Skip to main content
Log in

Salicylic acid enhances the activity of the alternative pathway of respiration in tobacco leaves and induces thermogenicity

  • Published:
Planta Aims and scope Submit manuscript

Abstract

A rise in the level of endogenous salicylic acid (SA) during flowering of the thermogenic voodoo lily, Sauromatum guttatum, leads to a pronounced temperature elevation by stimulation of the alternative respiratory pathway. We have studied the thermal response of tobacco (Nicotiana tabacum L.) leaves, a non-thermogenic tissue, to exogenous SA, and its relation to alternative respiration. A reproducible increase in surface temperature of 0.5–1.0°C was registered with high-resolution infrared cameras. The same phenomenon was observed when 2,6-dihydroxybenzoic acid, an active analogue of SA, was used. Non-active SA analogues, such as 3- and 4-hydroxybenzoic acid, did not induce thermogenicity. The thermal effect of SA was abolished with inhibitors of the alternative pathway, such as salicylhydroxamic acid and propyl gallate. Polarographic measurement of the respiratory activity, including that of the alternative pathway in SA-treated plants, showed a significant increase of both total respiration and the alternative pathway compared with non-treated controls. Therefore, we postulate that, as in thermogenic species, SA enhances the activity of total respiration and of the cyanide-resistant pathway in tobacco leaves, subsequently leading to an elevation in surface temperature.

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.

Similar content being viewed by others

Abbreviations

AP:

alternative pathway

2,6-DHBA:

2,6-dihydroxybenzoic acid

3-HBA:

3-hydroxybenzoic acid

4-HBA:

4-hydroxybenzoic acid

IR:

infrared

PG:

propyl gallate

SA:

salicylic acid

SHAM:

salicylhydroxamic acid

References

  • Chen, Z., Silva, H., Klessig, D.F. (1993) Active oxygen species in the induction of plant systemic acquired resistance by salicylic acid. Science 262, 1883–1886

    CAS  PubMed  Google Scholar 

  • Dry, I.B., Moore, A.L., Day, D.A., Wiskich, J.T. (1989) Regulation of alternative pathway activity in plant mitochondria: nonlinear relationship between electron flux and the redox poise of the quinone pool. Arch. Biochem. Biophys. 273, 148–157

    Google Scholar 

  • Elthon, T.E., Nickels, R.L., McIntosh, L. (1989) Mitochondrial events during the development of thermogenesis in Sauromatum guttatum (Schott). Planta 180, 82–89

    Google Scholar 

  • Inoue, Y. (1990) Remote detection of physiological depression in crop plants with infrared thermal imagery. Jpn. J. Crop Sci. 59, 762–768

    Google Scholar 

  • Kapulnik, Y., Yalpani, N., Raskin, I. (1992) Salicylic acid induces cyanide-resistant respiration in tobacco cell-suspension cultures. Plant Physiol. 100, 1921–1926

    Google Scholar 

  • Klir, J.J., Heath, J. (1992) An infrared thermographic study of surface temperature in relation to external thermal stress in three species of foxes: the red fox (Vulpes vulpes), Arctic fox (Alopex lagopus), and kit fox (Vulpes macrotis). Physiol. Zool. 65, 1011–1021

    Google Scholar 

  • Kumar, A.M., Söll, D. (1992) Arabidopsis alternative oxidase sustains Escherichia coli respiration. Proc. Natl. Acad. Sci. USA 89, 10842–10846

    Google Scholar 

  • Lambers, H. (1982) Cyanide-resistant respiration: a non-phosphorylating electron transport pathway acting as an energy overflow. Physiol. Plant. 55, 478–485

    Google Scholar 

  • Lambers, H., van der Werf, A., Bergkette, M. (1993) Respiration: the alternative pathway. In: Methods in comparative plant ecology: A laboratory manual, pp. 140–144, Hendry, G.A.F., Grime, J.P., eds. Chapman & Hall, London

    Google Scholar 

  • Lance, C., Chauveau, M., Dizengremel, P. (1985) The cyanideresistant pathway of plant mitochondria. In: Encyclopedia of plant physiology, n.s., vol. 18: Higher plant cell respiration, pp. 202–247, Douce, R., Day, D.A., eds. Springer, Berlin

    Google Scholar 

  • Larqué-Saavedra, A. (1978) The antitranspirant effect of acetylsalicylic acid on Phaseolus vulgaris. Physiol. Plant. 43, 126–128

    Google Scholar 

  • Larqué-Saavedra, A. (1979) Stomatal closure in response to acetylsalicylic acid treatment. Z. Pflanzenphysiol. 93, 371–375

    Google Scholar 

  • Laties, G.G. (1982) The cyanide-resistant, alternative path in higher plant respiration. Annu. Rev. Plant Physiol. 33, 519–555

    Google Scholar 

  • León, J., Yalpani, N., Raskin, I., Lawton, M.A. (1993) Induction of benzoic acid 2-hydroxylase in virus-inoculated tobacco. Plant Physiol. 103, 323–328

    Google Scholar 

  • Malamy, J., Carr, J.P., Klessig, D.F., Raskin, I. (1990) Salicylic acid: a likely endogenous signal in the resistance response in tobacco to viral infection. Science 250, 1002–1004

    Google Scholar 

  • Maliga, P., Sz.-Breznovits, A., Márton, L. (1973) Streptomycinresistant plants from callus culture of haploid tobacco. Nature New Biol. 244, 29–30

    Google Scholar 

  • McIntosh, L. (1994) Molecular biology of the alternative oxidase. Plant Physiol., 105, 781–786

    Google Scholar 

  • Meeuse, B.J.D. (1975) Thermogenic respiration in aroids. Annu. Rev. Plant Physiol. 26, 117–126

    Google Scholar 

  • Métraux, J.P., Signer, H., Ryals, J., Ward, E., Wyss-Benz, M., Gaudin, J., Raschdorf, K., Schmid, E., Blum, W., Inverardi, B. (1990) Increase in salicyclic acid at the onset of systemic acquired resistance in cucumber. Science 250, 1004–1006

    Google Scholar 

  • Nobel, P.S., ed. (1991) Physicochemical and environmental plant physiology. Academic Press, San Diego

    Google Scholar 

  • Omasa, K., Tajima, A., Miyasaka, K. (1990) Diagnosis of street trees by thermography: Zelkova trees in Sendai city. J. Agric. Meteorol. 45, 271–275

    Google Scholar 

  • Palmer, J.M. (1976) The organization and regulation of electron transport in plant mitochondria. Annu. Rev. Plant Physiol. 27, 133–157

    Google Scholar 

  • Pinter, P.J., Stanghellini, M.E., Reginato, R.J., Idso, S.B., Jenkins, A.D., Jackson, R.D. (1979) Remote detection of biological stresses in plants with infrared thermometry. Science 205, 585–587

    Google Scholar 

  • Raskin, I., Ehmann, A., Melander, W.R., Meeuse, B.J.D. (1987) Salicylic acid: a natural inducer of heat production in Arum lilies. Science 237, 1601–1602

    Google Scholar 

  • Raskin, I., Turner, I.M., Melander, W.R. (1989) Regulation of heat production in the inflorescences of an Arum lily by endogenous salicylic acid. Proc. Natl. Acad. Sci. USA 86, 2214–2218

    Google Scholar 

  • Rasmussen, J.B., Hammerschmidt, R., Zook, M.N. (1991) Systemic induction of salicylic acid accumulation in cucumber after inoculation with Pseudomonas syringae pv syringae. Plant Physiol. 97, 1342–1347

    Google Scholar 

  • Rhoads, D.M., McIntosh, L. (1991) Isolation and characterization of a cDNA clone encoding an alternative oxidase protein of Sauromatum guttatum (Schott). Proc. Natl. Acad. Sci. USA 88, 2122–2126

    Google Scholar 

  • Rhoads, D.M., McIntosh, L. (1992) Salicylic acid regulation of respiration in higher plants: alternative oxidase expression. Plant Cell 4, 1131–1139

    Article  CAS  PubMed  Google Scholar 

  • Vanlerberghe, G.C., McIntosh, L. (1992) Lower growth temperature increases alternative pathway capacity and alternative oxidase protein in tobacco. Plant Physiol. 100, 115–119

    Google Scholar 

  • Vanlerberghe, G.C., McIntosh, L. (1994) Mitochondrial electron transport regulation of nuclear gene expression. Studies with the alternative oxidase gene of tobacco. Plant Physiol. 105, 867–874

    Google Scholar 

  • Whelan, J., McIntosh, L., Day, D.A. (1993) Sequencing of a soybean alternative oxidase cDNA clone. Plant Physiol. 103, 1481

    Google Scholar 

  • Yalpani, N., Silverman, P., Wilson, T.M.A., Kleier, D.A., Raskin, I. (1991) Salicylic acid is a systemic signal and an inducer of pathogenesis-related proteins in virus-infected tobacco. Plant Cell 3, 809–818

    Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Additional information

D.V.D.S. and G.S. thank Rob Welschen (Department of Plant Ecology and Evolutionary Biology, Universiteit Utrecht, The Netherlands) for teaching them the procedure for measurement of alternative respiration. Eric Messens (Laboratorium voor Genetica, Universiteit Gent, Belgium) is acknowledged for the SA determinations, and Ludwig De Temmerman (Instituut voor Scheikundig Onderzoek, Tervuren, Belgium) for lending us the porometer and leaf area meter. We are also grateful to Karel Spruyt for the photographs, and to Martine De Cock for lay-out of the manuscript. This work was supported by grants from the National Fund for Scientific Research. G.S. is indebted to the European Union for a short-term fellowship and to the Bulgarian National Fund for Scientific Research for a research grant. D.V.D.S. and L.C. are Senior Research Associate and a Research Assistant of the National Fund for Scientific Research (Belgium).

Rights and permissions

Reprints and permissions

About this article

Cite this article

Van Der Straeten, D., Chaerle, L., Sharkov, G. et al. Salicylic acid enhances the activity of the alternative pathway of respiration in tobacco leaves and induces thermogenicity. Planta 196, 412–419 (1995). https://doi.org/10.1007/BF00203637

Download citation

  • Received:

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF00203637

Key words

Navigation