Register      Login
Functional Plant Biology Functional Plant Biology Society
Plant function and evolutionary biology
RESEARCH ARTICLE

Isoprene prevents the negative consequences of high temperature stress in Platanus orientalis leaves

Violeta Velikova A D , Francesco Loreto B , Tsonko Tsonev A , Federico Brilli B and Aglika Edreva C
+ Author Affiliations
- Author Affiliations

A Institute of Plant Physiology, Bulgarian Academy of Sciences, 1113 Sofia, Bulgaria.

B CNR-Istituto di Biologia Agroambientale e Forestale, Monterotondo Scalo, Rome, Italy.

C Institute of Genetics, Bulgarian Academy of Sciences, 1113 Sofia, Bulgaria.

D Corresponding author. Email: violet@obzor.bio21.bas.bg

Functional Plant Biology 33(10) 931-940 https://doi.org/10.1071/FP06058
Submitted: 24 March 2006  Accepted: 7 June 2006   Published: 2 October 2006

Abstract

The phenomenon of enhanced plant thermotolerance by isoprene was studied in leaves of the same age of 1- or 2-year-old Platanus orientalis plants. Our goals were to determine whether the isoprene emission depends on the age of the plant, and whether different emission rates can influence heat resistance in plants of different age. Two-year-old plants emit greater amounts of isoprene and possess better capacity to cope with heat stress than 1-year-old plants. After a high temperature treatment (38°C for 4 h), photosynthetic activity, hydrogen peroxide content, lipid peroxidation and antiradical activity were preserved in isoprene emitting leaves of 1- and 2-year-old plants. However, heat inhibited photosynthesis and PSII efficiency, caused accumulation of H2O2, and increased all indices of membrane damage and antioxidant capacity in leaves of plants of both ages in which isoprene was inhibited by fosmidomycin. In isoprene-inhibited leaves fumigated with exogenous isoprene during the heat treatment, the negative effects on photosynthetic capacity were reduced. These results further support the notion that isoprene plays an important role in protecting photosynthesis against damage at high temperature. It is suggested that isoprene is an important compound of the non-enzymatic defence of plants against thermal stress, possibly contributing to scavenging of reactive oxygen species (ROS) and membrane stabilising capacity, especially in developed plants.

Keywords: hydrogen peroxide, isoprene, lipid peroxidation, photosynthesis.


Acknowledgments

This study was funded by a NATO Reintegration Grant (No 981279), by the European Science Foundation program VOCBAS, and by a bilateral project within the framework agreement between Italian National Research Council and Bulgarian Academy of Sciences.


References


Able AJ, Sutherland MW, Guest DI (2003) Production of reactive oxygen species during non-specific elicitation, non-host resistance and field resistance expression in cultures of tobacco cells. Functional Plant Biology 30, 91–99.
Crossref | GoogleScholarGoogle Scholar | open url image1

Affek HP, Yakir D (2002) Protection by isoprene against singlet oxygen in leaves. Plant Physiology 129, 269–277.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Alscher RG, Donahue JL, Cramer CL (1997) Reactive oxygen species and antioxidants; relationships in green cells. Physiologia Plantarum 100, 224–233.
Crossref | GoogleScholarGoogle Scholar | open url image1

Benzie IFF, Strain J-J (1999) Ferric reducing antioxidant power assay: direct measure of total antioxidant activity of biological fluids and modified version of simultaneous measurement of total antioxidant power and ascorbic concentration. Methods in Enzymology 299, 15–27.
PubMed |
open url image1

Brand-Williams W, Cuvelier ME, Berset C (1995) Use of a free radical method to evaluate antioxidant activity. Lebensmittel-Wissenschaft und Technologie 28, 25–30. open url image1

Bukhov HG, Wiese C, Neimanis S, Heber U (1999) Heat sensitivity of chloroplasts and leaves: leakage of protons from thylakoids and reversible activation of cyclic electron transport. Photosynthesis Research 59, 81–93.
Crossref | GoogleScholarGoogle Scholar | open url image1

Camejo D, Jiménez A, Alarcón JJ, Torres W, Gómez JM, Sevilla F (2006) Changes in photosynthetic parameters and antioxidant activities following heat-shock treatment in tomato plants. Functional Plant Biology 33, 177–187.
Crossref | GoogleScholarGoogle Scholar | open url image1

Edreva A (2005) Generation and scavenging of reactive oxygen species in chloroplasts: a submolecular approach. Agriculture Ecosystems & Environment 106, 119–133.
Crossref | GoogleScholarGoogle Scholar | open url image1

Elstner EF (1991) Mechanisms of oxygen activation in different compartments of plant cells. In ‘Active oxygen / oxidative stress and plant metabolism’. (Eds EJ Pell, KL Steffen) pp. 13–25. (American Society of Plant Physiology: Rockville)

Fischbach RJ, Staudt M, Zimmer I, Rambal S, Schnitzler JP (2002) Seasonal pattern of monoterpene synthase activities in leaves of the evergreen tree Quercus ilex. Physiologia Plantarum 114, 354–360.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Foyer DH, Lelandais M, Kunert KJ (1994) Photooxidative stress in plants. Plant Physiology 92, 696–717.
Crossref | GoogleScholarGoogle Scholar | open url image1

Genty B, Briantais J-M, Baker NR (1989) The relationship between the quantum yield of photosynthetic electron transport and quenching of chlorophyll fluorescence. Biochimica et Biophysica Acta 990, 87–92. open url image1

Guenther A, Hewitt CN, Erickson D, Fall R, Geron C, Graedel T, Harley P, Klinger L, Lerdau M, Mckay WA, Pierce T, Scholes B, Steinbrecher R, Tallamraju R, Taylor J, Zimmerman P (1995) A global model of natural volatile organic compound emissions. Journal of Geophysical Research — Atmospheres 100, 8873–8892.
Crossref | GoogleScholarGoogle Scholar | open url image1

Heath RL, Packer L (1968) Photoperoxidation in isolated chloroplasts. I. Kinetics and stoichiometry of fatty acid peroxidation. Archives of Biochememistry and Biophysics 125, 189–198.
Crossref | GoogleScholarGoogle Scholar | open url image1

Kesselmeier J, Staudt M (1999) Biogenic volatile organic compounds (VOC): an overview on emission, physiology and ecology. Journal of Atmospheric Chemistry 33, 23–88.
Crossref | GoogleScholarGoogle Scholar | open url image1

Kuhn U, Rottenberger S, Biesenthal T, Wolf A, Schebeske G, Ciccioli P, Kesselmeier J (2004) Strong correlation between isoprene emission and gross photosynthetic capacity during leaf phenology of the tropical tree species Hymenaea courbaril with fundamental changes in volatile organic compounds emission composition during early leaf development. Plant, Cell & Environment 27, 1469–1485.
Crossref | GoogleScholarGoogle Scholar | open url image1

Kuzma J, Fall R (1993) Leaf isoprene emission rate is dependent on leaf development and the level of isoprene synthase. Plant Physiology 101, 435–440.
PubMed |
open url image1

Lehning A, Zimmer I, Steinbrecher R, Brüggemann N, Schnitzler JP (1999) Isoprene synthase activity and its relation to isoprene emission in Quercus robur leaves. Plant, Cell & Environment 22, 495–504.
Crossref | GoogleScholarGoogle Scholar | open url image1

Lehning A, Zimmer W, Zimmer I, Schnitzler JP (2001) Modeling of annual variations of oak (Quercus robur L.) isoprene synthase activity to predict isoprene emission rates. Journal of Geophysical Research — Atmospheres 106, 3157–3166.
Crossref | GoogleScholarGoogle Scholar | open url image1

Loreto F (2002) 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. Perspectives in Plant Ecology, Evolution and Systematics 5, 185–192.
Crossref | GoogleScholarGoogle Scholar | open url image1

Loreto F, Sharkey TD (1990) A gas-exchange study of photosynthesis and isoprene emission in Quercus rubra. Planta 182, 523–531.
Crossref | GoogleScholarGoogle Scholar | open url image1

Loreto F, Velikova V (2001) Isoprene produced by leaves protects the photosynthetic apparatus against ozone damage, quenches ozone products, and reduces lipid peroxidation of cellular membranes. Plant Physiology 127, 1781–1787.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Loreto F, Di Marco G, Tricoli D, Sharkey TD (1994) Measurements of mesophyll conductance, photosynthetic electron transport and alternative sinks of field grown wheat leaves. Photosynthesis Research 41, 397–403.
Crossref | GoogleScholarGoogle Scholar | open url image1

Loreto F, Mannozzi M, Maris C, Nascetti P, Ferranti F, Pasqualini S (2001) Ozone quenching properties of isoprene and its antioxidant role in plants. Plant Physiology 126, 993–1000.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Mohammed GH, Binder WD, Gillies SL (1995) Chlorophyll fluorescence: a review of its practical forestry applications and instrumentation. Scandinavian Journal of Forest Research 10, 383–410. open url image1

Monson RK, Jaeger CH, Adams WW, Driggers EM, Silver GM, Fall R (1992) Relationships among isoprene emission rate, photosynthesis, and isoprene synthase activity as influenced by temperature. Plant Physiology 98, 1175–1180.
PubMed |
open url image1

Niinemets U, Seufert G, Steinbrecher R, Tenhunen JD (2002) A model coupling foliar monoterpene emissions to leaf photosynthetic characteristics in Mediterranean evergreen Quercus species. New Phytologist 153, 257–275.
Crossref | GoogleScholarGoogle Scholar | open url image1

Pastenes C, Horton P (1996) Effect of high temperature on photosynthesis in beans. 1. Oxygen evolution and chlorophyll fluorescence. Plant Physiology 112, 1245–1251.
PubMed |
open url image1

Peñuelas J, Llusià J, Asensio D, Munné-Bosch S (2005) Linking isoprene with plant thermotolerance, antioxidants and monoterpene emissions. Plant, Cell & Environment 28, 278–286.
Crossref | GoogleScholarGoogle Scholar | open url image1

Polle A , Rennenberg H (1994) Photooxidative stress in trees. In ‘Photoxidative stresses in plants: causes and amelioration’. (Eds C Foyer, P Mullineaux) pp. 199–218. (CRC Press, Inc.: Boca Raton)

Scandalios JG (1997) ‘Oxidative stress and the molecular biology of antioxidant defenses.’ (Cold Spring Harbor Laboratory Press: Plainview)

Sharkey TD, Loreto F (1993) Water stress, temperature, and light effects on the capacity for isoprene emission and photosynthesis of kudzu leaves. Oecologia 95, 328–333.
Crossref | GoogleScholarGoogle Scholar | open url image1

Sharkey TD, Singsaas EL (1995) Why plants emit isoprene. Nature 374, 769.
Crossref | GoogleScholarGoogle Scholar | open url image1

Sharkey TD, Yeh S (2001) Isoprene emission from plants. Annual Review of Plant Physiology and Plant Molecular Biology 52, 407–436.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Sharkey TD, Singsaas EL, Vanderveer PJ, Geron CD (1996) Field measurements of isoprene emission from trees in response to temperature and light. Tree Physiology 16, 649–654.
PubMed |
open url image1

Sharkey TD, Chen X, Yeh S (2001) Isoprene increases thermotolerance of fosmidomycin-fed leaves. Plant Physiology 125, 2001–2006.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Shigeoka S, Ishikawa T, Tamoi M, Miyagawa Y, Takeda T, Yabuta Y, Yoshimura K (2002) Regulation and function of ascorbate peroxidase isoenzymes. Journal of Experimental Botany 53, 1305–1319.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Singsaas EL, Sharkey TD (1998) The regulation of isoprene emission responses to rapid leaf temperature fluctuations. Plant, Cell & Environment 21, 1181–1188.
Crossref | GoogleScholarGoogle Scholar | open url image1

Singsaas EL, Sharkey TD (2000) The effects of high temperature on isoprene synthesis in oak leaves. Plant, Cell & Environment 23, 751–757.
Crossref | GoogleScholarGoogle Scholar | open url image1

Singsaas EL, Lerdau M, Winter K, Sharkey TD (1997) Isoprene increases thermotolerance of isoprene-emitting species. Plant Physiology 115, 1413–1420.
PubMed |
open url image1

Takeda T, Yokota A, Shigeoka S (1995) Resistance of photosynthesis to hydrogen peroxide in algae. Plant & Cell Physiology 36, 1089–1095. open url image1

Velikova V, Loreto F (2005) 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 & Environment 28, 318–327.
Crossref | GoogleScholarGoogle Scholar | open url image1

Velikova V, Yordanov I, Edreva A (2000) Oxidative stress and some antioxidant systems in acid rain-treated bean plants. Protective role of exogenous polyamines. Plant Science 151, 59–66.
Crossref | GoogleScholarGoogle Scholar | open url image1

Velikova V, Edreva A, Loreto F (2004) Endogenous isoprene protects Phragmites australis leaves against singlet oxygen. Physiologia Plantarum 122, 219–225.
Crossref | GoogleScholarGoogle Scholar | open url image1

Velikova V, Pinelli P, Loreto F (2005) Consequences of inhibition of isoprene synthesis in Phragmites australis leaves exposed to elevated temperatures. Agriculture Ecosystems & Environment 106, 209–217.
Crossref | GoogleScholarGoogle Scholar | open url image1

Zeidler J, Schwender J, Müller C, Wiesner J, Weidemeyer C, Back E, Jomaa H, Lichtenthaler HK (1998) Inhibition of the non-mevalonate 1-deoxy-d-xylulose-5-phosphate pathway of plant isoprenoid biosynthesis by fosmidomycin. Zeitschrift für Naturforschung 53c, 980–986. open url image1

Zhang X, Mu Y, Song W, Zhuang Y (2000) Seasonal variations of isoprene emissions from deciduous trees. Atmospheric Environment 34, 3027–3032.
Crossref | GoogleScholarGoogle Scholar | open url image1