deciphering chemical language of plant communication, Signaling and communication in plants. Springer International Publishing, Berlin, pp 35–59CrossRefGoogle Scholar
  27. 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 139:485–496PubMedPubMedCentralCrossRefGoogle Scholar
  28. Copolovici L, Kännaste A, Remmel T, Vislap V, Niinemets Ü (2011) Volatile emissions from Alnus glutinosa induced by herbivory are quantitatively related to the extent of damage. J Chem Ecol 37:18–28PubMedCrossRefGoogle Scholar
  29. 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 169:664–672PubMedCrossRefGoogle Scholar
  30. Copolovici L, Kännaste A, Remmel T, Niinemets Ü (2014a) Volatile organic compound emissions from Alnus glutinosa under interacting drought and herbivory stresses. Environ Exp Bot 100:55–63PubMedPubMedCentralCrossRefGoogle Scholar
  31. Copolovici L, Väärtnõu F, Portillo Estrada M, Niinemets Ü (2014b) Oak powdery mildew (Erysiphe alphitoides)-induced volatile emissions scale with the degree of infection in Quercus robur. Tree Physiol 34:1399–1410PubMedPubMedCentralCrossRefGoogle Scholar
  32. D’Alessandro M, Held M, Triponez Y, Turlings TCJ (2006) The role of indole and other shikimic acid derived maize volatiles in the attraction of two parasitic wasps. J Chem Ecol 32:2733–2748PubMedCrossRefGoogle Scholar
  33. 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 158:1008–1014PubMedCrossRefGoogle Scholar
  34. DeLucia EH, Casteel CL, Nabity PD, O’Neill BF (2008) Insects take a bigger bite out of plants in a warmer, higher carbon dioxide world. Proc Natl Acad Sci U S A 105:1781–1782PubMedPubMedCentralCrossRefGoogle Scholar
  35. Dicke M, Baldwin IT (2010) The evolutionary context for herbivore-induced plant volatiles: beyond the ‘cry for help’. Trends Plant Sci 15:167–175PubMedCrossRefGoogle Scholar
  36. Dicke M, van Loon JJA, Soler R (2009) Chemical complexity of volatiles from plants induced by multiple attack. Nat Chem Biol 5:317–324PubMedCrossRefGoogle Scholar
  37. Dindorf T, Kuhn U, Ganzeveld L, Schebeske G, Ciccioli P, Holzke C, Köble R, Seufert G, Kesselmeier J (2006) Significant light and temperature dependent monoterpene emissions from European beech (Fagus sylvatica L.) and their potential impact on the European volatile organic compound budget. J Geophys Res Atmos 111:D16305CrossRefGoogle Scholar
  38. Dong L, Jongedijk E, Bouwmeester H, Van Der Krol A (2016) Monoterpene biosynthesis potential of plant subcellular compartments. New Phytol 209:679–690PubMedCrossRefGoogle Scholar
  39. Ehn M, Thornton JA, Kleist E, Sipilä M, Junninen H, Pullinen I, Springer M, Rubach F, Tillmann R, Lee B, Lopez-Hilfiker F, Andres S, Acir I-H, Rissanen M, Jokinen T, Schobesberger S, Kangasluoma J, Kontkanen J, Nieminen T, Kurtén T, Nielsen LB, Jørgensen S, Kjaergaard HG, Canagaratna M, Dal Maso M, Berndt T, Petäjä T, Wahner A, Kerminen V-M, Kulmala M, Worsnop DR, Wildt J, Mentel TF (2014) A large source of low-volatility secondary organic aerosol. Nature 506:476–479PubMedCrossRefGoogle Scholar
  40. Engelhart GJ, Asa-Awuku A, Nenes A, Pandis SN (2008) CCN activity and droplet growth kinetics of fresh and aged monoterpene secondary organic aerosol. Atmos Chem Phys 8:3937–3949CrossRefGoogle Scholar
  41. Falara V, Akhtar TA, Nguyen TTH, Spyropoulou EA, Bleeker PM, Schauvinhold I, Matsuba Y, Bonini ME, Schilmiller AL, Last RL, Schuurink RC, Pichersky E (2011) The tomato terpene synthase gene family. Plant Physiol 157:770–789PubMedPubMedCentralCrossRefGoogle Scholar
  42. Fall R (2003) Abundant oxygenates in the atmosphere: a biochemical perspective. Chem Rev 103:4941–4952PubMedCrossRefGoogle Scholar
  43. Fall R, Benson AA (1996) Leaf methanol – the simplest natural product from plants. Trends Plant Sci 1:296–301CrossRefGoogle Scholar
  44. Farquhar GD, Roderick ML (2003) Pinatubo, diffuse light, and the carbon cycle. Science 299:1997–1998PubMedCrossRefGoogle Scholar
  45. Farré-Armengol G, Filella I, Llusià J, Primante C, Peñuelas J (2015) Enhanced emissions of floral volatiles by Diplotaxis erucoides (L.) in response to folivory and florivory by Pieris brassicae (L.) Biochem Syst Ecol 63:51–58CrossRefGoogle Scholar
  46. Fehsenfeld F, Calvert J, Fall R, Goldan P, Guenther AB, Hewitt CN, Lamb B, Liu S, Trainer M, Westberg H, Zimmerman P (1992) Emissions of volatile organic compounds from vegetation and the implications for atmospheric chemistry. Glob Biogeochem Cycles 6:389–430CrossRefGoogle Scholar
  47. Field CB, Barros VR, Dokken DJ, Mach KJ, Mastrandrea MD, Bilir TE, Chatterjee M, Ebi KL, Estrada YO, Genova RC, Girma B (eds) (2014) Climate change 2014: impacts, adaptation, and vulnerability. Part A: global and sectoral aspects. Contribution of Working Group II to the fifth assessment report of the Intergovernmental Panel on Climate Change. Cambridge University Press, Cambridge, UK/New York, USAGoogle Scholar
  48. 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, Tree physiology, vol 5. Springer, Berlin, pp 1–20CrossRefGoogle Scholar
  49. Flexas J, Díaz-Espejo A, Conesa MA, Coopman R, Douthe C, Gago J, Gallé A, Galmés J, Medrano H, Ribas-Carbo M, Tomàs M, Niinemets Ü (2016) Mesophyll conductance to CO2 and Rubisco as targets for improving intrinsic water use efficiency in C3 plants. Plant Cell Environ 39:965–982PubMedCrossRefGoogle Scholar
  50. 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 Meteorol Soc 81:1537–1575CrossRefGoogle Scholar
  51. Gray DW, Goldstein AH, Lerdau M (2006) Thermal history regulates methylbutenol basal emission rate in Pinus ponderosa. Plant Cell Environ 29:1298–1308PubMedCrossRefGoogle Scholar
  52. Gray DW, Breneman SR, Topper LA, Sharkey TD (2011) Biochemical characterization and homology modeling of methylbutenol synthase and implications for understanding hemiterpene synthase evolution in plants. J Biol Chem 286:20582–20590PubMedPubMedCentralCrossRefGoogle Scholar
  53. 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, Tree physiology, vol 5. Springer, Berlin, pp 315–355CrossRefGoogle Scholar
  54. Gu L, Baldocchi D, Verma SB, Black TA, Vesala T, Falge EM, Dowty PR (2002) Advantages of diffuse radiation for terrestrial ecosystem productivity. J Geophys Res 107.
  55. Gu L, Baldocchi DD, Wofsy SC, Munger JW, Michalsky JJ, Urbanski SP, Boden TA (2003) Response of a deciduous forest to the Mount Pinatubo eruption: enhanced photosynthesis. Science 299:2035–2038PubMedCrossRefGoogle Scholar
  56. Guenther A (2013a) Biological and chemical diversity of biogenic volatile organic emissions into the atmosphere. ISRN Atmos Sci 2013:786290Google Scholar
  57. Guenther A (2013b) 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, Tree physiology, vol 5. Springer, Berlin, pp 391–414CrossRefGoogle Scholar
  58. Guenther AB, Jiang X, Heald CL, Sakulyanontvittaya T, Duhl T, Emmons LK, Wang X (2012) The model of emissions of gases and aerosols from nature version 2.1 (MEGAN2.1): an extended and updated framework for modeling biogenic emissions. Geosci Model Dev 5:1471–1492CrossRefGoogle Scholar
  59. Gutierrez AP, Ponti L (2014) Analysis of invasive insects: links to climate change. In: Ziska LH, Dukes JS (eds) Invasive species and global climate change. CABI Publishing, Wallingford, pp 45–61Google Scholar
  60. Hantula J, Kurkela T, Hendry S, Yamaguchi T (2009) Morphological measurements and ITS sequences show that the new alder rust in Europe is conspecific with Melampsoridium hiratsukanum in eastern Asia. Mycologia 101:622–631PubMedCrossRefGoogle Scholar
  61. Harley P, Greenberg J, Niinemets Ü, Guenther A (2007) Environmental controls over methanol emission from leaves. Biogeosciences 4:1083–1099CrossRefGoogle Scholar
  62. Hartikainen K, Nerg A-M, Kivimäenpää M, Kontunen-Sopplea S, Mäenpää M, Oksanen E, Rousi M, 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 29:1163–1173PubMedCrossRefGoogle Scholar
  63. Helmig D, Revermann T, Pollmann J, Kaltschmidt O, Hernandez AJ, Bocquet F, David D (2003) Calibration system and analytical considerations for quantitative sesquiterpene measurements in air. J Chromatogr A 1002:193–211PubMedCrossRefGoogle Scholar
  64. Himanen SJ, Blande JD, Klemola T, Pulkkinen J, Heijari J, Holopainen JK (2010) Birch (Betula spp.) leaves adsorb and re-release volatiles specific to neighbouring plants – a mechanism for associational herbivore resistance? New Phytol 186:722–732PubMedCrossRefGoogle Scholar
  65. 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, Tree physiology, vol 5. Springer, Berlin, pp 285–314CrossRefGoogle Scholar
  66. Huang S-H, Cheng C-H, Wu W-J (2010) Possible impacts of climate change on rice insect pests and management tactics in Taiwan. Crop Environ Bioinform 7:269–279Google Scholar
  67. Huff Hartz KE, Rosenørn T, Ferchak SR, Raymond TM, Bilde M, Donahue NM, Pandis SN (2005) Cloud condensation nuclei activation of monoterpene and sesquiterpene secondary organic aerosol. J Geophys Res Atmos 110:D14208,
  68. Hüve K, Christ MM, Kleist E, Uerlings R, Niinemets Ü, Walter A, Wildt J (2007) Simultaneous growth and emission measurements demonstrate an interactive control of methanol release by leaf expansion and stomata. J Exp Bot 58:1783–1793PubMedCrossRefGoogle Scholar
  69. Jacob DJ, Field BD, Li Q, Blake DR, de Gouw J, Warneke C, Hansel A, Wisthaler A, Singh HB, Guenther A (2005) Global budget of methanol: constraints from atmospheric observations. J Geophys Res Atmos 110:D08303,
  70. Jiang Y, Ye J, Li S, Niinemets Ü (2016a) Regulation of floral terpenoid emission and biosynthesis in sweet basil (Ocimum basilicum). J Plant Growth Regul 35:921–935PubMedPubMedCentralCrossRefGoogle Scholar
  71. Jiang Y, Ye J, Veromann L-L, Niinemets Ü (2016b) Scaling of photosynthesis and constitutive and induced volatile emissions with severity of leaf infection by rust fungus (Melampsora larici-populina) in Populus balsamifera var. suaveolens. Tree Physiol 38:856–872CrossRefGoogle Scholar
  72. Karl T, Guenther A, Turnipseed A, Patton EG, Jardine K (2008) Chemical sensing of plant stress at the ecosystem scale. Biogeosciences 5:1287–1294CrossRefGoogle Scholar
  73. Karlik JF, Winer AM (2001) Measured isoprene emission rates of plants in California landscapes: comparison to estimates from taxonomic relationships. Atmos Environ 35:1123–1131CrossRefGoogle Scholar
  74. Kask K, Kännaste A, Talts E, Copolovici L, Niinemets Ü (2016) How specialized volatiles respond to chronic and short-term physiological and shock heat stress in Brassica nigra. Plant Cell Environ 39:2027–2042PubMedPubMedCentralCrossRefGoogle Scholar
  75. Keenan T, Niinemets Ü, Sabate S, Gracia C, Peñuelas J (2009) Process based inventory of isoprenoid emissions from European forests: model comparisons, current knowledge and uncertainties. Atmos Chem Phys 9:4053–4076CrossRefGoogle Scholar
  76. Kirkby J, Duplissy J, Sengupta K, Frege C, Gordon H, Williamson C, Heinritzi M, Simon M, Yan C, Almeida J, Tröstl J, Nieminen T, Ortega IK, Wagner R, Adamov A, Amorim A, Bernhammer A-K, Bianchi F, Breitenlechner M, Brilke S, Chen X, Craven J, Dias A, Ehrhart S, Flagan RC, Franchin A, Fuchs C, Guida R, Hakala J, Hoyle CR, Jokinen T, Junninen H, Kangasluoma J, Kim J, Krapf M, Kürten A, Laaksonen A, Lehtipalo K, Makhmutov V, Mathot S, Molteni U, Onnela A, Peräkylä O, Piel F, Petäjä T, Praplan AP, Pringle K, Rap A, Richards NAD, Riipinen I, Rissanen MP, Rondo L, Sarnela N, Schobesberger S, Scott CE, Seinfeld JH, Sipilä M, Steiner G, Stozhkov Y, Stratmann F, Tomé A, Virtanen A, Vogel AL, Wagner AC, Wagner PE, Weingartner E, Wimmer D, Winkler PM, Ye P, Zhang X, Hansel A, Dommen J, Donahue NM, Worsnop DR, Baltensperger U, Kulmala M, Carslaw KS, Curtius J (2016) Ion-induced nucleation of pure biogenic particles. Nature 533:521–526PubMedCrossRefGoogle Scholar
  77. Kirtman B, Power SB, Adedoyin JA, Boer GJ, Bojariu R, Camilloni I, Doblas-Reyes FJ, Fiore AM, Kimoto M, Meehl GA, Prather M, Sarr A, Schär C, Sutton R, van Oldenborgh GJ, Vecchi G, Wang HJ (2013) Near-term climate change: projections and predictability. In: Stocker TF et al (eds) Climate change 2013: the physical science basis. Contribution of Working Group I to the fifth assessment report of the Intergovernmental Panel on Climate Change. Cambridge University Press, Cambridge, UK/New York, USA, pp 953–1028Google Scholar
  78. Kleist E, Mentel TF, Andres S, Bohne A, Folkers A, Kiendler-Scharr A, Rudich Y, Springer M, Tillmann R, Wildt J (2012) Irreversible impacts of heat on the emissions of monoterpenes, sesquiterpenes, phenolic BVOC and green leaf volatiles from several tree species. Biogeosciences 9:5111–5123CrossRefGoogle Scholar
  79. Kosina J, Dewulf J, Viden I, Pokorska O, Van Langenhove H (2013) Dynamic capillary diffusion system for monoterpene and sesquiterpene calibration: quantitative measurement and determination of physical properties. Int J Environ Anal Chem 93:637–649CrossRefGoogle Scholar
  80. 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, Tree physiology, vol 5. Springer, Berlin, pp 237–252CrossRefGoogle Scholar
  81. Kreuzwieser J, Kühnemann F, Martis A, Rennenberg H, Urban W (2000) Diurnal pattern of acetaldehyde emission by flooded poplar trees. Physiol Plant 108:79–86CrossRefGoogle Scholar
  82. Kreuzwieser J, Harren FJM, Laarhoven LJJ, Boamfa I, te Lintel HS, Scheerer U, Huglin C, Rennenberg H (2001) Acetaldehyde emission by the leaves of trees – correlation with physiological and environmental parameters. Physiol Plant 113:41–49CrossRefGoogle Scholar
  83. Kulmala M, Laakso L, Lehtinen KEJ, Riipinen I, Dal Maso M, Anttila T, Kerminen V-M, Hõrrak U, Vana M, Tammet H (2004a) Initial steps of aerosol growth. Atmos Chem Phys 4:2553–2560CrossRefGoogle Scholar
  84. Kulmala M, Suni T, Lehtinen KEJ, Dal Maso M, Boy M, Reissell A, Rannik Ü, Aaalto P, Keronen P, Hakola H, Bäck J, Hoffmann T, Vesala T, Hari P (2004b) A new feedback mechanism linking forests, aerosols, and climate. Atmos Chem Phys 4:557–562CrossRefGoogle Scholar
  85. 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, Tree physiology, vol 5. Springer, Berlin, pp 489–508CrossRefGoogle Scholar
  86. Lerdau M (2007) A positive feedback with negative consequences. Science 316:212–213PubMedCrossRefGoogle Scholar
  87. Lerdau M, Slobodkin K (2002) Trace gas emissions and species-dependent ecosystem services. Trends Ecol Evol 17:309–312CrossRefGoogle Scholar
  88. Li Z, Sharkey TD (2013) 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, Tree physiology, vol 5. Springer, Berlin, pp 119–151CrossRefGoogle Scholar
  89. Liavonchanka A, Feussner N (2006) Lipoxygenases: occurrence, functions and catalysis. J Plant Physiol 163:348–357PubMedCrossRefGoogle Scholar
  90. Llusià J, Peñuelas J, Sardans J, Owen SM, Niinemets Ü (2010) Measurement of volatile terpene emissions in 70 dominant vascular plant species in Hawaii: aliens emit more than natives. Glob Ecol Biogeogr 19:863–874CrossRefGoogle Scholar
  91. Llusià J, Sardans J, Niinemets Ü, Owen SM, Peñuelas J (2014) A screening study of leaf terpene emissions of 43 rainforest species in Danum Valley Conservation Area (Borneo) and their relationships with chemical and morphological leaf traits. Plant Biosyst 148:307–317CrossRefGoogle Scholar
  92. Loreto F, Fares S (2007) Is ozone flux inside leaves only a damage indicator? Clues from volatile isoprenoid studies. Plant Physiol 143:1096–1100PubMedPubMedCentralCrossRefGoogle Scholar
  93. Loreto F, Förster A, Dürr 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 21:101–107CrossRefGoogle Scholar
  94. Loreto F, Nascetti P, Graverini A, Mannozzi M (2000) Emission and content of monoterpenes in intact and wounded needles of the Mediterranean pine, Pinus pinea. Funct Ecol 14:589–595CrossRefGoogle Scholar
  95. Loreto F, Pinelli P, Manes F, Kollist H (2004) Impact of ozone on monoterpene emissions and evidence for an isoprene-like antioxidant action of monoterpenes emitted by leaves. Tree Physiol 24:361–367PubMedCrossRefGoogle Scholar
  96. Malm WC, Gebhart KA, Molenar J, Cahill T, Eldred R, Huffman D (1994) Examining the relationship between atmospheric aerosols and light extinction at Mount Rainier and North Cascades National Parks. Atmos Environ 28:347–360CrossRefGoogle Scholar
  97. 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 9:4387–4406CrossRefGoogle Scholar
  98. Mercado LM, Bellouin N, Sitch S, Boucher O, Huntingford C, Wild M, Cox PM (2009) Impact of changes in diffuse radiation on the global land carbon sink. Nature 458:1014–1017PubMedCrossRefGoogle Scholar
  99. Micheli F (2001) Pectin methylesterases: cell wall enzymes with important roles in plant physiology. Trends Plant Sci 6:414–419PubMedCrossRefGoogle Scholar
  100. Misson L, Lunden M, McKay M, Goldstein AH (2005) Atmospheric aerosol light scattering and surface wetness influence the diurnal pattern of net ecosystem exchange in a semi-arid ponderosa pine plantation. Agric For Meteorol 129:69–83CrossRefGoogle Scholar
  101. Monson RK, Grote R, Niinemets Ü, Schnitzler J-P (2012) Tansley review. Modeling the isoprene emission rate from leaves. New Phytol 195:541–559PubMedCrossRefGoogle Scholar
  102. Nemecek-Marshall M, MacDonald RC, Franzen JJ, Wojciechowski CL, Fall R (1995) Methanol emission from leaves. Enzymatic detection of gas-phase methanol and relation of methanol fluxes to stomatal conductance and leaf development. Plant Physiol 108:1359–1368PubMedPubMedCentralCrossRefGoogle Scholar
  103. Niinemets Ü, Tenhunen JD, Harley PC, Steinbrecher R (1999) A model of isoprene emission based on energetic requirements for isoprene synthesis and leaf photosynthetic properties for Liquidambar and Quercus. Plant Cell Environ 22:1319–1336CrossRefGoogle Scholar
  104. Niinemets Ü, Hauff K, Bertin N, Tenhunen JD, Steinbrecher R, Seufert G (2002a) Monoterpene emissions in relation to foliar photosynthetic and structural variables in Mediterranean evergreen Quercus species. New Phytol 153:243–256CrossRefGoogle Scholar
  105. Niinemets Ü, Reichstein M, Staudt M, Seufert G, Tenhunen JD (2002b) Stomatal constraints may affect emission of oxygenated monoterpenoids from the foliage of Pinus pinea. Plant Physiol 130:1371–1385PubMedPubMedCentralCrossRefGoogle Scholar
  106. Niinemets Ü, Loreto F, Reichstein M (2004) Physiological and physicochemical controls on foliar volatile organic compound emissions. Trends Plant Sci 9:180–186PubMedCrossRefGoogle Scholar
  107. Niinemets Ü, Arneth A, Kuhn U, Monson RK, Peñuelas J, Staudt M (2010a) The emission factor of volatile isoprenoids: stress, acclimation, and developmental responses. Biogeosciences 7:2203–2223CrossRefGoogle Scholar
  108. Niinemets Ü, Monson RK, Arneth A, Ciccioli P, Kesselmeier J, Kuhn U, Noe SM, Peñuelas J, Staudt M (2010b) The leaf-level emission factor of volatile isoprenoids: caveats, model algorithms, response shapes and scaling. Biogeosciences 7:1809–1832CrossRefGoogle Scholar
  109. Niinemets Ü, Flexas J, Peñuelas J (2011) Evergreens favored by higher responsiveness to increased CO2. Trends Ecol Evol 26:136–142PubMedCrossRefGoogle Scholar
  110. Niinemets Ü, Kännaste A, Copolovici L (2013) Quantitative patterns between plant volatile emissions induced by biotic stresses and the degree of damage. Front Plant Sci Front Plant-Microbe Interact 4:262Google Scholar
  111. Niinemets Ü, Sun Z, Talts E (2015) Controls of the quantum yield and saturation light of isoprene emission in different-aged aspen leaves. Plant Cell Environ 38:2707–2720PubMedPubMedCentralCrossRefGoogle Scholar
  112. Noe SM, Copolovici L, Niinemets Ü, Vaino E (2008) Foliar limonene uptake scales positively with leaf lipid content: “non-emitting” species absorb and release monoterpenes. Plant Biol 10:129–137PubMedCrossRefGoogle Scholar
  113. Nölscher AC, Williams J, Sinha V, Custer T, Song W, Johnson AM, Axinte R, Bozem H, Fischer H, Pouvesle N, Phillips G, Crowley JN, Rantala P, Rinne J, Kulmala M, Gonzales D, Valverde-Canossa J, Vogel A, Hoffmann T, Ouwersloot HG, Vilà-Guerau de Arellano J, Lelieveld J (2012) Summertime total OH reactivity measurements from boreal forest during HUMPPA-COPEC 2010. Atmos Chem Phys 12:8257–8270CrossRefGoogle Scholar
  114. Pazouki L, Niinemets Ü (2016) Multi-substrate terpenoid synthases: their occurrence and physiological significance. Front Plant Sci 7:1019PubMedPubMedCentralCrossRefGoogle Scholar
  115. Pazouki L, Kanagendran A, Li S, Kännaste A, Rajabi Memari H, Bichele R, Niinemets Ü (2016) Mono- and sesquiterpene release from tomato (Solanum lycopersicum) leaves upon mild and severe heat stress and through recovery: from gene expression to emission responses. Environ Exp Bot 132:1–15PubMedPubMedCentralCrossRefGoogle Scholar
  116. Peng J, van Loon JJ, Zheng S, Dicke M (2011) Herbivore-induced volatiles of cabbage (Brassica oleracea) prime defence responses in neighbouring intact plants. Plant Biol 13:276–284PubMedCrossRefGoogle Scholar
  117. Peñuelas J, Llusià J (2004) Plant VOC emissions: making use of the unavoidable. Trends Ecol Evol 19:402–404PubMedCrossRefGoogle Scholar
  118. Peñuelas J, Staudt M (2010) BVOCs and global change. Trends Plant Sci 15:133–144PubMedCrossRefGoogle Scholar
  119. Põldmaa K (1997) Explosion of Melampsoridium sp. on Alnus incana. Folia Cryptogamica Estonica 31:48–51Google Scholar
  120. Portillo-Estrada M, Kazantsev T, Talts E, Tosens T, Niinemets Ü (2015) Emission timetable and quantitative patterns of wound-induced volatiles across different damage treatments in aspen (Populus tremula). J Chem Ecol 41:1105–1117PubMedPubMedCentralCrossRefGoogle Scholar
  121. Possell M, Hewitt CN (2011) Isoprene emissions from plants are mediated by atmospheric CO2 concentrations. Glob Chang Biol 17:1595–1610CrossRefGoogle Scholar
  122. Possell M, Loreto F (2013) The role of volatile organic compounds in plant resistance to abiotic stresses: responses and mechanisms. In: Niinemets Ü, Monson RK (eds) Biology, controls and models of tree volatile organic compound emissions, Tree physiology, vol 5. Springer, Berlin, pp 209–235CrossRefGoogle Scholar
  123. 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, Tree physiology, vol 5. Springer, Berlin, pp 47–93CrossRefGoogle Scholar
  124. 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 154:1558–1570PubMedPubMedCentralCrossRefGoogle Scholar
  125. Rasulov B, Bichele I, Hüve K, Vislap V, Niinemets Ü (2015) Acclimation of isoprene emission and photosynthesis to growth temperature in hybrid aspen: resolving structural and physiological controls. Plant Cell Environ 38:751–766PubMedCrossRefGoogle Scholar
  126. 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 129:21–30PubMedCrossRefGoogle Scholar
  127. 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, Tree physiology, vol 5. Springer, Berlin, pp 95–118CrossRefGoogle Scholar
  128. Rottenberger S, Kleiss B, Kuhn U, Wolf A, Piedade MTF, Junk W, Kesselmeier J (2008) The effect of flooding on the exchange of the volatile C2-compounds ethanol, acetaldehyde and acetic acid between leaves of Amazonian floodplain tree species and the atmosphere. Biogeosciences 5:1085–1100CrossRefGoogle Scholar
  129. Russo A, Escobedo FJ, Zerbe S (2016) Quantifying the local-scale ecosystem services provided by urban treed streetscapes in Bolzano, Italy. AIMS Environ Sci 3:58–76CrossRefGoogle Scholar
  130. Sharkey TD, Chen XY, Yeh S (2001) Isoprene increases thermotolerance of fosmidomycin-fed leaves. Plant Physiol 125:2001–2006PubMedPubMedCentralCrossRefGoogle Scholar
  131. Shindell D, Faluvegi G, Lacis A, Hansen J, Ruedy R, Aguilar E (2006) Role of tropospheric ozone increases in 20th-century climate change. J Geophys Res Atmos 111:D08302, 083. CrossRefGoogle Scholar
  132. Simon V, Dumergues L, Ponche J-L, Torres L (2006) The biogenic volatile organic compounds emission inventory in France. Application to plant ecosystems in the Berre-Marseilles area (France). Sci Total Environ 372:164–182PubMedCrossRefGoogle Scholar
  133. Sinha V, Williams J, Lelieveld J, Ruuskanen TM, Kajos MK, Patokoski J, Hellen H, Hakola H, Mogensen D, Boy M, Rinne J, Kulmala M (2010) OH reactivity measurements within a boreal forest: evidence for unknown reactive emissions. Environ Sci Technol 44:6614–6620PubMedCrossRefGoogle Scholar
  134. Sitch S, Cox PM, Collins WJ, Huntingford C (2007) Indirect radiative forcing of climate change through ozone effects on the land-carbon sink. Nature 448:791–794PubMedCrossRefGoogle Scholar
  135. Spracklen DV, Bonn B, Carslaw KS (2008) Boreal forests, aerosols and the impacts on clouds and climate. Philos Trans R Soc Lond A 366:4613–4626CrossRefGoogle Scholar
  136. 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 21:385–395CrossRefGoogle Scholar
  137. Staudt M, Lhoutellier L (2011) Monoterpene and sesquiterpene emissions from Quercus coccifera exhibit interacting responses to light and temperature. Biogeosciences 8:2757–2771CrossRefGoogle Scholar
  138. Staudt M, Mir C, Joffre R, Rambal S, Bonin A, Landais D, Lumaret R (2004) Isoprenoid emissions of Quercus spp. (Q. suber and Q. ilex) in mixed stands contrasting in interspecific genetic introgression. New Phytol 163:573–584CrossRefGoogle Scholar
  139. Stavrakou T, Guenther A, Razavi A, Clarisse L, Clerbaux C, Coheur P-F, Hurtmans D, Karagulian F, De Maziére M, Vigouroux C, Amelynck C, Schoon N, Laffineur Q, Heinesch B, Aubinet M, Rinsland C, Müller J-F (2011) First space-based derivation of the global atmospheric methanol emission fluxes. Atmos Chem Phys 11:4873–4898Google Scholar
  140. Still CJ, Riley WJ, Biraud SC, Noone DC, Buenning NH, Randerson JT, Torn MS, Welker JM, White JWC, Vachon R, Farquhar GD, Berry JA (2009) Influence of clouds and diffuse radiation on ecosystem-atmosphere CO2 and CO18O exchanges. J Geophys Res Biogeosci 114:G01018CrossRefGoogle Scholar
  141. Stocker TF, Qin D, Plattner G-K, Tignor M, Allen SK, Boschung J, Nauels A, Xia Y, Bex V, Midgley PM (eds) (2014) Climate change 2014: the physical science basis. Contribution of Working Group I to the fifth assessment report of the Intergovernmental Panel on Climate Change. Cambridge University Press, Cambridge, UK/New York, USAGoogle Scholar
  142. 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 Chang Biol 18:3423–3440CrossRefGoogle Scholar
  143. Sun Z, Hüve K, Vislap V, Niinemets Ü (2013) Elevated [CO2] magnifies isoprene emissions under heat and improves thermal resistance in hybrid aspen. J Exp Bot 64:5509–5523PubMedPubMedCentralCrossRefGoogle Scholar
  144. Tholl D, Lee S (2011) Terpene specialized metabolism in Arabidopsis thaliana. Arabidopsis Book 9:e0143PubMedPubMedCentralCrossRefGoogle Scholar
  145. Tholl D, Sohrabi R, Huh J-H, Lee S (2011) The biochemistry of homoterpenes – common constituents of floral and herbivore-induced plant volatile bouquets. Phytochemistry 72:1635–1646PubMedCrossRefGoogle Scholar
  146. Tooker JF, Frank SD (2012) Genotypically diverse cultivar mixtures for insect pest management and increased crop yields. J Appl Ecol 49:974–985CrossRefGoogle Scholar
  147. Vanhanen H (2008) Invasive insects in Europe – the role of climate change and global trade. Dissertationes Forestales 57. Faculty of Forest Sciences, University of Joensuu, 33 pagesGoogle Scholar
  148. Velikova V, Sharkey TD, Loreto F (2012) Stabilization of thylakoid membranes in isoprene-emitting plants reduces formation of reactive oxygen species. Plant Signal Behav 7:139–141PubMedPubMedCentralCrossRefGoogle Scholar
  149. Vickers CE, Gershenzon J, Lerdau MT, Loreto F (2009) A unified mechanism of action for volatile isoprenoids in plant abiotic stress. Nat Chem Biol 5:283–291PubMedCrossRefGoogle Scholar
  150. von Dahl C, Hävecker M, Schlögl R, Baldwin IT (2006) Caterpillar-elicited methanol emission: a new signal in plant-herbivore interaction? Plant J 46:948–960CrossRefGoogle Scholar
  151. Voulgarakis A, Naik V, Lamarque J-F, Shindell DT, Young PJ, Prather MJ, Wild O, Field RD, Bergmann D, Cameron-Smith P, Cionni I, Collins WJ, Dalsøren SB, Doherty RM, Eyring V, Faluvegi G, Folberth GA, Horowitz LW, Josse B, MacKenzie IA, Nagashima T, Plummer DA, Righi M, Rumbold ST, Stevenson DS, Strode SA, Sudo K, Szopa S, Zeng G (2013) Analysis of present day and future OH and methane lifetime in the ACCMIP simulations. Atmos Chem Phys 13:2563–2587CrossRefGoogle Scholar
  152. Widegren JA, Bruno TJ (2010) Vapor pressure measurements on low-volatility terpenoid compounds by the concatenated gas saturation method. Environ Sci Technol 44:388–393PubMedCrossRefGoogle Scholar
  153. Wilkinson MJ, Monson RK, Trahan N, Lee S, Brown E, Jackson RB, Polley HW, Fay PA, Fall R (2009) Leaf isoprene emission rate as a function of atmospheric CO2 concentration. Glob Chang Biol 15:1189–1200CrossRefGoogle Scholar
  154. Winters AJ, Adams MA, Bleby TM, Rennenberg H, Steigner D, Steinbrecher R, Kreuzwieser J (2009) Emissions of isoprene, monoterpene and short-chained carbonyl compounds from Eucalyptus spp. in southern Australia. Atmos Environ 43:3035–3043CrossRefGoogle Scholar
  155. Zhang P-J, Zheng S-J, van Loona JJA, Boland W, David A, Mumm R, Dicke M (2009) Whiteflies interfere with indirect plant defense against spider mites in lima bean. Proc Natl Acad Sci U S A 106:21202–21207PubMedPubMedCentralCrossRefGoogle Scholar

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© Springer International Publishing AG, part of Springer Nature 2018

Authors and Affiliations

  1. 1.Institute of Agricultural and Environmental Sciences, Estonian University of Life SciencesTartuEstonia

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