Skip to main content

Thank you for visiting nature.com. You are using a browser version with limited support for CSS. To obtain the best experience, we recommend you use a more up to date browser (or turn off compatibility mode in Internet Explorer). In the meantime, to ensure continued support, we are displaying the site without styles and JavaScript.

  • Perspective
  • Published:

A unified mechanism of action for volatile isoprenoids in plant abiotic stress

Abstract

The sessile nature of plants has resulted in the evolution of an extraordinarily diverse suite of protective mechanisms against biotic and abiotic stresses. Though volatile isoprenoids are known to be involved in many types of biotic interactions, they also play important but relatively unappreciated roles in abiotic stress responses. We review those roles, discuss the proposed mechanistic explanations and examine the evolutionary significance of volatile isoprenoid emission. We note that abiotic stress responses generically involve production of reactive oxygen species in plant cells, and volatile isoprenoids mitigate the effects of oxidative stress by mediating the oxidative status of the plant. On the basis of these observations, we propose a 'single biochemical mechanism for multiple physiological stressors' model, whereby the protective effect against abiotic stress is exerted through direct or indirect improvement in resistance to damage by reactive oxygen species.

This is a preview of subscription content, access via your institution

Access options

Buy this article

Prices may be subject to local taxes which are calculated during checkout

Figure 1: Plants are exposed to a variety of abiotic stresses.
Figure 2: The chloroplastic antioxidant/enzyme defense network reactions in response to increased light and temperature.
Figure 3: Isoprenoid biosynthetic pathways (simplified).
Figure 4: Chemical structures of isoprenoids with antioxidant properties.
Figure 5: The 'single biochemical mechanism for multiple physiological stressors' model.

Similar content being viewed by others

References

  1. Intergovernmental Panel on Climate Change. Climate Change 2001: The Scientific Basis (Cambridge University Press, Cambridge, UK, 2001).

  2. Apel, K. & Hirt, H. Reactive oxygen species: metabolism, oxidative stress, and signal transduction. Annu. Rev. Plant Biol. 55, 373–399 (2004).

    CAS  Google Scholar 

  3. Dietz, K.J. Redox control, redox signaling, and redox homeostasis in plant cells. Int. Rev. Cytol. 228, 141–193 (2003).

    CAS  PubMed  Google Scholar 

  4. Kwak, J.M., Nguyen, V. & Schroeder, J.I. The role of reactive oxygen species in hormonal responses. Plant Physiol. 141, 323–329 (2006).

    CAS  PubMed  PubMed Central  Google Scholar 

  5. Rohmer, M. The discovery of a mevalonate-independent pathway for isoprenoid biosynthesis in bacteria, algae and higher plants. Nat. Prod. Rep. 16, 565–574 (1999).

    CAS  PubMed  Google Scholar 

  6. Lange, B.M., Rujan, T., Martin, W. & Croteau, R. Isoprenoid biosynthesis: the evolution of two ancient and distinct pathways across genomes. Proc. Natl. Acad. Sci. USA 97, 13172–13177 (2000).

    CAS  PubMed  Google Scholar 

  7. Lichtenthaler, H.K. Non-mevalonate isoprenoid biosynthesis: enzymes, genes and inhibitors. Biochem. Soc. Trans. 28, 785–789 (2000).

    CAS  PubMed  Google Scholar 

  8. Dudareva, N. et al. The nonmevalonate pathway supports both monoterpene and sesquiterpene formation in snapdragon flowers. Proc. Natl. Acad. Sci. USA 102, 933–938 (2005).

    CAS  PubMed  Google Scholar 

  9. Laule, O. et al. Crosstalk between cytosolic and plastidial pathways of isoprenoid biosynthesis in Arabidopsis thaliana. Proc. Natl. Acad. Sci. USA 100, 6866–6871 (2003).

    CAS  PubMed  Google Scholar 

  10. Bick, J.A. & Lange, B.M. Metabolic cross talk between cytosolic and plastidial pathways of isoprenoid biosynthesis: unidirectional transport of intermediates across the chloroplast envelope membrane. Arch. Biochem. Biophys. 415, 146–154 (2003).

    CAS  PubMed  Google Scholar 

  11. Wu, S.Q. et al. Redirection of cytosolic or plastidic isoprenoid precursors elevates terpene production in plants. Nat. Biotechnol. 24, 1441–1447 (2006).

    CAS  PubMed  Google Scholar 

  12. Dudareva, N., Negre, F., Nagegowda, D.A. & Orlova, I. Plant volatiles: recent advances and future perspectives. Crit. Rev. Plant Sci. 25, 417–440 (2006).

    CAS  Google Scholar 

  13. Sharkey, T.D. & Yeh, S. Isoprene emission from plants. Annu. Rev. Plant Physiol. Plant Mol. Biol. 52, 407–436 (2001).

    CAS  PubMed  Google Scholar 

  14. Brilli, F. et al. Response of isoprene emission and carbon metabolism to drought in white poplar (Populus alba) saplings. New Phytol. 175, 244–254 (2007).

    CAS  PubMed  Google Scholar 

  15. Loreto, F. & Sharkey, T.D. A gas-exchange study of photosynthesis and isoprene emission in Quercus rubra L. Planta 182, 523–531 (1990).

    CAS  PubMed  Google Scholar 

  16. Monson, R.K. & Fall, R. Isoprene emission from aspen leaves: influence of environment and relation to photosynthesis and photorespiration. Plant Physiol. 90, 267–274 (1989).

    CAS  PubMed  PubMed Central  Google Scholar 

  17. Gershenzon, J. Plant volatiles carry both public and private messages. Proc. Natl. Acad. Sci. USA 104, 5257–5258 (2007).

    CAS  PubMed  Google Scholar 

  18. Baldwin, I.T., Halitschke, R., Paschold, A., von Dahl, C.C. & Preston, C.A. Volatile signaling in plant-plant interactions: “talking trees” in the genomics era. Science 311, 812–815 (2006).

    CAS  PubMed  Google Scholar 

  19. Loreto, F., Forster, A., Durr, M., Csiky, O. & Seufert, G. 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, 101–107 (1998).

    CAS  Google Scholar 

  20. Loreto, F., Barta, C., Brilli, F. & Nogues, I. 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 (2006).

    CAS  PubMed  Google Scholar 

  21. Sharkey, T.D. & Loreto, F. Water stress, temperature, and light effects on the capacity for isoprene emission and photosynthesis of kudzu leaves. Oecologia 95, 328–333 (1993).

    PubMed  Google Scholar 

  22. Tingey, D.T., Evans, R. & Gumpertz, M. Effects of environmental conditions on isoprene emission from live oak. Planta 152, 565–570 (1981).

    CAS  PubMed  Google Scholar 

  23. Filella, I., Peñuelas, J. & Llusia, J. 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 (2006).

    CAS  PubMed  Google Scholar 

  24. Martin, D.M., Gershenzon, J. & Bohlmann, J. Induction of volatile terpene biosynthesis and diurnal emission by methyl jasmonate in foliage of norway spruce. Plant Physiol. 132, 1586–1599 (2003).

    CAS  PubMed  PubMed Central  Google Scholar 

  25. Schnitzler, J.P. et al. Contribution of different carbon sources to isoprene biosynthesis in poplar leaves. Plant Physiol. 135, 152–160 (2004).

    CAS  PubMed  PubMed Central  Google Scholar 

  26. Funk, J.L., Mak, J.E. & Lerdau, M.T. Stress-induced changes in carbon sources for isoprene production in Populus deltoides. Plant Cell Environ. 27, 747–755 (2004).

    CAS  Google Scholar 

  27. Rosenstiel, T.N., Ebbets, A.L., Khatri, W.C., Fall, R. & Monson, R.K. Induction of poplar leaf nitrate reductase: a test of extrachloroplastic control of isoprene emission rate. Plant Biol. (Stuttg) 6, 12–21 (2004).

    CAS  Google Scholar 

  28. Sanadze, G.A. Biogenic isoprene (a review). Russ. J. Plant Physiol. 51, 729–741 (2004).

    CAS  Google Scholar 

  29. Magel, E. et al. Photosynthesis and substrate supply for isoprene biosynthesis in poplar leaves. Atmos. Environ. 40 (suppl. 1): 138–151 (2006).

    Google Scholar 

  30. Sharkey, T.D., Wiberley, A.E. & Donohue, A.R. Isoprene emission from plants: why and how. Ann. Bot. (Lond.) 101, 5–18 (2008).

    CAS  Google Scholar 

  31. Laothawornkitkul, J. et al. Isoprene emissions influence herbivore feeding decisions. Plant Cell Environ. 31, 1410–1415 (2008).

    CAS  PubMed  Google Scholar 

  32. Loivamäki, M., Mumm, R., Dicke, M. & Schnitzler, J.P. Isoprene interferes with the attraction of bodyguards by herbaceous plants. Proc. Natl. Acad. Sci. USA 105, 17430–17435 (2008).

    PubMed  Google Scholar 

  33. Kuzuyama, T., Shimizu, T., Takahashi, S. & Seto, H. Fosmidomycin, a specific inhibitor of 1-deoxy-D-xylulose 5-phosphate reductoisomerase in the nonmevalonate pathway for terpenoid biosynthesis. Tetrahedr. Lett. 39, 7913–7916 (1998).

    CAS  Google Scholar 

  34. Sharkey, T.D. & Singsaas, E.L. Why plants emit isoprene. Nature 374, 769 (1995).

    CAS  Google Scholar 

  35. Velikova, V., Loreto, F., Tsonev, T., Brilli, F. & Edreva, A. Isoprene prevents the negative consequences of high temperature stress in Platanus orientalis leaves. Funct. Plant Biol. 33, 931–940 (2006).

    CAS  Google Scholar 

  36. Velikova, V., Pinelli, P. & Loreto, F. Consequences of inhibition of isoprene synthesis in Phragmites australis leaves exposed to elevated temperatures. Agric. Ecosyst. Environ. 106, 209–217 (2005).

    CAS  Google Scholar 

  37. Velikova, V. & Loreto, F. 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, 318–327 (2005).

    CAS  Google Scholar 

  38. Barta, C. & Loreto, F. The relationship between the methyl-erythritol phosphate pathway leading to emission of volatile isoprenoids and abscisic acid content in leaves. Plant Physiol. 141, 1676–1683 (2006).

    CAS  PubMed  PubMed Central  Google Scholar 

  39. Loivamäki, M. et al. Arabidopsis, a model to study biological functions of isoprene emission? Plant Physiol. 144, 1066–1078 (2007).

    PubMed  PubMed Central  Google Scholar 

  40. Sasaki, K. et al. Plants utilize isoprene emission as a thermotolerance mechanism. Plant Cell Physiol. 48, 1254–1262 (2007).

    CAS  PubMed  Google Scholar 

  41. Behnke, K. et al. Transgenic, non-isoprene emitting poplars don't like it hot. Plant J. 51, 485–499 (2007).

    CAS  PubMed  Google Scholar 

  42. Molinier, J., Ries, G., Zipfel, C. & Hohn, B. Transgeneration memory of stress in plants. Nature 442, 1046–1049 (2006).

    CAS  PubMed  Google Scholar 

  43. Vickers, C.E. et al. Isoprene synthesis protects transgenic plants from oxidative stress. Plant Cell Environ. published online, doi:10.1111/j.1365–3040.2009.01946.x (22 January 2009).

  44. Delfine, S., Csiky, O., Seufert, G. & Loreto, F. 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, 27–36 (2000).

    CAS  Google Scholar 

  45. Loreto, F. et al. Ozone quenching properties of isoprene and its antioxidant role in leaves. Plant Physiol. 126, 993–1000 (2001).

    CAS  PubMed  PubMed Central  Google Scholar 

  46. Loreto, F. & Velikova, V. Isoprene produced by leaves protects the photosynthetic apparatus against ozone damage, quenches ozone products, and reduces lipid peroxidation of cellular membranes. Plant Physiol. 127, 1781–1787 (2001).

    CAS  PubMed  PubMed Central  Google Scholar 

  47. Ledford, H.K. & Niyogi, K.K. Singlet oxygen and photo-oxidative stress management in plants and algae. Plant Cell Environ. 28, 1037–1045 (2005).

    CAS  Google Scholar 

  48. Affek, H.P. & Yakir, D. Protection by isoprene against singlet oxygen in leaves. Plant Physiol. 129, 269–277 (2002).

    CAS  PubMed  PubMed Central  Google Scholar 

  49. Velikova, V., Edreva, A. & Loreto, F. Endogenous isoprene protects Phragmites australis leaves against singlet oxygen. Physiol. Plant. 122, 219–225 (2004).

    CAS  Google Scholar 

  50. Loreto, F. & Fares, S. Is ozone flux Inside leaves only a damage indicator? Clues from volatile isoprenoid studies. Plant Physiol. 143, 1096–1100 (2007).

    CAS  PubMed  PubMed Central  Google Scholar 

  51. Calogirou, A., Larsen, B.R. & Kotzias, D. Gas-phase terpene oxidation products: a review. Atmos. Environ. 33, 1423–1439 (1999).

    CAS  Google Scholar 

  52. Duhl, T.R., Helmig, D. & Guenther, A. Sesquiterpene emissions from vegetation: a review. Biogeosciences Discuss. 4, 3987–4023 (2007).

    Google Scholar 

  53. Helmig, D., Bocquet, F., Pollmann, J. & Revermann, T. Analytical techniques for sesquiterpene emission rate studies in vegetation enclosure experiments. Atmos. Environ. 38, 557–572 (2004).

    CAS  Google Scholar 

  54. Siwko, M.E. et al. Does isoprene protect plant membranes from thermal shock? A molecular dynamics study. Biochim. Biophys. Acta 1768, 198–206 (2007).

    CAS  PubMed  Google Scholar 

  55. Milne, P.J., Riemer, D.D., Zika, R.G. & Brand, L.E. Measurement of vertical distribution of isoprene in surface seawater, its chemical fate, and its emission from several phytoplankton monocultures. Mar. Chem. 48, 237–244 (1995).

    CAS  Google Scholar 

  56. Logan, B.A. & Monson, R.K. Thermotolerance of leaf discs from four isoprene-emitting species is not enhanced by exposure to exogenous isoprene. Plant Physiol. 120, 821–826 (1999).

    CAS  PubMed  PubMed Central  Google Scholar 

  57. Logan, B.A., Anchordoquy, T.J., Monson, R.K. & Pan, R.S. The effect of isoprene on the properties of spinach thylakoids and phosphatidylcholine liposomes. Plant Biol. (Stuttg) 1, 602–606 (1999).

    CAS  Google Scholar 

  58. Velikova, V. et al. Isoprene decreases the concentration of nitric oxide in leaves exposed to elevated ozone. New Phytol. 166, 419–425 (2005).

    CAS  PubMed  Google Scholar 

  59. Thompson, A.M. The oxidizing capacity of the earth's atmosphere - probable past and future changes. Science 256, 1157–1165 (1992).

    CAS  PubMed  Google Scholar 

  60. Monson, R.K. & Holland, E.A. Biospheric trace gas fluxes and their control over tropospheric chemistry. Annu. Rev. Ecol. Syst. 32, 547–576 (2001).

    Google Scholar 

  61. Pierce, T. et al. Influence of increased isoprene emissions on regional ozone modeling. J. Geophys. Res. Atmos. 103, 25611–25629 (1998).

    CAS  Google Scholar 

  62. Mullineaux, P.M., Karpinski, S. & Baker, N.R. Spatial dependence for hydrogen peroxide-directed signaling in light-stressed plants. Plant Physiol. 141, 346–350 (2006).

    CAS  PubMed  PubMed Central  Google Scholar 

  63. Mullineaux, P. et al. Are diverse signalling pathways integrated in the regulation of Arabidopsis antioxidant defence gene expression in response to excess excitation energy? Phil. Trans. R. Soc. Lond. B 355, 1531–1540 (2000).

    CAS  Google Scholar 

  64. Munné-Bosch, S. & Alegre, L. The function of tocopherols and tocotrienols in plants. Crit. Rev. Plant Sci. 21, 31–57 (2002).

    Google Scholar 

  65. Sauer, F., Schäfer, C., Neeb, P., Horie, O. & Moorgat, G.K. Formation of hydrogen peroxide in the ozonolysis of isoprene and and simple alkenes under humid conditions. Atmos. Environ. 33, 229–241 (1999).

    CAS  Google Scholar 

  66. Fares, S., Loreto, F., Kleist, E. & Wildt, J. Stomatal uptake and stomatal deposition of ozone in isoprene and monoterpene emitting plants. Plant Biol. (Stuttg) 10, 44–54 (2008).

    CAS  Google Scholar 

  67. Alméras, E. et al. Reactive electrophile species activate defense gene expression in Arabidopsis. Plant J. 34, 205–216 (2003).

    PubMed  Google Scholar 

  68. Santos, L.S., Dalmazio, I., Eberlin, M.N., Claeys, M. & Augusti, R. 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, 2104–2108 (2006).

    CAS  PubMed  Google Scholar 

  69. Zeidler, J.G., Lichtenthaler, H.K., May, H.U. & Lichtenthaler, F.W. Is isoprene emitted by plants synthesized via the novel isopentenyl pyrophosphate pathway? Z. Naturforsch. 52c, 15–23 (1997).

    Google Scholar 

  70. Foyer, C., Trebst, A. & Noctor, G. Signaling and integration of defense functions of tocopherol, ascorbate and glutathione. in Photoprotection, Photoinhibition, Gene Regulation, and Environment (eds. Demmig-Adams, B., Adams, W.W. III & Mattoo, A.K.) 241–268 (Springer, Dordrecht, The Netherlands, 2006).

    Google Scholar 

  71. Triantaphylides, C. et al. Singlet oxygen is the major reactive oxygen species involved in photooxidative damage to plants. Plant Physiol. 148, 960–968 (2008).

    CAS  PubMed  PubMed Central  Google Scholar 

  72. Pasqualini, S. et al. Ozone-induced cell death in tobacco cultivar Bel W3 plants. The role of programmed cell death in lesion formation. Plant Physiol. 133, 1122–1134 (2003).

    CAS  PubMed  PubMed Central  Google Scholar 

  73. Gould, K.S., Lamotte, O., Klinguer, A., Pugin, A. & Wendehenne, D. Nitric oxide production in tobacco leaf cells: a generalized stress response? Plant Cell Environ. 26, 1851–1862 (2003).

    CAS  Google Scholar 

  74. Wilson, I.D., Neill, S.J. & Hancock, J.T. Nitric oxide synthesis and signalling in plants. Plant Cell Environ. 31, 622–631 (2008).

    CAS  PubMed  Google Scholar 

  75. Beligni, M.V. & Lamattina, L. Nitric oxide interferes with plant photo-oxidative stress by detoxifying reactive oxygen species. Plant Cell Environ. 25, 737–748 (2002).

    CAS  Google Scholar 

  76. Velikova, V., Fares, S. & Loreto, F. Isoprene and nitric oxide reduce damages in leaves exposed to oxidative stress. Plant Cell Environ. 31, 1882–1894 (2008).

    CAS  PubMed  Google Scholar 

  77. Harley, P.C., Monson, R.K. & Lerdau, M.T. Ecological and evolutionary aspects of isoprene emission from plants. Oecologia 118, 109–123 (1999).

    PubMed  Google Scholar 

  78. Sharkey, T.D. et al. Evolution of the isoprene biosynthetic pathway in kudzu. Plant Physiol. 137, 700–712 (2005).

    CAS  PubMed  PubMed Central  Google Scholar 

  79. Harley, P., Guenther, A. & Zimmerman, P. Environmental controls over isoprene emission in deciduous oak canopies. Tree Physiol. 17, 705–714 (1997).

    CAS  PubMed  Google Scholar 

  80. Loreto, F. et al. Different sources of reduced carbon contribute to form three classes of terpenoid emitted by Quercus ilex L. leaves. Proc. Natl. Acad. Sci. USA 93, 9966–9969 (1996).

    CAS  PubMed  Google Scholar 

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

    CAS  PubMed  Google Scholar 

  82. Loreto, F. 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, 185–192 (2002).

    Google Scholar 

  83. Lerdau, M. A positive feedback with negative consequences. Science 316, 212–213 (2007).

    CAS  PubMed  Google Scholar 

  84. Rosenstiel, T.N., Potosnak, M.J., Griffin, K.L., Fall, R. & Monson, R.K. Increased CO2 uncouples growth from isoprene emission in an agriforest ecosystem. Nature 421, 256–259 (2003).

    CAS  PubMed  Google Scholar 

  85. Loreto, F. et al. The relationship between isoprene emission rate and dark respiration rate in white poplar (Populus alba L.) leaves. Plant Cell Environ. 30, 662–669 (2007).

    CAS  PubMed  Google Scholar 

  86. Scheel, D. & Wasternac, C. Plant Signal Transduction (Oxford University Press, Oxford, 2002).

    Google Scholar 

  87. Schilmiller, A.L. & Howe, G.A. Systemic signaling in the wound response. Curr. Opin. Plant Biol. 8, 369–377 (2005).

    CAS  PubMed  Google Scholar 

  88. Jenks, M.A. & Hasegawa, P.M. Plant Abiotic Stress (Blackwell, Oxford, 2005).

    Google Scholar 

  89. Hirt, H. & Shinozaki, K. Plant Responses to Abiotic Stress (Springer, Berlin, 2004).

    Google Scholar 

  90. Zhu, J.K. Salt and drought stress signal transduction in plants. Annu. Rev. Plant Biol. 53, 247–273 (2002).

    CAS  PubMed  PubMed Central  Google Scholar 

  91. Krieger-Liszkay, A. Singlet oxygen production in photosynthesis. J. Exp. Bot. 56, 337–346 (2005).

    CAS  PubMed  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Claudia E Vickers.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Vickers, C., Gershenzon, J., Lerdau, M. et al. A unified mechanism of action for volatile isoprenoids in plant abiotic stress. Nat Chem Biol 5, 283–291 (2009). https://doi.org/10.1038/nchembio.158

Download citation

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1038/nchembio.158

This article is cited by

Search

Quick links

Nature Briefing

Sign up for the Nature Briefing newsletter — what matters in science, free to your inbox daily.

Get the most important science stories of the day, free in your inbox. Sign up for Nature Briefing