Abstract
Biogenic isoprene was discovered in the mid-1950s as a component of volatile substances emitted from leaves. In plant species emitting isoprene under illumination, this process is closely related to photosynthesis. Thus, a photobiological phenomenon termed “isoprene effect” or isoprene emission (IE) was discovered. Subsequent studies showed that leaves are capable of releasing isoprene also in darkness, though at a rate two orders of magnitude lower than that in illuminated leaves. It is presently known that the isoprene is emitted not by all plant species from various taxonomic groups, whereas the dark release of isoprene occurs in cells of all living organisms. This review presents a brief historical account of studies dealt with IE. A special emphasis is placed on the roles of light as an energy source and of CO2 as a carbon source; these factors create the energy–metabolite flow that runs through the green photosynthesizing cell. The data available suggest that IE can be considered as a manifestation of excretory function of the leaf. An attempt is made to describe IE from the standpoint of thermodynamics of irreversible processes. It is shown that the cell represents a dissipative structure whose organization and stability is provided by irreversible processes running far from equilibrium. General view on isoprene emission is that it results from regulated conversions of carbon and free energy in a series of photosynthetic reactions under stressful conditions caused by CO2 deficit inside illuminated autotrophic cells. This stress generates the energy overflow, far in excess of the energy-consuming capacity. The necessity of discharging this energy excess is dictated by the fact that the living cell is a dissipative structure.
REFERENCES
Sanadze, G.A., Emission of Gaseous Organic Sub-stances from Plants, Rep. Akad. Nauk GruzSSR, 1956, vol. 17, pp. 429–433.
Sanadze, G.A., Nature of Gaseous Substances from the Robinia pseudoacacia Leaves, Rep. Akad. Nauk GruzSSR, 1957, vol. 19, pp. 83–86.
Sanadze, G.A., Seasonal Dynamics of Gaseous Organic Substances Emission from Leaves, Tez. X nauchn. konf. aspirantov i molodykh nauchnykh rabotnikov (Abst. X Conf. Post-Graduate Students and Young Scientists), Tbilisi, 1959, p. 130.
Sanadze, G.A., Hydroxylamine-Inhibited Emission of Gaseous Phytogenic Substances, Sbornik dokl. aspirantov i molodykh nauchnykh rabotnikov (Proc. Rep. Post-Graduate Students and Young Scientists), Tbilisi: Akad. Nauk GruzSSR, 1960, pp 55–59.
Sanadze, G.A. and Dolidze, G.M., Mass-Spectrometric Identification of C5 H8 (Isoprene)-Type Compound from Gaseous Excrete from Plant Leaves, Rep. Akad. Nauk GruzSSR, 1961, vol. 27, pp. 747–750.
Sanadze, G.A., Light and Gaseous Organic Metabolites from Plants, Rep. Akad. Nauk GruzSSR, 1959, vol. 22, pp. 449–454.
Sanadze, G.A., Conditions for Diene C5 H8 (Isoprene) Emission from Leaves, Fiziol. Rast., 1964, vol. 2, pp. 49–52 (Sov. Plant Physiol., Engl. Transl.).
Sanadze, G.A., Biosynthesis and Light-Dependent Isoprene Emission from Leaves, Doctoral (Biol.) Dissertation, Moscow: Inst. Plant Physiol., 1967.
Sanadze, G.A., Light-Dependent Emission of Molecular Isoprene, Progr. Photosynth. Res., 1969, vol. 2, pp. 701–707.
Sanadze, G.A., Mgaloblishvili, M.P., and Dalakishvili, K.G., The Influence of Tserulenine, Phosphoorganic Substances, and Synthetic Carbohydrates on the CO2 Assimilation and Isoprene Effect in Isolated Protoplasts from Poplar Leaves, Fiziol. Rast., 1990, vol. 37, pp. 6–11 (Sov. Plant Physiol., Engl. Transl.).
Deneris, E.S., Stein, R.A., and Mead, J.F., Acid-Catalyzed Formation of Isoprene from a Mevalonate-Derived Product Using a Rat Liver Cytosolic Fraction, J. Biol. Chem., 1985, vol. 260, pp. 1382–1385.
Sanadze, G.A., Emission of Gaseous Organic Substances from Plants, Sbornik dokl. aspirantov i molodykh nauchnykh rabotnikov (Proc. Rep. Post-Graduate Students and Young Scientists), Tbilisi: Akad. Nauk GruzSSR, 1961, pp. 75–79.
Prigozhin, I. and Stengers, I., Poryadok iz khaosa: Novyi dialog cheloveka s prirodoi (The Order from Chaos: New Dialog between Man and Nature), Moscow: Progress, 1986.
Prigozhin, I. and Kondepudi, D., Sovremennaya termodinamika. Ot teplovykh mashin do dissipativnykh struktur (Current Thermodynamics: From Heat Engines to Dissipative Structures), Moscow: Mir, 2002.
Molish, H., Der Einfluss einer Pflanze auf die Andere, Allelopatie (Jena), 1937, p. 3.
Rasmussen, R.A., Isoprene: Identified as a Forest-Type Emission to the Atmosphere, Environ. Sci. Technol., 1970, vol. 4, pp. 667–671.
Sanadze, G.A. and Chiabrishvili, H., Use of NMR-Spectroscopy for Identification of Phytogenic Isoprene, Fiziol. Rast., 1972, vol. 23, pp. 1070–1073 (Sov. Plant Physiol., Engl. Transl.).
Sanadze, G.A., Light-Dependent Mechanism of Diene C5 H8 (Isoprene) Origin in Plant Leaves, Fiziol. Rast., 1966, vol. 13, pp. 753–761 (Sov. Plant Physiol., Engl. Transl.).
Gaffron, H., Energy Storage: Photosynthesis, Plant Physiology, Steward, F.C., Ed., New York: Academic, 1960.
Voskresenskaya, N.P., Fotosintez i spektral'nyi sostav sveta (Photosynthesis and Light Quality), Moscow: Nauka, 1965.
Galston, A., Davies, P., and Satter, R., The Life of the Green Plant, New Jersey: Prentice-Hall, 1983.
Polevoi, V.V., Fiziologiya rastenii (Plant Physiology), Moscow: Vysshaya Shkola, 1989.
Loreto, F. and Sharkey, T.D., A Gas Exchange Study of Photosynthesis and Isoprene Emission in Quercus rubra, L., Planta, 1991, vol. 182, pp. 523–531.
Sharkey, T.D. and Yeh, S., Isoprene Emission from Plants, Annu. Rev. Plant Physiol. Plant Mol. Biol., 2001, vol. 52, pp. 407–436.
Mgaloblishvili, M.P., Khetsuriani, N.D., and Sanadze, G.A., The Influence of Cycloheximide and Chloramphenicol on the Activity of Isolated Chloroplasts, Photosynthesis, and Isoprene Effect in Poplar Leaves, Tez. dokl. 2-i resp. nauchn. konf. po vopr. biokhimii rast. (Abst. the 2nd Republ. Conf. Plant Biochemistry), Tbilisi: Akad. Nauk GruzSSR, 1977, p. 137.
Mgaloblishvili, M.P., Khetsuriani, N.D., Kalandadze, A.N., and Sanadze, G.A., Localization of Isoprene Biosynthesis in the Chloroplasts of Poplar Leaves, Fiziol. Rast., 1978, vol. 25, pp. 1055–1061 (Sov. Plant Physiol., Engl. Transl.).
Baazov, D.I. and Sanadze, G.A., Action Spectrum and an Increase in the Isoprene Emission from Poplar Leaves, Fiziol. Rast., 1987, vol. 34, pp. 213–220 (Sov. Plant Physiol., Engl. Transl.).
Tarkhnishvili, G.M., Kalandadze, A.N., and Sanadze, G.A., The Influence of Partial Pressure of CO2 in the Atmosphere on the Rate of Isoprene Synthesis by Poplar Leaves under Saturating Light Intensity, Rep. Akad. Nauk GruzSSR, 1985, vol. 119, pp. 173–176.
Tarkhnishvili, G.M., Isoprene Effects and Gas Exchange in Poplar Leaves, Cand. Sci. (Biol.) Dissertation, Tbilisi: Tbilis. Gos. Univ., 1988.
Affek, H. and Yakir, D., Natural Abundance Carbon Isotope Composition of Isoprene Reflects Incomplete Coupling between Isoprene Synthesis and Photosynthetic Carbon Flow, Plant Physiol., 2003, vol. 131, pp. 1727–1736.
Egorova, E.A., Bukhov, N.G., Heber, U., Samson, G., and Carpentier, R., Effect of the Pool Size of Stromal Reductants on the Alternative Pathway of Electron Transfer to Photosystem I in Chloroplasts of Intact Leaves, Fiziol. Rast., 2003, vol. 50, pp. 485–495 (Russ. J. Plant Physiol., Engl. Transl.).
Sanadze, G.A., Mgaloblishvili, M.P., and Dalakishvili, K.G., Independence of Carbohydrate Exchange Pathways in the Reactions of Benson–Calvin Cycle and Isoprene Effects, Fiziol. Rast., 1986, vol. 23, pp. 856–863 (Sov. Plant Physiol., Engl. Transl.).
Lyutova, M.N., Karpilova, I.F., Sharkova, V.E., and Romanova, A.K., The Influence of Temperature on the Ribulosodiphosphate Carboxylase from Cucumber and Melon Leaves, Fiziol. Rast., 1985, vol. 32, pp. 1041–1045 (Sov. Plant Physiol., Engl. Transl.).
Lehninger, A.L., Principles of Biochemistry, Worth Publ., 1982, vol. 2.
Goodwin, T.W. and Mercer, E.I., Introduction to Plant Biochemistry, Oxford: Pergamon, 1986, vol. 2.
Heber, U., Conformational Changes of Chloroplasts Induced by Illumination of Leaves In Vivo, Biochim. Biophys. Acta, 1969, vol. 180, pp. 302–319.
Mehler, A.H., Studies on the Reaction of Illuminated Chloroplasts, Arch. Biochem. Biophys., 1951, vol. 34, pp. 339–351.
Sharkey, T.D. and Singsaas, E.L. Why Plants Emit Isoprene, Nature, 1995, vol. 374, p. 769.
Rhomer, M., Khani, M., Simonin, P., and Sahm, H., Isoprenoid Biosynthesis in Bacteria: A Novel Pathway for the Early Steps Leading to Isopentenyl Diphosphate, Biochem. J., 1993, vol. 295, pp. 517–524.
Lichtenthaler, H.K., Schwender, J., Disch, A., and Rohmer, M., Biosynthesis of Isoprenoids in Higher Plant Chloroplasts Proceeds via a Mevalonate-Independent Pathway, FEBS Lett., 1997, vol. 400, pp. 271–274.
Kalandadze, A.N., The Influence of Inhibitors of Metabolism on the Isoprene Emission from Populus nigra Leaves:, Cand. Sci. (Biol.) Dissertation, Tbilisi: Tbilis. Gos. Univ., 1967.
Smillie, R.M., Bishop, D.J., Jibbons, J.C., Graham, D., Gnieve, A.M., Raison, J.K., and Reger, B.J., Determination of the Sites of Synthesis of Proteins and Lipids of the Chloroplast Using Chloramphenicol and Cycloheximide, Anatomy and Biogenesis of Mitochondria and Chloroplasts, Amsterdam: North-Holland, 1971, pp. 422–433.
Sanadze, G.A., Isoprene Effect–Light-Dependent Emission of Isoprene by Green Parts of Plants, Trace Gas Emission by Plants, San Diego: Academic, 1991, pp. 135–152.
Sanadze, G.A. and Dzhaiani, G.I., Carbohydrate Partition within Isoprene Molecule from Photosynthetically Assimilated CO2, Fiziol. Rast., 1972, vol. 19, pp. 1082–1089 (Sov. Plant Physiol., Engl. Transl.).
Tingey, D.T., Manning, M., Grothaus, L., and Burns, W.F., The Influence of Light and Temperature on Isoprene Emission Rates from Live Oak, Physiol. Plant., 1979, vol. 47, pp. 112–118.
Tingey, D.T., Evans, R.C., and Gumpertz, M.L., Effects of Environmental Conditions on Isoprene Emission from Live Oak, Planta, 1981, vol. 152, pp. 565–570.
Tingey, D.T., Evans, R.C., Bates, E.H., and Gumpertz, M.L., Isoprene Emission and Photosynthesis in Three Ferns—the Influence of Light and Temperature, Physiol. Plant., 1987, vol. 69, pp. 609–616.
Rabinovich, E., Fotosintez (Photosynthesis), Moscow: Inostrannaya Literatura, 1951, vol. 1.
Slobodskaya, G.A., Nitrates Assimilation by Photosynthesizing Leaves, Fiziol. Rast., 1968, vol. 15, pp. 511–520 (Sov. Plant Physiol., Engl. Transl.).
Nathan, C., Nitric Oxide as a Secretory Product of Mammalian Cells, FASEB J., 1992, vol. 6, pp. 3051–3064.
Rasmussen, R.A. and Went, F.W., Volatile Organic Material of Plant Origin in the Atmosphere, Proc. Natl. Acad. Sci. USA, 1964, vol. 53, p. 215.
Rasmussen, R.A. and Jones, C.A., Emission of Isoprene from Leaf Discs of Hamamelis, Phytochemistry, 1973, vol. 12, pp. 15–19.
Rasmussen, R.A. and Khalil, M.A.K., Isoprene over the Amazon Basin, J. Geophys. Res., 1988, vol. 93, pp. 1417–1421.
Loomis, D.W. and Croteau, R., Biochemistry of Terpenoids, The Biochemistry of Plants: A Comprehensive Treatise, Stumph, P.K., Ed., New York: Academic, 1980, vol. 4, pp. 364–410.
Khananashvili, O.V. and Sanadze, G.A., Localization of Acetyl-CoA Synthetase in the Chloroplasts of Poplar Leaves, Fiziol. Rast., 1980, vol. 27, pp. 327–335 (Sov. Plant Physiol., Engl. Transl.).
Sanadze, G.A. and Tarkhnishvili, G.M., Effects of Molecular Oxygen on the Isoprene Biosynthesis in Leaves under Saturating Light Intensity, Dokl. Akad. Nauk SSSR, 1986, vol. 286, pp. 501–503.
Fehsenfeld, F.C., Calvert, J., Fall, R., Goldan, P., and Guenther, A.B., Emissions of Volatile Organic Compounds from Vegetation and the Implications for Atmospheric Chemistry, Global Biogeochemical Cycles, 1992, vol. 6, pp. 389–430.
Harley, P.C., Monson, R.K., and Lerdau, M.T., Ecological and Evolutionary Aspects of Isoprene Emission from Plants, Oecologia, 1999, vol. 118, pp. 109–123.
Kesselmeier, J. and Staudt, M., Biogenic Volatile Organic Compounds (VOC): An Overview on Emission, Physiology and Ecology, J. Atmos. Chem., 1999, vol. 33, pp. 23–88.
Fuentes, J.D., Lerdau, M., Atkinson, R., Baldocchi, D., and Bottenheim, J.W., Biogenic Hydrocarbons in the Atmospheric Boundary Layer: A Review, Bull. Am. Meteorol. Soc., 2000, vol. 81, pp. 1537–1575.
Silver, G.M. and Fall, R., Enzymatic Synthesis of Isoprene from Dimethylallyl Diphosphate in Aspen Leaf Extracts, Plant Physiol., 1991, vol. 97, pp. 1588–1591.
Shnitzler, J.-P., Arenz, R., Steinbrecher, R., and Lehning, A., Characterization of an Isoprene Synthase from Leaves of Quercus petrae (Mattuschka), Liebl. Bot. Acta, 1996, vol. 109, pp. 216–221.
Wildermuth, M.C., Subcellular Location and Biophysical Regulation of Foliar Isoprene Production (Chloroplasts), Cand. Sci. (Biol.) Thesis, Boulder, USA: Univ. Colorado, 1997, p. 307.
Wildermuth, M. and Fall, R., Light-Dependent Isoprene Emission – Characterization of Thylakoid-Bound Isoprene Synthase in Salix dicolor Chloroplasts, Plant Physiol., 1996, vol. 112, pp. 171–182.
Kuzma, J. and Fall, R., Leaf Isoprene Emission Rate Is Dependent on Leaf Development and the Level of Isoprene Synthase, Plant Physiol., 1993, vol. 101, pp. 435–440.
Kuzma, J., Nemecek-Marshall, M., Pollok, W.H., and Fall, R., Bacteria Produce the Volatile Hydrocarbon Isoprene, Curr. Microbiol., 1995, vol. 30, pp. 97–103.
Datukishvili, N.T., Tarkhnishvili, G.M., Mikeladze, D.G., Beridze, T.G., and Sanadze, G.A., Isolation and Purification of Protein Responsible for the Conversion of Dimethylallyl Pyrophosphate from Poplar Leaves into Isoprene, Fiziol. Rast., 2001, vol. 48, pp. 257–261 (Russ. J. Plant Physiol., Engl. Transl.).
Loreto, F. and Sharky, T.D., A Gas Exchange Study of Photosynthesis and Isoprene Emission in Quercus rubra, L., Planta, 1990, vol. 182, pp. 523–531.
Fall, R. and Monson, R.K., Isoprene Emission Rate and Intercellular Isoprene Concentration as Influenced by Stomatal Distribution and Conductance, Plant Physiol., 1992, vol. 100, pp. 987–992.
Zimmerman, P.R., Chatfield, R.B., Fishman, J., Crutzen, P.J., and Hanst, P.L., Estimation of the Production of CO2 and H2 from the Oxidation of Hydrocarbon Emission from Vegetation Isoprene, Geophys. Rev. Lett., 1978, vol. 5, pp. 679–682.
Zimmerman, P.R., Determination of Emission Rates of Hydrocarbons from Indigenous Species of Vegetation in the Tampa/St. Petersberg, Florida Area, EPA Rep., 1979, vol. 904/977, pp. 1-104.
Zimmerman, P.R., Greenberg, J.P., and Westberg, C.E., Measurements of Atmospheric Hydrocarbons and Biogenic Emission Fluxes in the Amazon Boundary Layer, J. Geophys. Res., 1988, vol. 93, pp. 1407–1416.
Monson, R.K., Guenther, A.B., and Fall, R., Physiological Reality in Relation to Ecosystem-and Global-Level Estimates of Isoprene Emission, Trace Gas Emissions, Sharkey, T.D., Ed., New York: Academic, 1991, pp. 185–206.
Rosenstiel, T.N., Potosnak, M.J., Griffin, K.L., Fall, R., and Monson, R.K., Increased CO2Uncouples Growth from Isoprene Emission in an Agriforest Ecosystem, Nature, 2003, vol. 421, pp. 256–259.
Hanson, D.T., Swanson, S., Graham, L.E., and Sharky, T.D., Evolutionary Significance of Isoprene Emission from Mosses, Am. J. Bot., 1999, vol. 86, pp. 634–639.
Logan, B.A. and Monson, R.K., Thermotolerance of Leaf Discs from Four Isoprene-Emitting Species Is Not Enhanced by Exposure to Exogenous Isoprene, Plant Physiol., 1999, vol. 120, pp. 821–825.
Wagner, W.P. and Nemeček-Marshall, M., Three Distinct Phases of Isoprene Formation during Growth and Sporulation of Bacillus subtilis, J. Bacteriol., 1999, vol. 181, pp. 4700–4703.
Logan, B.A., Monson, R.K., and Potosnak, M.J., Biochemistry and Physiology of Foliar Isoprene Production, Trends Plant Sci., 2000, vol. 5, pp. 477–481.
Prigozhin, I., Konets opredelennosti: vremya, khaos i novye zakony prirody (The End of Definiteness: Time, Chaos, and New Laws of Nature), Izhevsk: Nauch. Issled. Tsentr "Regulyarnaya i khaoticheskaya dinamika", 2001.
Nemeček-Marshall, M., MacDonald, R., Franzen, J., Wojciechowski, Ch., and Fall, R., Methanol Emission from Leaves, Plant Physiol., 1995, vol. 108, pp. 1359–1368.
Author information
Authors and Affiliations
Rights and permissions
About this article
Cite this article
Sanadze, G.A. Biogenic Isoprene (A Review). Russian Journal of Plant Physiology 51, 729–741 (2004). https://doi.org/10.1023/B:RUPP.0000047821.63354.a4
Issue Date:
DOI: https://doi.org/10.1023/B:RUPP.0000047821.63354.a4