Russian Journal of Plant Physiology

, Volume 66, Issue 3, pp 403–413 | Cite as

Respiration and Involvement of an Alternative Pathway as Related to Age and Phenological Strategy of the Leaf

  • E. V. GarmashEmail author


Plants of spring wheat (Triticum aestivum L.) and winter rye (Secale cereale L.) pursuing different phenological strategies were studied. Respiratory activity, ratio of respiratory pathways, and effect of the alterative pathway (AP) on the YATP/glucose coefficient, which expresses the energy efficiency of respiration (EER), were studied over the leaf ontogeny. At 20°C, the respiratory capacity of the wheat leaf was higher than that of rye due to the decrease in rye metabolism in an autumn period of vegetation. Respiration decreased with age and relative growth rate (RGR) of the leaf. In the young leaf whose area was 20–30% of the final value, respiration mainly proceeded by the cytochrome pathway because of energy expenses for de novo synthesis. In the spring wheat leaf, the AP fraction of its respiration increased from 25 to 40% with age; this indicates the AP belonging to maintenance respiration component. In the mature rye leaf, the AP contribution decreased from 35 to 15% of a total respiration that maintained EER during plant adaptation to low temperatures. A change in the direction of respiratory gradient along the leaf was also found. In leaves of different age, the meristematically active zone manifested the greatest values of such indices as rate of respiration, fraction of AP (up to 45% of a total respiration), and rate of thermogenesis; this shows participation of alternative respiration in energy dissipation and energy balance control. Altogether, the value YATP/glucose did not change at the level of wheat and rye leaf of different ages. On average, it was 20 mole ATP/mole glucose, which is one third lower than the theoretically assumed value. This may be interpreted so that the metabolic level corresponds to environmental conditions and is adapted to them.


Triticum aestivum Secale cereale leaf age phonological strategy respiration alterative pathway energy efficiency of respiration 



The work was carried out in terms of the budget theme “Physiology and Stress-Resistance of Plant Photosynthesis and that of Poikilohydric Photoautotrophs under Conditions of the North,” project no. GR AAAA-A17-117033010038-7.


The authors declare that they have no conflict of interest. This article does not contain any studies involving animals or human participants performed by any of the authors.


  1. 1.
    Mokronosov, A.T., Mesostructure and functional activity of the photosynthetic apparatus, in Mezostruktura i funktsional’naya aktivnost' fotosinteticheskogo apparata (Mesostructure and Functional Activity of the Photosynthetic Apparatus), Mokronosov, A.T., Borzenkova, R.A., Tsel’niker, Yu.L., and Nekrasova, G.F., Eds., Sverdlovsk, 1978, pp. 5–31.Google Scholar
  2. 2.
    Mokoronosov, A.T., Ontogeneticheskii aspekt fotosinteza (Ontogenetic Aspect of Photosynthesis), Moscow: Nauka, 1981.Google Scholar
  3. 3.
    Mokronosov, A.T., Fotosinteticheskaya funktsiya i tselostnost' rastitel’nogo organizma, 42-e Timiryazevskoe chteniye (Photosynthetic Function and Integrity of the Plant Organism, the 42nd Timiryazev Lecture), Moscow: Nauka, 1983.Google Scholar
  4. 4.
    Semikhatova, O.A., Energy aspects of the integration of physiological processes in plants, Sov. Plant Physiol., 1980, vol. 27, pp. 1005–1017.Google Scholar
  5. 5.
    Garmash, E.V., Mitochondrial respiration of the photosynthesizing cell, Russ. J. Plant Physiol., 2016, vol. 63, pp. 13–25.CrossRefGoogle Scholar
  6. 6.
    Golovko, T.K., Dykhanie rastenii (fiziologicheskie aspekty) (Plant Respiration (Physiological Aspects)), St. Petersburg: Nauka, 1999.Google Scholar
  7. 7.
    Li, L., Nelson, C.J., Trösch, J., Castleden, I., Huang, S., and Millar, A.H., Protein degradation rate in Arabidopsis thaliana leaf growth and development, Plant Cell, 2017, vol. 29, pp. 207–228.CrossRefGoogle Scholar
  8. 8.
    Millenaar, F.F. and Lambers, H., The alternative oxidase: in vivo regulation and function, Plant Biol., 2003, vol. 2, pp. 2–15.CrossRefGoogle Scholar
  9. 9.
    Semikhatova, O.A., Energetika dykhaniya v norme i pri ekologicheskom stresse, 48-e Timiryazevskoe chteniye (Respiratory Energy in Normal and under Environmental Stress, the 48th Timiryazev Lecture), Moscow: Nauka, 1990.Google Scholar
  10. 10.
    Rakhmankulova, Z.F., Levels of energy metabolism control in plants, Vestn. Bashkir. Gos. Univ., 2009, vol. 14, no. 3 (I), pp. 1141–1154.Google Scholar
  11. 11.
    Noguchi, K., Effects of light intensity and carbohydrate status on leaf and root respiration, in Plant Respiration: From Cell to Ecosystem, Ch. 5, Lambers, H. and Ribas-Carbo, M., Eds., Dordrecht: Springer, 2005, pp. 63–83.Google Scholar
  12. 12.
    Florez-Sarasa, I.D., Bouma, T.J., Medrano, H., Azcon-Bieto, J., and Ribas-Carbo, M., Contribution of the cytochrome and alternative pathways to growth respiration and maintenance respiration in Arabidopsis thaliana, Physiol. Plant., 2007, vol. 129, pp. 143–151.CrossRefGoogle Scholar
  13. 13.
    Priault, P., Vidal, G., de Paepe, R., and Ribas-Carbo, M., Leaf age-related changes in respiratory pathways are dependent on complex I activity in Nicotiana sylvestris, Physiol. Plant., 2007, vol. 129, pp. 152–162.CrossRefGoogle Scholar
  14. 14.
    Ivanova, T.I., Kirpichnikova, O.V., Sherstneva, O.A., and Yudina, O.S., Annual cycle of respiration in the leaves of evergreen plants, Russ. J. Plant Physiol., 1998, vol. 45, pp. 786–793.Google Scholar
  15. 15.
    Golovko, T.K. and Pystina, N.V., The alternative respiration pathway in leaves of Rhodiola rosea and Ajuga reptans: presumable physiological role, Russ. J. Plant Physiol., 2001, vol. 48, pp. 733–740.CrossRefGoogle Scholar
  16. 16.
    Shugaev, A.G., Vyskrebentseva, A.I., and Shugaeva, N.A., Seasonal changes in the activity of mitochondrial oxidases detected by the traditional inhibitor analysis in disks cut from mature sugar beet leaves, Russ. J. Plant Physiol., 1998, vol. 45, pp. 574–581.Google Scholar
  17. 17.
    Tarchevskii, I.A., Metabolizm rastenii pri stresse (izbrannye trudy) (Plant Metabolism under Stress (Selected Works)), Kazan: Fen, 2001.Google Scholar
  18. 18.
    Kikuzawa, K., Leaf phenology as an optimal strategy for carbon gain in plants, Can. J. Bot., 1995, vol. 73, pp. 158–163.CrossRefGoogle Scholar
  19. 19.
    Radford, P.J., Growth analysis formulae—their use and abuse, Crop Sci., 1967, vol. 7, pp. 171–175.CrossRefGoogle Scholar
  20. 20.
    Møller, I.M., Berczi, A., Plas van der L.H.W., and Lambers, H., Measurement of the activity and capacity of the alternative pathway in intact plant tissue: identification of problems and possible solution, Physiol. Plant., 1988, vol. 72, pp. 642–649.Google Scholar
  21. 21.
    Amthor, J.S., The McCree-de Wit-Penning de Vries-Thornley respiration paradigms: 30 years later, Ann. Bot., 2000, vol. 86, pp. 1–20.CrossRefGoogle Scholar
  22. 22.
    Bradford, M.M., A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein–dye binding, Anal. Biochem., 1976, vol. 72, pp. 248–254.CrossRefGoogle Scholar
  23. 23.
    Moskalev, A.A. and Novakovskii, A.B., Statisticheskie metody v ekologii s ispol’zovaniem R, Statistica, Excel i SPSS (Statistical Methods in Ecology Using R, Statistica, Excel, and SPSS), Syktyvkar: Syktyvkar Gos. Univ., 2014.Google Scholar
  24. 24.
    Edwards, J.M., Roberts, T.H., and Atwell, B.J., Quantifying ATP turnover in anoxic coleoptiles of rice (Oryza sativa) demonstrates preferential allocation of energy to protein synthesis, J. Exp. Bot., 2012, vol. 63, pp. 4389–4402.CrossRefGoogle Scholar
  25. 25.
    Grabel'nykh, O.I., Mitochondrial energy dispersive systems of plants under the action of low temperatures, Extended Abstract of Doctoral (Biol.) Dissertation, Irkutsk: Sib. Inst. Plant Physiol. Biochem., Sib. Branch, Russ. Acad. Sci., 2014.Google Scholar
  26. 26.
    Garmash, E.V., Malyshev, R.V., Shelyakin, M.A., and Golovko, T.K., Activities of respiratory pathways and the pool of nonstructural carbohydrates in greening leaves of spring wheat seedlings, Russ. J. Plant Physiol., 2014, vol. 56, pp. 160–168.CrossRefGoogle Scholar
  27. 27.
    Garmash, E.V. and Golovko, T.K., Effect of growth rate of barley plants grown at different temperatures and mineral nutrition levels on alternative respiratory pathway activity, Fiziol. Biokhim. Kult. Rast., 2011, vol. 43, pp. 113–121.Google Scholar
  28. 28.
    Shugaeva, N.A., Vyskrebentseva, E.I., Orekhova, S.O., and Shugaev, A.G., Effect of water deficit on respiration of conducting bundles in leaf petioles of sugar beet, Russ. J. Plant Physiol., 2007, vol. 54, pp. 329–335.CrossRefGoogle Scholar
  29. 29.
    Sayed, M.A., Umekawa, Y., and Kikukatsu, I., Metabolic interplay between cytosolic phosphoenolpyruvate carboxylase and mitochondrial alternative oxidase in thermogenic skunk cabbage, Symplocarpus renifolius, Plant Signal. Behav., 2016, vol. 11, no. 11: e1247138. CrossRefGoogle Scholar
  30. 30.
    Shane, M.W., Cramer, M.D., Funayama-Noguchi, S., Cawthray, G.R., Millar, A.H., Day, D.A., and Lambers, H., Developmental physiology of cluster-root carboxylate synthesis and exudation in Harsh Hakea. Expression of phosphoenolpyruvate carboxylase and the alternative oxidase, Plant Physiol., 2004, vol. 135, pp. 549–560.CrossRefGoogle Scholar

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© Pleiades Publishing, Ltd. 2019

Authors and Affiliations

  1. 1.Institute of Biology, Komi Scientific Center, Ural Branch, Russian Academy of SciencesSyktyvkarRussia

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