Download PDF
Plant Biol (Stuttg) 2007; 9: e79-e86
DOI: 10.1055/s-2007-965239
Research Paper

Georg Thieme Verlag Stuttgart KG · New York

Foliar Limonene Uptake Scales Positively with Leaf Lipid Content: “Non-Emitting” Species Absorb and Release Monoterpenes

S. M. Noe1 , L. Copolovici2 , Ü. Niinemets1 , 3 , E. Vaino1
  • 1Department of Plant Physiology, University of Tartu, Riia 23, 51010 Tartu, Estonia
  • 2Department of Inorganic Chemistry, Babes-Bolay University, 11 Arany Janos, 400028 Cluj-Napoca, Romania
  • 3Institute of Agricultural and Environmental Sciences, Estonian University of Life Sciences, Kreutzwaldi 64, 51014 Tartu, Estonia
Further Information

Publication History

Received: December 11, 2006

Accepted: March 9, 2007

Publication Date:
12 June 2007 (online)

   Permissions and Reprints

Abstract

Monoterpenes synthesized and released by emitting vegetation can be taken up by neighboring non-emitting plants, but the uptake capacity of non-emitting species has not been studied extensively. We investigated the foliar uptake potential of the hydrophobic monoterpene limonene in 13 species of contrasting leaf structure and lipid content to determine the structural and chemical controls of monoterpene uptake. Leaf dry mass per unit area (M A,D) varied 6.5-fold, dry to fresh mass ratio (D F) 2.7-fold, lipid content per dry mass (L M) 2.5-fold and per unit area (L A) 4.6-fold across the studied species. Average foliar limonene uptake rate (U A) from air at saturating limonene partial pressures varied from 0.9 to 6 nmol m−2 s−1, and limonene leaf to air partition coefficient (K FA, ratio of limonene content per dry mass to limonene partial pressure) from 0.7 to 6.8 µmol kg−1 Pa−1. U A and K FA scaled positively with leaf lipid content, and were independent of D F, indicating that variation in leaf lipid content was the primary determinant of species differences in monoterpene uptake rate and K FA. Mass-based limonene uptake rates further suggested that thinner leaves with greater surface area per unit dry mass have higher uptake rates. In addition, limonene lipid to air partition coefficient (K LA = K FA/L M) varied 19-fold, indicating large differences in limonene uptake capacity at common leaf lipid content. We suggest that the significant uptake of hydrophobic monoterpenes when monoterpene ambient air concentration is high and release when the concentration is low should be included in large-scale monoterpene emission models.

Key words

Lipid content - monoterpene uptake - monoterpenes in non-emitting species - partition coefficients.

References

  • 1 Andreae M. O., Artaxo P., Brandao C., Carswell F. E., Ciccioli P., da Costa A. L., Culf A. D., Esteves J. L., Gash J. H. C., Grace J., Kabat P., Lelieveld J., Malhi Y., Manzi A. O., Meixner F. X., Nobre A. D., Nobre C., Ruivo M., Silva-Dias M. A., Stefani P., Valentini R., von Jouanne J., Waterloo M. J.. Biogeochemical cycling of carbon, water, energy, trace gases, and aerosols in Amazonia: the LBA-EUSTACH experiments.  Journal of Geophysical Research – Atmospheres. (2002);  107 D20
    PubMedGoogle Scholar
  • 2 Aziz A., Larher F.. Osmotic stress induced changes in lipid composition and peroxidation in leaf discs of Brassica napus L.  Journal of Plant Physiology. (1998);  153 754-762
    PubMedGoogle Scholar
  • 3 Bauer K., Garbe D., Surburh H.. Flavors and fragrances. Ullmann's Encyclopedia of Industrial Chemistry. The CD‐ROM Edition. Berlin; Wiley-VCH Verlag (1998)
    Google Scholar
  • 4 Baur P., Marzouk H., Schönherr J.. Estimation of path lengths for diffusion of organic compounds through leaf cuticles.  Plant, Cell and Environment. (1999);  22 291-299
    CrossrefPubMedGoogle Scholar
  • 5 Benjamin M. T., Sudol M., Bloch L., Winer A. M.. Low-emitting urban forests: a taxonomic methodology for assigning isoprene and monoterpene emission rates.  Atmospheric Environment. (1996);  30 1437-1452
    CrossrefPubMedGoogle Scholar
  • 6 Benjamin M. T., Sudol M., Vorsatz D., Winer A. M.. A spatially and temporally resolved biogenic hydrocarbon emissions inventory for the California South Coast Air Basin.  Atmospheric Environment. (1997);  31 3087-3100
    CrossrefPubMedGoogle Scholar
  • 7 Bertin N., Staudt M.. Effect of water stress on monoterpene emissions from young potted holm oak (Quercus ilex L.) trees.  Oecologia. (1996);  107 456-462
    CrossrefPubMedGoogle Scholar
  • 8 Blande J. D., Tiiva P., Freiwald V., Oksanen E., Holopainen J. K.. The effects of herbivore damage and elevated ozone concentration on the volatile terpenoids produced by two hybrid aspen (Populus tremula × tremuloides) clones. In Abstracts. XVII International Botanical Congress, Vienna, Austria, 17 – 23 July 2005, Vienna. (2005): 1-544
    Google Scholar
  • 9 Brown R. L., Stein S. E.. Boiling point data. Linstrom, P. J. and Mallard, W. G., eds. NIST Chemistry WebBook.  http://webbook.nist.gov Gaithersburg, MD; National Institute of Standards and Technology (2001)
    Google Scholar
  • 10 Chameides W., Lindsay R., Richardson J., Kiang C.. The role of biogenic hydrocarbons in urban photochemical smog: Atlanta as a case study.  Science. (1988);  241 1473-1475
    PubMedGoogle Scholar
  • 11 Ciccioli P., Brancaleoni E., Cecinato A., Sparapani R., Frattoni M.. Identification and determination of volatile organic compounds in forest areas of Northern and Southern Europe and remote sites of the Himalaya region by high-resolution gas chromatography-mass spectrometry.  Journal of Chromatography A. (1993);  643 55-69
    CrossrefPubMedGoogle Scholar
  • 12 Ciccioli P., Cecinato A., Brancaleoni E., Frattoni M.. Identification and quantitative evaluation of C4-C14 volatile organic compounds in some urban, suburban and forest sites in Italy.  Fresenius Environonmental Bulletin. (1992);  1 73-78
    PubMedGoogle Scholar
  • 13 Copolovici L. O., Filella I., Llusià J., Niinemets Ü., Peñuelas J.. The capacity for thermal protection of photosynthetic electron transport varies for different monoterpenes in Quercus ilex.  Plant Physiology. (2005);  139 485-496
    CrossrefPubMedGoogle Scholar
  • 14 Copolovici L. O., Niinemets Ü.. Temperature dependencies of Henry's law constants and octanol/water partition coefficients for key plant volatile monoterpenoids.  Chemosphere. (2005);  61 1390-1400
    CrossrefPubMedGoogle Scholar
  • 15 Daubert T. E., Danner R. P., Sibul H. M., Stebbins C. C.. Physical and Thermodynamic Properties of Pure Chemicals: Data Compilation. Washington, DC; Taylor and Francis (1998)
    Google Scholar
  • 16 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.  The New Phytologist. (2000);  146 27-36
    CrossrefPubMedGoogle Scholar
  • 17 Diamantoglou S., Rhizopoulou S., Herbig A., Kull U.. Seasonal trends in energy content and storage substances in the mediterranean shrub Ephedra.  Acta Oecologica/Oecologia Plantarum. (1989);  10 263-274
    PubMedGoogle Scholar
  • 18 Fichan I., Larroche C., Gros J. B.. Water solubility, vapor pressure, and activity coefficients of terpenes and terpenoids.  Journal of Chemical and Engineering Data. (1999);  44 56-62
    CrossrefPubMedGoogle Scholar
  • 19 Fischbach R. J., Staudt M., Zimmer I., Rambal S., Schnitzler J. P.. Seasonal pattern of monoterpene synthase activities in leaves of the evergreen tree Quercus ilex.  Physiologia Plantarum. (2002);  114 354-360
    CrossrefPubMedGoogle Scholar
  • 20 França Faria M. A., de Sá C. F., Lima G. R., Filho J. I. B. C., Martins R. J., de Cardoso M. M. J. E., Barcia O. E.. Measurement of density and viscosity of binary 1-alkanol systems (C8-C11) at 101 kPa and temperatures from (283.15 to 313.15) K.  Journal of Chemical and Engineering Data. (2005);  50 1938-1943
    CrossrefPubMedGoogle Scholar
  • 21 Fuentes J. D., Lerdau M., Atkinson R., Baldocchi D., Bottenheim J. W., Ciccioli P., Lamb B., Geron C., Gu L., Guenther A., Sharkey T. D., Stockwell W.. Biogenic hydrocarbons in the atmospheric boundary layer: a review.  Bulletin of the American Meteorological Society. (2000);  81 1537-1575
    CrossrefPubMedGoogle Scholar
  • 22 Gershenzon J., Croteau R. B.. Terpenoid biosynthesis: the basic pathway and formation of monoterpenes, sesquiterpenes, and diterpenes. Moore, T. S., ed. Lipid Metabolism in Plants. Boca Raton, Ann Arbor, London, Tokyo; CRC Press (1993): 339-388
    Google Scholar
  • 23 Gleizes M., Pauly G., Bernard-Dagan C., Belingheri L.. Conditions of monoterpene and sesquiterpene biosynthesis in Pinus and Citus species.  Biochemical Society Transactions. (1983);  11 590
    PubMedGoogle Scholar
  • 24 Guenther A., Geron C., Pierce T., Lamb B., Harley P., Fall R.. Natural emissions of non-methane volatile organic compounds, carbon monoxide, and oxides of nitrogen from North America.  Atmospheric Environment. (2000);  34 2205-2230
    CrossrefPubMedGoogle Scholar
  • 25 Guenther A., Karl T., Harley P., Wiedinmyer C., Palmer P. I., Geron C.. Estimates of global terrestrial isoprene emissions using MEGAN (Model of Emissions of Gases and Aerosols from Nature).  Atmospheric Chemistry and Physics. (2006);  6 3181-3210
    PubMedGoogle Scholar
  • 26 Hakola H., Laurila T., Lindfors V., Hellen H., Gaman A., Rinne J.. Variation of the VOC emission rates of birch species during the growing season.  Boreal Environment Research. (2001);  6 237-249
    PubMedGoogle Scholar
  • 27 Hakola H., Rinne J., Laurila T.. The hydrocarbon emission rates of tea-leafed willow (Salix phylicifolia), silver birch (Betula pendula) and European aspen (Populus tremula).  Atmospheric Environment. (1998);  32 1825-1833
    CrossrefPubMedGoogle Scholar
  • 28 He N.-P., Han X.-G., Pan Q.-M.. Variations in the volatile organic compound emission potential of plant functional groups in the temperate grassland vegetation of inner Mongolia, China.  Journal of Integrative Plant Biology. (2005);  47 13-19
    PubMedGoogle Scholar
  • 29 Howard P. H., Meylan W. M.. Handbook of Physical Properties of Organic Chemicals. Boca Raton, New York, London, Tokyo; Lewis Publishers (1997): 1-1585
    Google Scholar
  • 30 Jordan T. E.. Vapor Pressure of Organic Compounds. New York, London; Interscience Publishers (1954)
    Google Scholar
  • 31 Kesselmeier J.. Exchange of short-chain oxygenated volatile organic compounds (VOCs) between plants and the atmosphere: a compilation of field and laboratory studies.  Journal of Atmospheric Chemistry. (2001);  39 219-233
    PubMedGoogle Scholar
  • 32 Kesselmeier J., Staudt M.. Biogenic volatile organic compounds (VOC): an overview on emission, physiology and ecology.  Journal of Atmospheric Chemistry. (1999);  33 23-88
    CrossrefPubMedGoogle Scholar
  • 33 Kulmala M., Suni T., Lehtinen K. E. J., Dal Maso M., Boy M., Reissell A., Rannik Ü., Aaalto P., Keronen P., Hakola H., Bäck J., Hoffmann T., Vesala T., Hari P.. A new feedback mechanism linking forests, aerosols, and climate.  Atmospheric Chemistry and Physics Discussions. (2003);  3 6093-6107
    PubMedGoogle Scholar
  • 34 Lichtenthaler H. K.. The 1-deoxy-D-xylulose-5-phosphate pathway of isoprenoid biosynthesis in plants.  Annual Review of Plant Physiology and Plant Molecular Biology. (1999);  50 47-65
    PubMedGoogle Scholar
  • 35 Lichtenthaler H. K., Schwender J., Disch A., Rohmer M.. Biosynthesis of isoprenoids in higher plant chloroplasts proceeds via a mevalonate-independent pathway.  FEBS Letters. (1997);  400 271-274
    CrossrefPubMedGoogle Scholar
  • 36 Llusià J., Peñuelas J., Asensio D., Munné-Bosch S.. Airborne limonene confers limited thermotolerance to Quercus ilex.  Physiologia Plantarum. (2005);  123 40-48
    CrossrefPubMedGoogle Scholar
  • 37 Loreto F., Ciccioli P., Brancaleoni E., Cecinato A., Frattoni M.. Measurement of isoprenoid content in leaves of Mediterranean Quercus spp. by a novel and sensitive method and estimation of the isoprenoid partition between liquid and gas phase inside the leaves.  Plant Science. (1998 a);  136 25-30
    CrossrefPubMedGoogle Scholar
  • 38 Loreto F., Ciccioli P., Brancaleoni E., Valentini R., De Lillis M., Csiky O., Seufert G.. A hypothesis on the evolution of isoprenoid emission by oaks based on the correlation between emission type and Quercus taxonomy.  Oecologia. (1998 b);  115 302-305
    CrossrefPubMedGoogle Scholar
  • 39 Loreto F., Fischbach R. J., Schnitzler J. P., Ciccioli P., Brancaleoni E., Calfapietra C., Seufert G.. Monoterpene emission and monoterpene synthase activities in the Mediterranean evergreen oak Quercus ilex L. grown at elevated CO2.  Global Change Biology. (2001);  7 709-717
    CrossrefPubMedGoogle Scholar
  • 40 Loreto F., Förster A., Dürr 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 and Environment. (1998 c);  21 101-107
    CrossrefPubMedGoogle Scholar
  • 41 Loreto F., Pinelli P., Manes F., Kollist H.. Impact of ozone on monoterpene emissions and evidence for an isoprene-like antioxidant action of monoterpenes emitted by Quercus ilex leaves.  Tree Physiology. (2004);  24 361-367
    PubMedGoogle Scholar
  • 42 Meylan W. M., Howard P. H.. Estimating octanol-air partition coefficients with octanol-water partition coefficients and Henry's law constants.  Chemosphere. (2005);  61 640-644
    CrossrefPubMedGoogle Scholar
  • 43 Napier J. A., Michaelson L. V., Stobart A. K.. Plant desaturases: harvesting the fat of the land.  Current Opinion in Plant Biology. (1999);  2 123-127
    CrossrefPubMedGoogle Scholar
  • 44 Niinemets Ü.. Costs of production and physiology of emission of volatile leaf isoprenoids. Hemantaranjan, A., ed. Advances in Plant Physiology. Jodhpur; Scientific Publishers (2004): 241-278
    Google Scholar
  • 45 Niinemets Ü., Loreto F., Reichstein M.. Physiological and physico-chemical controls on foliar volatile organic compound emissions.  Trends in Plant Science. (2004);  94 180-186
    PubMedGoogle Scholar
  • 46 Niinemets Ü., Reichstein M.. A model analysis of the effects of nonspecific monoterpenoid storage in leaf tissues on emission kinetics and composition in Mediterranean sclerophyllous Quercus species.  Global Biogeochemical Cycles. (2002);  16 1110 DOI: 10.1029/2002GB001927
    CrossrefPubMedGoogle Scholar
  • 47 Niinemets Ü., Reichstein M., Staudt M., Seufert G., Tenhunen J. D.. Stomatal constraints may affect emission of oxygenated monoterpenoids from the foliage of Pinus pinea.  Plant Physiology. (2002);  130 1371-1385
    CrossrefPubMedGoogle Scholar
  • 48 Noe S. M., Ciccioli P., Brancaleoni E., Loreto F., Niinemets Ü.. Emissions of monoterpenes linalool and ocimene respond differently to environmental changes due to differences in physico-chemical characteristics.  Atmospheric Environment. (2006);  40 4649-4662
    CrossrefPubMedGoogle Scholar
  • 49 Olsson M.. Alterations in lipid composition, lipid peroxidation and anti-oxidative protection during senescence in drought stressed plants and non-drought stressed plants of Pisum sativum.  Plant Physiology and Biochemistry. (1995);  33 547-553
    PubMedGoogle Scholar
  • 50 Owen S., Boissard C., Street R. A., Duckham S. C., Csiky O., Hewitt C. N.. Screening of 18 Mediterranean plant species for volatile organic compound emissions.  Atmospheric Environment. (1997);  31 101-117
    CrossrefPubMedGoogle Scholar
  • 51 Pääkkönen E., Holopainen T., Kärenlampi L.. Ageing-related anatomical and ultrastructural changes in leaves of birch (Betula pendula Roth.) clones as affected by low ozone exposure.  Annals of Botany. (1995);  75 285-294
    CrossrefPubMedGoogle Scholar
  • 52 Peters R. J. B., Duivenbode J. A. D., Duyzer J. H., Verhagen H. L. M.. The determination of terpenes in forest air.  Atmospheric Environment. (1994);  28 2413-2419
    CrossrefPubMedGoogle Scholar
  • 53 Petersson G.. High ambient concentrations of monoterpenes in a Scandinavian pine forest.  Atmospheric Environment. (1988);  22 2617-2619
    PubMedGoogle Scholar
  • 54 Poorter H., Bergkotte M.. Chemical composition of 24 wild species differing in relative growth rate.  Plant, Cell and Environment. (1992);  15 221-229
    PubMedGoogle Scholar
  • 55 Poorter H., De Jong R.. A comparison of specific leaf area, chemical composition and leaf construction costs of field plants from 15 habitats differing in productivity.  The New Phytologist. (1999);  143 163-176
    CrossrefPubMedGoogle Scholar
  • 56 Ricklefs R. E., Matthew K. K.. Chemical characteristics of the foliage of some deciduous trees in southeastern Ontario.  Canadian Journal of Botany. (1982);  60 2037-2045
    PubMedGoogle Scholar
  • 57 Schnitzler J. P., Bauknecht N., Bruggemann N., Einig W., Forkel R., Hampp R., Heiden A. C., Heizmann U., Hoffmann T., Holzke C., Jaeger L., Klauer M., Komenda M., Koppmann R., Kreuzwieser J., Mayer H., Rennenberg H., Smiatek G., Steinbrecher R., Wildt J., Zimmer W.. Emission of biogenic volatile organic compounds: an overview of field, laboratory and modelling studies performed during the “Tropospheric Research Program” (TFS) 1997 – 2000.  Journal of Atmospheric Chemistry. (2002);  42 159-177
    CrossrefPubMedGoogle Scholar
  • 58 Sharkey T. D.. Isoprene synthesis by plants and animals.  Endeavour. (1996);  20 74-78
    CrossrefPubMedGoogle Scholar
  • 59 Sharkey T. D., Chen X. Y., Yeh S.. Isoprene increases thermotolerance of fosmidomycin-fed leaves.  Plant Physiology. (2001);  1254 2001-2006
    PubMedGoogle Scholar
  • 60 Simon V., Riba M. L., Waldhart A., Torres L.. Breakthrough volume of monoterpenes on tenax TA: influence of temperature and concentration for α-pinene.  Journal of Chromatography A. (1995);  704 465-471
    CrossrefPubMedGoogle Scholar
  • 61 Turner G. W., Croteau R.. Organization of monoterpene biosynthesis in Mentha. Immunocytochemical localizations of geranyl diphosphate synthase, limonene-6-hydrolase, isopiperitenol dehydrogenase, and pulegone reductase.  Plant Physiology. (2004);  136 4215-4227
    CrossrefPubMedGoogle Scholar
  • 62 Valentini R., Greco S., Seufert G., Bertin N., Ciccioli P., Cecinato A., Brancaleoni E., Frattoni M.. Fluxes of biogenic VOC from Mediterranean vegetation by trap enrichment relaxed eddy accumulation.  Atmospheric Environment. (1997);  31 229-238
    CrossrefPubMedGoogle Scholar
  • 63 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 and Environment. (2005);  28 318-327
    CrossrefPubMedGoogle Scholar
  • 64 Weidenhamer J. D., Macias F. A., Fischer N. H., Williamson G. B.. Just how insoluble are monoterpenes?.  Journal of Chemical Ecology. (1993);  19 1799-1807
    CrossrefPubMedGoogle Scholar
  • 65 Winer A. M., Karlik J.. Development and validation of databases for modelling biogenic hydrocarbon emissions in California's airsheds. Los Angeles, California; California Air Resources Board – California Environmental Protection Agency (2001)
    Google Scholar
  • 66 Zhang H. Z., Li Y. Q., Xia J. R., Davidovits P., Williams L. R., Jayne J. T., Kolb C. E., Worsnop D. R.. Uptake of gas-phase species by 1-octanol. 1. Uptake of α-pinene, γ-terpinene, p-cymene, and 2-methyl-2-hexanol as afFunction of relative humidity and temperature.  Journal of Physical Chemistry A. (2003);  107 6388-6397
    CrossrefPubMedGoogle Scholar

S. M. Noe

Department of Plant Physiology
University of Tartu

Riia 23

51010 Tartu

Estonia

Email: snoe@ut.ee

Guest Editor: F. Loreto

      >