Journal of Chemical Ecology

, Volume 41, Issue 12, pp 1105–1117 | Cite as

Emission Timetable and Quantitative Patterns of Wound-Induced Volatiles Across Different Leaf Damage Treatments in Aspen (Populus Tremula)

  • Miguel Portillo-EstradaEmail author
  • Taras Kazantsev
  • Eero Talts
  • Tiina Tosens
  • Ülo Niinemets


Plant-feeding herbivores can generate complex patterns of foliar wounding, but it is unclear how wounding-elicited volatile emissions scale with the severity of different wounding types, and there is no common protocol for wounding experiments. We investigated the rapid initial response to wounding damage generated by different numbers of straight cuts and punctures through leaf lamina as well as varying area of lamina squeezing in the temperate deciduous tree Populus tremula. Wounding-induced volatile emission time-courses were continuously recorded by a proton-transfer-reaction time-of-flight mass-spectrometer. After the mechanical wounding, an emission cascade was rapidly elicited resulting in sequential emissions of key stress volatiles methanol, acetaldehyde, and volatiles of the lipoxygenase pathway, collectively constituting more than 97 % of the total emission. The maximum emission rates, reached after one to three minutes after wounding, and integrated emissions during the burst were strongly correlated with the severity in all damage treatments. For straight cuts and punch hole treatments, the emissions per cut edge length were constant, indicating a direct proportionality. Our results are useful for screening wounding-dependent emission capacities.


Abiotic stress Green volatiles Hexenal LOX products Mass spectrometry Proton-transfer-reaction 



We thank Peter C. Harley for insightful comments on the MS. We thank the two reviewers and Editors for helpful advice that significantly improved the manuscript. This work was supported by the Estonian Ministry of Science and Education [institutional grant IUT-8-3], Estonian Science Foundation [grant 9253], the European Commission through the European Regional Fund [Center of Excellence in Environmental Adaptation] and Marie Curie [grant ERMOS73] and through the Transnational Access to Research Infrastructures activity [ExpeER], the European Research Council [advanced grant 322603, SIP-VOL+] and the European Social fund ESF [MJD 438].

Compliance with Ethical Standards

Conflict of Interest

The authors declare no conflict of interest.


  1. Ament K, Kant MR, Sabelis MW, Haring MA, Schuurink RC (2004) Jasmonic acid is a key regulator of spider mite-induced volatile terpenoid and methyl salicylate emission in tomato. Plant Physiol 135:2025–2037PubMedCentralCrossRefPubMedGoogle Scholar
  2. Arimura G, Kost C, Boland W (2005) Herbivore-induced, indirect plant defences. Bba-Mol Cell Biol L 1734:91–111Google Scholar
  3. Arneth A, Niinemets Ü (2010) Induced BVOCs: how to bug our models? Trends Plant Sci 15:118–125CrossRefPubMedGoogle Scholar
  4. Balek J, Pavlík O (1977) Sap stream velocity as an indicator of the transpirational process. J Hydrol 34:193–200CrossRefGoogle Scholar
  5. Baluška F, Liners F, Hlavačka A, Schlicht M, Van Cutsem P, McCurdy DW, Menzel D (2005) Cell wall pectins and xyloglucans are internalized into dividing root cells and accumulate within cell plates during cytokinesis. Protoplasma 225:141–155CrossRefPubMedGoogle Scholar
  6. Beauchamp J et al. (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
  7. Benikhlef L et al. (2013) Perception of soft mechanical stress in arabidopsis leaves activates disease resistance. BMC Plant Biol 13:133PubMedCentralCrossRefPubMedGoogle Scholar
  8. Blande JD, Holopainen JK, Niinemets Ü (2014) Plant volatiles in polluted atmospheres: stress responses and signal degradation. Plant Cell Environ 37:1892–1904PubMedCentralCrossRefPubMedGoogle Scholar
  9. 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 175:244–254CrossRefPubMedGoogle Scholar
  10. Brilli F et al. (2011) Detection of plant volatiles after leaf wounding and darkening by proton transfer reaction "time-of-flight" mass spectrometry (PTR-TOF). PLoS One 6:e20419PubMedCentralCrossRefPubMedGoogle Scholar
  11. Brilli F et al. (2012) Qualitative and quantitative characterization of volatile organic compound emissions from cut grass. Environ Sci Technol 46:3859–3865CrossRefPubMedGoogle Scholar
  12. 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 37:18–28CrossRefPubMedGoogle Scholar
  13. 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 100:55–63CrossRefGoogle Scholar
  14. 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 34:1399–1410PubMedCentralCrossRefPubMedGoogle Scholar
  15. Croft KPC, Juttner F, Slusarenko AJ (1993) Volatile products of the lipoxygenase pathway evolved from Phaseolus vulgaris (L.) leaves inoculated with Pseudomonas syringae pv. Phaseolicola. Plant Physiol 101:13–24PubMedCentralPubMedGoogle Scholar
  16. Fall R, Benson AA (1996) Leaf methanol - the simplest natural product from plants. Trends Plant Sci 1:296–301CrossRefGoogle Scholar
  17. Fall R, Karl T, Hansel A, Jordan A, Lindinger W (1999) Volatile organic compounds emitted after leaf wounding: on-line analysis by proton-transfer-reaction mass spectrometry. J Geophys Res-Atmos 104:15963–15974CrossRefGoogle Scholar
  18. Fall R, Karl T, Jordon A, Lindinger W (2001) Biogenic C5 VOCs: release from leaves after freeze-thaw wounding and occurrence in air at a high mountain observatory. Atmos Environ 35:3905–3916CrossRefGoogle Scholar
  19. Farag MA, Fokar M, Zhang HA, Allen RD, Pare PW (2005) (Z)-3-hexenol induces defense genes and downstream metabolites in maize. Planta 220:900–909CrossRefPubMedGoogle Scholar
  20. Filella I, Peñuelas J, Llusià J (2006) Dynamics of the enhanced emissions of monoterpenes and methyl salicylate, and decreased uptake of formaldehyde, by quercus ilex leaves after application of jasmonic acid. New Phytol 169:135–144CrossRefPubMedGoogle Scholar
  21. Fisher AJ, Grimes HD, Fall R (2003) The biochemical origin of pentenol emissions from wounded leaves. Phytochemistry 62:159–163CrossRefPubMedGoogle Scholar
  22. Galle A, Lautner S, Flexas J, Ribas-Carbo M, Hanson D, Roesgen J, Fromm J (2013) Photosynthetic responses of soybean (Glycine max L.) to heat-induced electrical signalling are predominantly governed by modifications of mesophyll conductance for CO2. Plant Cell Environ 36:542–552CrossRefPubMedGoogle Scholar
  23. Ghirardo A, Gutknecht J, Zimmer I, Brüggemann N, Schnitzler J-P (2011) Biogenic volatile organic compound and respiratory CO2 emissions after 13C-labeling: online tracing of C translocation dynamics in poplar plants. PLoS One 6:e17393PubMedCentralCrossRefPubMedGoogle Scholar
  24. Graus M, Schnitzler JP, Hansel A, Cojocariu C, Rennenberg H, Wisthaler A, Kreuzwieser J (2004) Transient release of oxygenated volatile organic compounds during light-dark transitions in grey poplar leaves. Plant Physiol 135:1967–1975PubMedCentralCrossRefPubMedGoogle Scholar
  25. Graus M, Müller M, Hansel A (2010) High resolution PTR-TOF: quantification and formula confirmation of VOC in real time. J Am Soc Mass Spectrom 21:1037–1044CrossRefPubMedGoogle Scholar
  26. Jardine K, Karl T, Lerdau M, Harley P, Guenther A, Mak JE (2009) Carbon isotope analysis of acetaldehyde emitted from leaves following mechanical stress and anoxia. Plant Biol 11:591–597CrossRefPubMedGoogle Scholar
  27. Jardine K et al. (2012) Green leaf volatiles and oxygenated metabolite emission bursts from mesquite branches following light-dark transitions. Photosynthesis Res 113:321–333CrossRefGoogle Scholar
  28. Jordan A et al. (2009) A high resolution and high sensitivity proton-transfer-reaction time-of-flight mass spectrometer (PTR-TOF-MS). Int J Mass Spectrom 286:122–128CrossRefGoogle Scholar
  29. Karl T, Fall R, Jordan A, Lindinger W (2001) On-line analysis of reactive VOCs from urban lawn mowing. Environ Sci Technol 35:2926–2931CrossRefPubMedGoogle Scholar
  30. Karl T, Curtis AJ, Rosenstiel TN, Monson RK, Fall R (2002) Transient releases of acetaldehyde from tree leaves - products of a pyruvate overflow mechanism. Plant Cell Environ 25:1121–1131CrossRefGoogle Scholar
  31. Kessler A, Baldwin IT (2002) Plant responses to insect herbivory: the emerging molecular analysis. Annu Rev Plant Biol 53:299–328CrossRefPubMedGoogle Scholar
  32. Lautner S, Grams TEE, Matyssek R, Fromm J (2005) Characteristics of electrical signals in poplar and responses in photosynthesis. Plant Physiol 138:2200–2209PubMedCentralCrossRefPubMedGoogle Scholar
  33. Lee A et al. (2004) Inverse correlation between jasmonic acid and salicylic acid during early wound response in rice. Biochem Biophys Res Commun 318:734–738CrossRefPubMedGoogle Scholar
  34. Loreto F, Schnitzler J-P (2010) Abiotic stresses and induced BVOCs. Trends Plant Sci 15:154–166CrossRefPubMedGoogle Scholar
  35. 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 29:1820–1828CrossRefPubMedGoogle Scholar
  36. Matsui K, Sugimoto K, Ji M, Ozawa R, Takabayashi J (2012) Differential metabolisms of green leaf volatiles in injured and intact parts of a wounded leaf meet distinct ecophysiological requirements. PLoS One 7:e36433PubMedCentralCrossRefPubMedGoogle Scholar
  37. Micheli F (2001) Pectin methylesterases: cell wall enzymes with important roles in plant physiology. Trends Plant Sci 6:414–419CrossRefPubMedGoogle Scholar
  38. Mithöfer A, Boland W (2008) Recognition of herbivory-associated molecular patterns. Plant Physiol 146:825–831PubMedCentralCrossRefPubMedGoogle Scholar
  39. Moldau H, Wong S-C, Osmond CB (1993) Transient depression of photosynthesis in bean leaves during rapid water loss. Aust J Plant Physiol 20:45–54CrossRefGoogle Scholar
  40. 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, Tree Physiology, vol 5. Springer, Berlin, pp. 153–179CrossRefGoogle Scholar
  41. Niinemets Ü (2012) Whole plant photosynthesis. In: Flexas J, Loreto F, Medrano H (eds) Terrestrial photosynthesis in a changing environment, A molecular, physiological and ecological approach. Cambridge University Press, Cambridge, pp. 399–423CrossRefGoogle Scholar
  42. Niinemets Ü, Monson RK (2013) State-of-the-art of BVOC research: what do we have and what have we missed? A synthesis. In: Niinemets Ü, Monson RK (eds) Biology, controls and models of tree volatile organic compound emissions, Tree Physiology, vol 5. Springer, Berlin, pp. 509–528CrossRefGoogle Scholar
  43. 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 108:4208CrossRefGoogle Scholar
  44. Niinemets Ü, Loreto F, Reichstein M (2004) Physiological and physicochemical controls on foliar volatile organic compound emissions. Trends Plant Sci 9:180–186CrossRefPubMedGoogle Scholar
  45. Niinemets Ü et al. (2010) The leaf-level emission factor of volatile isoprenoids: caveats, model algorithms, response shapes and scaling. Biogeosciences 7:1809–1832CrossRefGoogle Scholar
  46. Niinemets Ü et al. (2011) Estimations of isoprenoid emission capacity from enclosure studies: measurements, data processing, quality and standardized measurement protocols. Biogeosciences 8:2209–2246CrossRefGoogle Scholar
  47. 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 4:262PubMedCentralCrossRefPubMedGoogle Scholar
  48. Paiva NL (2000) An introduction to the biosynthesis of chemicals used in plant-microbe communication. J Plant Growth Reg 19:131–143Google Scholar
  49. Ponzio C, Gols R, Weldegergis BT, Dicke M (2014) Caterpillar-induced plant volatiles remain a reliable signal for foraging wasps during dual attack with a plant pathogen or non-host insect herbivore. Plant Cell Environ 37:1924–1935CrossRefPubMedGoogle Scholar
  50. Portillo-Estrada M (2013) Advantages of PTR-MS and PTR-TOF-MS techniques for measuring volatile organic compounds (VOCs). Sci Bull Escorena 8:65–67Google Scholar
  51. Rasulov B, Hüve K, Välbe M, Laisk A, Niinemets Ü (2009) Evidence that light, carbon dioxide and oxygen dependencies of leaf isoprene emission are driven by energy status in hybrid aspen. Plant Physiol 151:448–460PubMedCentralCrossRefPubMedGoogle Scholar
  52. Ridley BL, O’Neill MA, Mohnen D (2001) Pectins: structure, biosynthesis, and oligogalacturonide-related signaling. Phytochemistry 57:929–967CrossRefPubMedGoogle Scholar
  53. Scala A, Allmann S, Mirabella R, Haring MA, Schuurink RC (2013) Green leaf volatiles: a plant’s multifunctional weapon against herbivores and pathogens. Int J Mol Sci 14:17781–17811PubMedCentralCrossRefPubMedGoogle Scholar
  54. Schaub A, Blande JD, Graus M, Oksanen E, Holopainen JK, Hansel A (2010) Real-time monitoring of herbivore induced volatile emissions in the field. Physiol Plant 138:123–133CrossRefPubMedGoogle Scholar
  55. Shen J et al. (2014) A 13-lipoxygenase, TomloxC, is essential for synthesis of C5 flavour volatiles in tomato. J Exp Bot 65:519–428CrossRefGoogle Scholar
  56. Smith L, Beck JJ (2013) Effect of mechanical damage on emission of volatile organic compounds from plant leaves and implications for evaluation of host plant specificity of prospective biological control agents of weeds. Biocontrol Sci Tech 23:880–907CrossRefGoogle Scholar
  57. 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
  58. Tian DL et al. (2012) Salivary glucose oxidase from caterpillars mediates the induction of rapid and delayed-induced defenses in the tomato plant. PLoS One 7:e36168PubMedCentralCrossRefPubMedGoogle Scholar
  59. Verlinden MS, Broeckx LS, Ceulemans R (2015) First vs. second rotation of a poplar short rotation coppice: above-ground biomass productivity and shoot dynamics. Biomass Bioenerg 73:174–185CrossRefGoogle Scholar
  60. Vuorinen T, Nerg AM, Syrjala L, Peltonen P, Holopainen JK (2007) Epirrita autumnata induced VOC emission of silver birch differ from emission induced by leaf fungal pathogen. Arthropod-Plant Inte 1:159–165CrossRefGoogle Scholar
  61. Wildt J, Kobel K, Schuh-Thomas G, Heiden AC (2003) Emissions of oxygenated volatile organic compounds from plants. Part II: Emissions of Saturated aLdehydes J Atmos Chem 45:173–196Google Scholar

Copyright information

© Springer Science+Business Media New York 2015

Authors and Affiliations

  • Miguel Portillo-Estrada
    • 1
    • 2
  • Taras Kazantsev
    • 1
  • Eero Talts
    • 1
  • Tiina Tosens
    • 1
  • Ülo Niinemets
    • 1
    • 3
  1. 1.Department of Plant Physiology, Institute of Agricultural and Environmental SciencesEstonian University of Life SciencesTartuEstonia
  2. 2.Centre of Excellence PLECO (Plant and Vegetation Ecology), Department of BiologyUniversity of AntwerpWilrijkBelgium
  3. 3.Estonian Academy of SciencesTallinnEstonia

Personalised recommendations