Advertisement

Russian Journal of Plant Physiology

, Volume 66, Issue 3, pp 365–374 | Cite as

Physiological Aspects of Photosynthesis–Respiration Interrelations

  • Z. F. RakhmankulovaEmail author
REVIEWS
  • 3 Downloads

Abstract

The review discusses up-to-date concepts of interrelations between photosynthesis and respiration. It considers the quantitative ratio of the processes in the leaf and that in the whole plant reported by Russian and other researches. Special attention is paid to performance of dark respiration in the light and to the methods of its exploration, which employ classical gas exchange, chlorophyll fluorescence, and carbon isotopes. Possible causes of conservatism and variability in the total respiration to gross photosynthesis ratio under stationary and stress conditions are also discussed along with prospects in further investigations.

Keywords:

higher plants carbon balance gross photosynthesis dark respiration mitochondrial respiration under light steady state stress 

Notes

FUNDING

This work was partially supported by the Russian Foundation for Basic Research, project no. 17-04-00853a.

COMPLIANCE WITH ETHICAL STANDARDS

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.

REFERENCES

  1. 1.
    Smith, N. and Dukes, J., Plant respiration and photosynthesis in global-scale models: incorporating acclimation to temperature and CO2, Global Change Biol., 2013, vol. 19, pp. 45–63.CrossRefGoogle Scholar
  2. 2.
    Van Oijen, M., Schapendonk, A., and Höglind, M., On the relative magnitudes of photosynthesis, respiration, growth and carbon storage in vegetation, Ann. Bot., 2010, vol. 105, pp. 793–797.CrossRefGoogle Scholar
  3. 3.
    Von Gaemmerer, S., Steady-state models of photosynthesis, Plant Cell Environ., 2013, vol. 36, pp. 1617–1630.CrossRefGoogle Scholar
  4. 4.
    Penning de Vries, F.W.T., The cost of maintenance processes in plant cells, Ann. Bot., 1975, vol. 39, pp. 77–92.CrossRefGoogle Scholar
  5. 5.
    Tcherkez, G., Gauthier, P., Buckley, T.N., Busch, F.A., Barbour, M.M., Bruhn, D., Heskel, M.A., Gong, X.Y., Crous, K., Griffin, K.L., Way, D., Turnbull, M., Adams, M.A., Atkin, O.K., Farquhar, G.D., et al., Leaf day respiration: low CO2 flux but high significance for metabolism and carbon balance, New Phytol., 2017, vol. 216, pp. 986–1001.  https://doi.org/10.1111/nph.14816 CrossRefGoogle Scholar
  6. 6.
    Atkin, O.K., Bloomfield, K.J., Reich, P.B., Tjoelker, M.G., Asner, G.P., Bonal, D., Bönisch, G., Bradford, M.G., Cernusak, L.A., Cosio, E.G., Creek, D., Crous, K.Y., Domingues, T.F., Dukes, J.S., Egerton, J.J., et al., Global variability in leaf respiration in relation to climate, plant functional types and leaf traits, New Phytol., 2015, vol. 206, pp. 614–636.  https://doi.org/10.1111/nph.13253 CrossRefGoogle Scholar
  7. 7.
    Atkin, O.K., Scheurwater, I., and Pons, T.L., Respiration as a percentage of daily photosynthesis in whole plants is homeostatic at moderate, but not high, growth temperatures, New Phytol., 2007, vol. 174, pp. 367–380.CrossRefGoogle Scholar
  8. 8.
    Campbell, C., Atkinson, L., Zaragoza-Castells, J., Lundmark, M., Atkin, O., and Hurry, V., Acclimation of photosynthesis and respiration is asynchronous in response to changes in temperature regardless of plant functional group, New Phytol., 2007, vol. 176, pp. 375–389.  https://doi.org/10.1111/j.1469-8137.2007.02183.x CrossRefGoogle Scholar
  9. 9.
    Huntingford, C., Atkin, O.K., Martinez-de la Torre, A., Mercado, L.M., Heskel, M.A., Harper, A.B., Bloomfield, K.J., O’Sullivan, O.S., Reich, P.B., Wythers, K.R., Butler, E.E., Chen, M., Griffin, K.L., Meir, P., Tjoelker, M.G., et al., Implications of improved representations of plant respiration in a changing climate, Nat. Commun., 2017, vol. 8, pp. 1–11.  https://doi.org/10.1038/s41467-017-01774-z CrossRefGoogle Scholar
  10. 10.
    Wullschleger, S.D., Warren, J.M., and Thornton, P.E., Leaf respiration (GlobResp)—global trait database supports Earth System Models, New Phytol., 2015, vol. 206, pp. 483–485.CrossRefGoogle Scholar
  11. 11.
    Araújo, W.L., Nunes-Nesi, A., and Fernie, A.R., On the role of plant mitochondrial metabolism and its impact on photosynthesis in both optimal and sub-optimal growth conditions, Photosynth. Res., 2014, vol. 119, pp. 141–156.  https://doi.org/10.1007/s11120-013-9807-4
  12. 12.
    Raghavendra, A.S. and Padmasree, K., Beneficial interactions of mitochondrial metabolism with photosynthetic carbon assimilation, Trends Plant Sci., 2003, vol. 8, pp. 546–553.  https://doi.org/10.1016/j.tplants.2003.09.015 CrossRefGoogle Scholar
  13. 13.
    Carrari, F., Nunes-Nesi, A., Gibon, Y., Lytovchenko, A., Loureiro, M.E., and Fernie, A.R., Reduced expression of aconitase results in an enhanced rate of photosynthesis and marked shifts in carbon partitioning in illuminated leaves of wild species tomato, Plant Physiol., 2003, vol. 133, pp. 1322–1335.  https://doi.org/10.1104/pp.103.026716 CrossRefGoogle Scholar
  14. 14.
    Hurry, V., Keerberg, O., Parnik, T., Oquist, G., and Gardestrom, P., Effect of cold hardening on the components of respiratory decarboxylation in the light and in the dark in leaves of winter rye, Plant Physiol., 1996, vol. 111, pp. 713–719.CrossRefGoogle Scholar
  15. 15.
    Gifford, R.M., Plant respiration in productivity models: conceptualization, representation and issues for global terrestrial carbon-cycle research, Funct. Plant Biol., 2003, vol. 30, pp. 171–186.CrossRefGoogle Scholar
  16. 16.
    Cannell, M.G.R. and Thornley, J.H.M., Modelling the components of plant respiration: some guiding principles, Ann. Bot., 2000, vol. 85, pp. 45–54.CrossRefGoogle Scholar
  17. 17.
    Thornley, J.H.M. and Cannell, M.G.R., Modelling the components of plant respiration: representation and realism, Ann. Bot., 2000, vol. 85, pp. 55–67.CrossRefGoogle Scholar
  18. 18.
    McCree, K.J., An equation for the rate of respiration of white clover plants grown under controlled conditions, in Prediction and Measurement of Photosynthetic Productivity, Setliik, I., Ed., Wageningen: Centre for Agricultural Publishing and Documentation, 1970, pp. 221–229.Google Scholar
  19. 19.
    Thornley, J.H.M., Plant growth and respiration re-visited: maintenance respiration defined—it is an emergent property of, not a separate process within, the system—and why the respiration: photosynthesis ratio is conservative, Ann. Bot., 2011, vol. 108, pp. 1365–1380.  https://doi.org/10.1093/aob/mcr238 CrossRefGoogle Scholar
  20. 20.
    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
  21. 21.
    Murrey, I.A., Components of productive respiration in photosynthetic plant tissues, Sov. Plant Physiol., 1985, vol. 32, pp. 61–69.Google Scholar
  22. 22.
    Murrey, I.A. and Rakhmankulova, Z.F., The ratio of photosynthesis and respiratory components in sugar beet plants during vegetative growth phase, Sov. Plant Physiol., 1990, vol. 37, pp. 462–467.Google Scholar
  23. 23.
    Rakhmankulova, Z.F., The relationship of photosynthesis and respiration of the whole plant under normal and stressful conditions, Zh. Obshch. Biol., 2002, vol. 63, pp. 44–53.Google Scholar
  24. 24.
    Nunes-Nesi, A., Sweetlove, L.J., and Fernie, A.R., Operation and function of the tricarboxylic acid cycle in the illuminated leaf, Physiol. Plant., 2007, vol. 129, pp. 45–56.  https://doi.org/10.1111/j.1399-3054.2006.00778.x CrossRefGoogle Scholar
  25. 25.
    Noguchi, K. and Yoshida, K., Interaction between photosynthesis and respiration in illuminated leaves, Mitochondrion, 2008, vol. 8, pp. 87–99.  https://doi.org/10.1016/j.mito.2007.09.003 CrossRefGoogle Scholar
  26. 26.
    Nunes-Nesi, A., Araújo, W.L., and Fernie, A.R., Targeting mitochondrial metabolism and machinery as a means to enhance photosynthesis, Plant Physiol., 2011, vol. 155, pp. 101–107.  https://doi.org/10.1104/pp.110.163816 CrossRefGoogle Scholar
  27. 27.
    Bauwe, H., Hagemann, M., Kern, R., and Timm, S., Photorespiration has a dual origin and manifold links to central metabolism, Curr. Opin. Plant Biol., 2012, vol. 15, pp. 269–275.  https://doi.org/10.1016/j.pbi.2012.01.008 CrossRefGoogle Scholar
  28. 28.
    Foyer, C.H., Noctor, G., and Hodges, M., Respiration and nitrogen assimilation: targeting mitochondria-associated metabolism as a means to enhance nitrogen use efficiency, J. Exp. Bot., 2011, vol. 62, pp. 1467–1482.  https://doi.org/10.1093/jxb/erq453 CrossRefGoogle Scholar
  29. 29.
    Gimeno, T.E., Sommerville, K.E., Valladares, F., and Atkin, O.K., Homeostasis of respiration under drought and its important consequences for foliar carbon balance in a drier climate: insights from two contrasting Acacia species, Funct. Plant Biol., 2010, vol. 37, pp. 323–333.CrossRefGoogle Scholar
  30. 30.
    Metcalfe, D.B., Lobo-do-Vale, R., Chaves, M.M., Maroco, J.P., Aragao, L., Malhi, Y., da Costa, A.L., Braga, A.P., Goncalves, P.L., de Athaydes, J., da Costa, M., Almeida, S.S., Campbell, C., Hurry, V., Williams, M., et al., Impacts of experimentally imposed drought on leaf respiration and morphology in an Amazon rain forest, Funct. Ecol., 2010, vol. 24, pp. 524–533.CrossRefGoogle Scholar
  31. 31.
    Nunes-Nesi, A., Fernie, A.R., and Stitt, M., Metabolic and signaling aspects underpinning the regulation of plant carbon nitrogen interactions, Mol. Plant, 2010, vol. 3, pp. 973–996.  https://doi.org/10.1093/mp/ssq049 CrossRefGoogle Scholar
  32. 32.
    Ghashghaie, J. and Badeck, F.W., Opposite carbon isotope discrimination during dark respiration in leaves versus roots—a review, New Phytol., 2013, vol. 201, pp. 751–769.CrossRefGoogle Scholar
  33. 33.
    Bidwell, R.G.S., Krotkov, G., and Reed, G.B., The influence of light and darkness on the metabolism of radioactive glucose and glutamine in wheat leaves, Can. J. Bot., 1955, vol. 33, pp. 189–196.CrossRefGoogle Scholar
  34. 34.
    Tovar-Mendez, A., Miernyk, J.A., and Randall, D.D., Regulation of pyruvate dehydrogenase complex activity in plant cells, Eur. J. Biochem., 2003, vol. 270, pp. 1043–1049.CrossRefGoogle Scholar
  35. 35.
    Tcherkez, G., Cornic, G., Bligny, R., Gout, E., and Ghashghaie, J., In vivo respiratory metabolism of illuminated leaves, Plant Physiol., 2005, vol. 138, pp. 1596–1606.CrossRefGoogle Scholar
  36. 36.
    Tcherkez, G., Bligny, R., Gout, E., Mahe, A., Hodges, M., and Cornic, G., Respiratory metabolism of illuminated leaves depends on CO2 and O2 conditions, Proc. Natl. Acad. Sci. USA, 2008, vol. 105, pp. 797–802.CrossRefGoogle Scholar
  37. 37.
    Gessler, A., Tcherkez, G., Karyanto, O., Keitel, C., Ferrio, J.P., Ghashghaie, J., Kreuzwieser, J., and Farquhar, G.D., On the metabolic origin of the carbon isotope composition of CO2 evolved from darkened light-acclimated leaves in Ricinus communis, New Phytol., 2009, vol. 181, pp. 374–386.CrossRefGoogle Scholar
  38. 38.
    Hurry, V., Igamberdiev, A.U., Keerberg, O., Pärnik, T., Atkin, O.K., Zaragoza-Castells, J., and Gardestrom, P., Respiration in photosynthetic cells: gas exchange components, interactions with photorespiration and the operation of mitochondria in the light, in Plant R-espiration, Lambers, H. and Ribas-Carbo, M., Eds., Berlin-Heidelberg: Springer Germany, 2005, pp. 43–61.Google Scholar
  39. 39.
    Farquhar, G.D. and Busch, F., Changes in the chloroplastic CO2 concentration explain much of the observed Kok effect: a model, New Phytol., 2017, vol. 214, pp. 570–584.CrossRefGoogle Scholar
  40. 40.
    Gong, X.Y., Tcherkez, G., Wenig, J., Schäufele, R., and Schnyder, H., Atmospheric CO2 mole fraction affects stand-scale carbon use efficiency of sunflower by stimulating respiration in light, Plant Cell Environ., 2017, vol. 40, pp. 401–412.CrossRefGoogle Scholar
  41. 41.
    Gong, X.Y., Tcherkez, G., Wenig, J., Schäufele, R., and Schnyder, H., Measurement of leaf day respiration using a new isotopic disequilibrium method compared with the Laisk method, bioRxiv, 2017.  https://doi.org/10.1101/201038
  42. 42.
    Kok, B., A critical consideration of the quantum yield of Chlorella photosynthesis, Enzymologia, 1948, vol. 13, pp. 1–56.Google Scholar
  43. 43.
    Kok, B., On the interrelation of respiration and photosynthesis in green plants, Biochim. Biophys. Acta, 1949, vol. 3, pp. 625–631.CrossRefGoogle Scholar
  44. 44.
    Laisk, A.Kh., Kinetika fotosinteza i fotodykhaniya C 3 ‑rastenii (Kinetics of Photosynthesis and Photorespiration of C3 Plants), Moscow: Nauka, 1977.Google Scholar
  45. 45.
    Atkin, O.K., Millar, A.H., Gardestrom, P., and Day,  D.A., Photosynthesis, carbohydrate metabolism and respiration in leaves of higher plants, in P-hotosynthesis: Physiology and Metabolism. Advances in Photosynthesis and Respiration, Leegood, R., Sharkey, T., and Caemmerer, S., Eds., London: Kluwer, 2000, vol. 9, pp. 53–175.Google Scholar
  46. 46.
    Cornic, G., Etude de l’inhibition de la respiration pars la lumiere chez la moutarde blanche (Sinapis alba L.), Physiol. Veg., 1973, vol. 11, pp. 663–679.Google Scholar
  47. 47.
    Pärnik, T. and Keerberg, O., Advanced radiogasometric method for the determination of the rates of photorespiratory and respiratory decarboxilations of primary and stored photosynthates under steady-state photosynthesis, Physiol. Plant., 2007, vol. 129, pp. 34–44.Google Scholar
  48. 48.
    Loreto, F., Velikova, V., and Di Marco, G., Respiration in the light measured by 12CO2 emission in 13CO2 atmosphere in maize leaves, Funct. Plant Biol., 2001, vol. 28, pp. 1103–1108.CrossRefGoogle Scholar
  49. 49.
    Gong, X.Y., Schaufele, R., Feneis, W., and Schnyder, H., 13CO2/12CO2 exchange fluxes in a clamp-on leaf cuvette: disentangling artefacts and flux components, Plant Cell Environ., 2015, vol. 38, pp. 2417–2432.CrossRefGoogle Scholar
  50. 50.
    Keerberg, O., Ivanova, H., Keerberg, H., and Pärnik, T., CO2 exchange of potato transformants with reduced activities of glycine decarboxylase, in Phytosfere'99—Hi-ghlights in European Plant Biotechnology, De Vries, G.E. and Metzlaff, K., Eds., Amsterdam: Elsevier, 1999, pp. 215–219.Google Scholar
  51. 51.
    Pärnik, T. and Keerberg, O., Decarboxylation of primary and end products of photosynthesis at different oxygen concentrations, J. Exp. Bot., 1995, vol. 46, pp. 1439–1440.Google Scholar
  52. 52.
    Sweetlove, L.J., Beard, K.F.M., Nunes-Nesi, A., Fernie, A.R., and Ratcliffe, R.G., Not just a circle: flux modes in the plant TCA cycle, Trends Plant Sci., 2010, vol. 15, pp. 462–470.CrossRefGoogle Scholar
  53. 53.
    Garmash, E.V., Mitochondrial respiration of the photosynthesizing cell, Russ. J. Plant Physiol., 2016, vol. 63, pp. 13–25.CrossRefGoogle Scholar
  54. 54.
    Huntingford, C., Harris, P.P., Gedney, N., Cox, P.M., Betts, R.A., Marengo, J.A., and Gash, J.H.C., Using a GCM analogue model to investigate the potential for Amazonian forest dieback, Theor. Appl. Climatol., 2004, vol. 78, pp. 177–185.CrossRefGoogle Scholar
  55. 55.
    Gifford, R.M., Whole plant respiration and photosynthesis of wheat under increased CO2 concentration and temperature: long-term vs short-term distinctions for modeling, Global Change Biol., 1995, vol. 1, pp. 385–396.CrossRefGoogle Scholar
  56. 56.
    Ryan, M.G., Hubbard, R.M., Pongracic, S., Raison, R.J., and McMurtrie, R.E., Foliage, fine-root, woody-tissue and stand respiration in Pinus radiata in relation to nitrogen status, Tree Physiol., 1996, vol. 16, pp. 333–343.CrossRefGoogle Scholar
  57. 57.
    Goetz, S.J. and Prince, S.D., Variability in carbon exchange and light utilization among boreal forest stands: implications for remote sensing of net primary production, Can. J. For. Res., 1998, vol. 28, pp. 375–389.Google Scholar
  58. 58.
    Winzeler, H., Hunt, L.A., and Mahon, J.D., Ontogenetic changes in respiration and photosynthesis in a uniculm barley, Crop Sci., 1976, vol. 16, pp. 786–790.CrossRefGoogle Scholar
  59. 59.
    Keith, H., Raison, R.J., and Jacobsen, K.L., Allocation of carbon in a mature eucalypt forest and some effects of soil phosphorus availability, Plant Soil, 1997, vol. 196, pp. 81–99.CrossRefGoogle Scholar
  60. 60.
    Monje, O. and Bugbee, B., Adaptation to high CO2 concentration in an optimal environment: radiation capture, canopy quantum yield and carbon use efficiency, Plant Cell Environ., 1998, vol. 21, pp. 315–324.CrossRefGoogle Scholar
  61. 61.
    Malhi, Y., Baldocchi, D.D., and Jarvis, P.G., The carbon balance of tropical, temperate and boreal forests, Plant Cell Environ., 1999, vol. 22, pp. 715–740.CrossRefGoogle Scholar
  62. 62.
    Atkin, O.K., Bruhn, D., Hurry, V.M., and Tjoelker, M.G., The hot and the cold: unravelling the variable response of plant respiration to temperature, Funct. Plant Biol., 2005, vol. 32, pp. 87–105.CrossRefGoogle Scholar
  63. 63.
    Murrey, I.A. and Shul’gin, I.A., Physiological analysis of incoming PAR to the plant, Bot. Zh., 1978, vol. 63, pp. 962–973.Google Scholar
  64. 64.
    Golovko, T.K., Dykhanie rastenii (fiziologicheskie aspekty) (Plant Respiration: Physiological Aspects), St. Petersburg: Nauka, 1999.Google Scholar
  65. 65.
    Mokronosov, A.T., Ontogeneticheskii aspekt fotosinteza (Ontogenetic Aspect of Photosynthesis), Moscow: Nauka, 1981.Google Scholar
  66. 66.
    Semikhatova, O.A., Ivanova, T.I., and Kirpichnikova, O.V., Respiration rate of Arctic plants as related to the production process, Russ. J. Plant Physiol., 2009, vol. 56, pp. 306–315.CrossRefGoogle Scholar
  67. 67.
    Semikhatova, O.A. and Zalenskii, O.V., Conjugacy of photosynthesis and respiration, in Fiziologiya fotosinteza (Physiology of Photosynthesis), Nichiporovich, A.A., Ed., Moscow: Nauka, 1982.Google Scholar
  68. 68.
    Murrey, I.A., Kinetics of photosynthesis and respiration of Zea mays plant after the dark period, Sov. Plant Physiol., 1984, vol. 31, pp. 433–438.Google Scholar
  69. 69.
    Murrey, I.A. and Velichkov, D.K., The rate of visible photosynthesis and respiration in sunflower and maize, Sov. Plant Physiol., 1981, vol. 28, pp. 1109–1118.Google Scholar
  70. 70.
    Murrey, I.A. and Velichkov, D.K., Analysis of productive respiration in photosynthetic tissues of the whole plant, Sov. Plant Physiol., 1983, vol. 30, pp. 1126–1133.Google Scholar
  71. 71.
    Murrey, I.A., Parameters of integral pools of assimilates in photosynthetic plant tissues, Sov. Plant Physiol., 1984, vol. 31, pp. 1049–1055.Google Scholar
  72. 72.
    Murrey, I.A. and Rakhmankulova, Z.F., The relationship between photosynthesis and dark modified respiration in the light of maize, Sov. Plant Physiol., 1990, vol. 37, pp. 468–475.Google Scholar

Copyright information

© Pleiades Publishing, Ltd. 2019

Authors and Affiliations

  1. 1.Timiryazev Institute of Plant Physiology, Russian Academy of SciencesMoscowRussia

Personalised recommendations