Skip to main content
Log in

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

  • Published:
Journal of Chemical Ecology Aims and scope Submit manuscript

Abstract

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.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6

Similar content being viewed by others

References

  • 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 135:2025–2037

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Arimura G, Kost C, Boland W (2005) Herbivore-induced, indirect plant defences. Bba-Mol Cell Biol L 1734:91–111

    CAS  Google Scholar 

  • Arneth A, Niinemets Ü (2010) Induced BVOCs: how to bug our models? Trends Plant Sci 15:118–125

    Article  CAS  PubMed  Google Scholar 

  • Balek J, Pavlík O (1977) Sap stream velocity as an indicator of the transpirational process. J Hydrol 34:193–200

    Article  Google Scholar 

  • 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 225:141–155

    Article  PubMed  Google Scholar 

  • 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 28:1334–1343

    Article  CAS  Google Scholar 

  • Benikhlef L et al. (2013) Perception of soft mechanical stress in arabidopsis leaves activates disease resistance. BMC Plant Biol 13:133

    Article  PubMed Central  PubMed  Google Scholar 

  • Blande JD, Holopainen JK, Niinemets Ü (2014) Plant volatiles in polluted atmospheres: stress responses and signal degradation. Plant Cell Environ 37:1892–1904

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • 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 175:244–254

    Article  CAS  PubMed  Google Scholar 

  • 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:e20419

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Brilli F et al. (2012) Qualitative and quantitative characterization of volatile organic compound emissions from cut grass. Environ Sci Technol 46:3859–3865

    Article  CAS  PubMed  Google Scholar 

  • 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 37:18–28

    Article  CAS  PubMed  Google Scholar 

  • 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 100:55–63

    Article  CAS  Google Scholar 

  • 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 34:1399–1410

    Article  PubMed Central  PubMed  Google Scholar 

  • 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 101:13–24

    PubMed Central  CAS  PubMed  Google Scholar 

  • Fall R, Benson AA (1996) Leaf methanol - the simplest natural product from plants. Trends Plant Sci 1:296–301

    Article  Google Scholar 

  • 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 104:15963–15974

    Article  CAS  Google Scholar 

  • 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 35:3905–3916

    Article  CAS  Google Scholar 

  • Farag MA, Fokar M, Zhang HA, Allen RD, Pare PW (2005) (Z)-3-hexenol induces defense genes and downstream metabolites in maize. Planta 220:900–909

    Article  CAS  PubMed  Google Scholar 

  • 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 169:135–144

    Article  CAS  PubMed  Google Scholar 

  • Fisher AJ, Grimes HD, Fall R (2003) The biochemical origin of pentenol emissions from wounded leaves. Phytochemistry 62:159–163

    Article  CAS  PubMed  Google Scholar 

  • 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 36:542–552

    Article  CAS  PubMed  Google Scholar 

  • 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:e17393

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • 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 135:1967–1975

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • 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 21:1037–1044

    Article  CAS  PubMed  Google Scholar 

  • 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 11:591–597

    Article  CAS  PubMed  Google Scholar 

  • Jardine K et al. (2012) Green leaf volatiles and oxygenated metabolite emission bursts from mesquite branches following light-dark transitions. Photosynthesis Res 113:321–333

    Article  CAS  Google Scholar 

  • 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 286:122–128

    Article  CAS  Google Scholar 

  • Karl T, Fall R, Jordan A, Lindinger W (2001) On-line analysis of reactive VOCs from urban lawn mowing. Environ Sci Technol 35:2926–2931

    Article  CAS  PubMed  Google Scholar 

  • 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 25:1121–1131

    Article  CAS  Google Scholar 

  • Kessler A, Baldwin IT (2002) Plant responses to insect herbivory: the emerging molecular analysis. Annu Rev Plant Biol 53:299–328

    Article  CAS  PubMed  Google Scholar 

  • Lautner S, Grams TEE, Matyssek R, Fromm J (2005) Characteristics of electrical signals in poplar and responses in photosynthesis. Plant Physiol 138:2200–2209

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Lee A et al. (2004) Inverse correlation between jasmonic acid and salicylic acid during early wound response in rice. Biochem Biophys Res Commun 318:734–738

    Article  CAS  PubMed  Google Scholar 

  • Loreto F, Schnitzler J-P (2010) Abiotic stresses and induced BVOCs. Trends Plant Sci 15:154–166

    Article  CAS  PubMed  Google Scholar 

  • 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 29:1820–1828

    Article  CAS  PubMed  Google Scholar 

  • 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:e36433

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Micheli F (2001) Pectin methylesterases: cell wall enzymes with important roles in plant physiology. Trends Plant Sci 6:414–419

    Article  CAS  PubMed  Google Scholar 

  • Mithöfer A, Boland W (2008) Recognition of herbivory-associated molecular patterns. Plant Physiol 146:825–831

    Article  PubMed Central  PubMed  Google Scholar 

  • Moldau H, Wong S-C, Osmond CB (1993) Transient depression of photosynthesis in bean leaves during rapid water loss. Aust J Plant Physiol 20:45–54

    Article  Google Scholar 

  • 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. 153–179

    Chapter  Google Scholar 

  • 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. 399–423

    Chapter  Google Scholar 

  • 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. 509–528

    Chapter  Google Scholar 

  • 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

    Article  Google Scholar 

  • Niinemets Ü, Loreto F, Reichstein M (2004) Physiological and physicochemical controls on foliar volatile organic compound emissions. Trends Plant Sci 9:180–186

    Article  CAS  PubMed  Google Scholar 

  • Niinemets Ü et al. (2010) The leaf-level emission factor of volatile isoprenoids: caveats, model algorithms, response shapes and scaling. Biogeosciences 7:1809–1832

    Article  CAS  Google Scholar 

  • Niinemets Ü et al. (2011) Estimations of isoprenoid emission capacity from enclosure studies: measurements, data processing, quality and standardized measurement protocols. Biogeosciences 8:2209–2246

    Article  CAS  Google Scholar 

  • 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 4:262

    Article  PubMed Central  PubMed  Google Scholar 

  • Paiva NL (2000) An introduction to the biosynthesis of chemicals used in plant-microbe communication. J Plant Growth Reg 19:131–143

    CAS  Google Scholar 

  • 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 37:1924–1935

    Article  PubMed  Google Scholar 

  • Portillo-Estrada M (2013) Advantages of PTR-MS and PTR-TOF-MS techniques for measuring volatile organic compounds (VOCs). Sci Bull Escorena 8:65–67

    Google Scholar 

  • 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 151:448–460

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Ridley BL, O’Neill MA, Mohnen D (2001) Pectins: structure, biosynthesis, and oligogalacturonide-related signaling. Phytochemistry 57:929–967

    Article  CAS  PubMed  Google Scholar 

  • 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 14:17781–17811

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • 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 138:123–133

    Article  CAS  PubMed  Google Scholar 

  • Shen J et al. (2014) A 13-lipoxygenase, TomloxC, is essential for synthesis of C5 flavour volatiles in tomato. J Exp Bot 65:519–428

    Article  Google Scholar 

  • 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 23:880–907

    Article  Google Scholar 

  • 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 18:3423–3440

    Article  Google Scholar 

  • 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:e36168

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • 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 73:174–185

    Article  Google Scholar 

  • 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 1:159–165

    Article  Google Scholar 

  • 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 45:173–196

    CAS  Google Scholar 

Download references

Acknowledgements

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].

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Miguel Portillo-Estrada.

Ethics declarations

Conflict of Interest

The authors declare no conflict of interest.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Portillo-Estrada, M., Kazantsev, T., Talts, E. et al. Emission Timetable and Quantitative Patterns of Wound-Induced Volatiles Across Different Leaf Damage Treatments in Aspen (Populus Tremula). J Chem Ecol 41, 1105–1117 (2015). https://doi.org/10.1007/s10886-015-0646-y

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10886-015-0646-y

Keywords

Navigation