Skip to main content
SpringerLink
Log in

Reorganization of chloroplast ultrastructure associated with low-temperature hardening of Arabidopsis plants

  • Research Papers
  • Published:
Russian Journal of Plant Physiology Aims and scope Submit manuscript

Abstract

When following low-temperature acclimation (5 days at 2°C) of cold-resistant plants of Arabidopsis (Arabidopsis thaliana Heynh. (L.), ecotype Columbia) in relation to the changes in chloroplast ultrastructure, we registered the high efficiency of hardening and the ability of hardened plants to lower a threshold of frost damage by about 3°C. During hardening, the area of grana in the chloroplasts more than doubled, with considerably increased numbers of thylakoids per granum and thylakoids per chloroplast. The rate of apparent photosynthesis decreased to lesser extent than the rate of dark respiration, as a result the content of soluble sugars increased fourfold, ensuring an adaptive reorganization of metabolism, which enabled the hardened plants to survive even at below-zero temperatures (up to −7°C). The authors conclude that a considerable increase in the number of thylakoids in the chloroplasts helps maintain photosynthesis at low above-zero temperatures and is a prerequisite for the accumulation of soluble sugars in Arabidopsis leaves.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

References

  1. Larcher, W., Physiological Plant Ecology. Ecophysiology and Stress Physiology of Functional Groups, Berlin: Springer-Verlag, 2003.

    Google Scholar 

  2. Sandukhidze, B.I., Rybakova, M.I., and Morozova, Z.A., Nauchnye osnovy selektsii ozimoi pshenitsy v nechernozemnoi zone Rossii (Scientific Basics for the Winter Wheat Breeding in the Non-Chernozem Zone of Russia), Moscow: Ros. Akad. S-Kh. Nauk, 2003.

    Google Scholar 

  3. Trunova, T.I., Rastenie i nizkotemperaturnyi stress, 64-e Timiryazevskoe chtenie (Plant and Low Temperature Stress, the 64th Timiryazev Lecture), Moscow: Nauka, 2007.

    Google Scholar 

  4. Upchurch, R.G., Fatty acid unsaturation, mobilization, and regulation in the response of plants to stress, Biotechnol. Lett., 2008, vol. 30, pp. 967–977.

    Article  PubMed  CAS  Google Scholar 

  5. Korn, M., Peterek, S., Mock, H.P., Heyer, A.G., and Hincha, D.K., Heterosis in the freezing tolerance and sugar and flavonoid contents of crosses between Arabidopsis thaliana accessions of widely varying freezing tolerance, Plant Cell Environ., 2008, vol. 31, pp. 813–827.

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  6. Moffatt, B., Ewart, V., and Eastman, A., Cold comfort: plant antifreeze proteins, Physiol. Plant., 2006, vol. 126, pp. 5–16.

    Article  CAS  Google Scholar 

  7. Shao, H.B., Chu, L.Y., Lu, Z.H., and Kang, C.M., Primary antioxidant free radical scavenging and redox signaling pathways in higher plant cells, Int. J. Biol. Sci., 2008, vol. 4, pp. 8–14.

    Article  CAS  PubMed Central  Google Scholar 

  8. Fowler, S. and Thomashow, M.F., Arabidopsis transcriptome profiling indicates that multiple regulatory pathways are activated during cold acclimation in addition to the CBF cold response pathway, Plant Cell, 2002, vol. 14, pp. 1675–1690.

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  9. Kreps, J.A., Wu, Y., Chang, H.S., Zhu, T., Wang, X., and Harper, J.F., Transcriptome changes for Arabidopsis in response to salt, osmotic and cold stress, Plant Physiol., 2002, vol. 130, pp. 2129–2141.

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  10. Vogel, J.T., Zarka, D.G., van Buskirk, H.A., Fowler, S.G., and Thomashow, M.F., Roles of the CBF2 and ZAT12 transcription factors in configuring the low temperature transcriptome of Arabidopsis, Plant J., 2005, vol. 41, pp. 195–211.

    Article  PubMed  CAS  Google Scholar 

  11. Hasdai, M., Weiss, B., Levi, A., Samach, A., and Porat, R., Differential responses of Arabidopsis ecotypes to cold, chilling and freezing temperatures, Ann. Appl. Biol., 2006, vol. 148, pp. 113–120.

    Article  Google Scholar 

  12. Zuther, E., Schulz, E., Childs, L.H., and Hincha, D.K., Clinal variation in the non-acclimated and cold-acclimated freezing tolerance of Arabidopsis thaliana accessions, Plant Cell Environ., 2012, vol. 35, pp. 1860–1878.

    Article  PubMed  CAS  Google Scholar 

  13. Campos, P.S., Quartin, V., Ramalho, J.C., and Nunes, M.A., Electrolyte leakage and lipid degradation account for cold sensitivity in leaves of Coffea sp. plants, J. Plant Physiol., 2003, vol. 160, pp. 283–292.

    Article  PubMed  CAS  Google Scholar 

  14. Turkina, M.V. and Sokolova, S.V., Methods for determination of monosaccharides and oligosaccharides, Biokhimicheskie metody v fiziologii rastenii (Biochemical Methods in Plant Physiology), Pavlinova, O.A., Ed., Moscow: Nauka, 1971, pp. 7–34.

    Google Scholar 

  15. Klimov, S.V., Cold hardening of plants — the result of maintaining an elevated ratio photosynthesis/respiration under low temperatures, Izv. Akad. Nauk, Ser. Biol., 2003, vol. 30, pp. 57–62.

    Google Scholar 

  16. Trunova, T.I., Astakhova, N.V., Deryabin, A.N., and Sabel’nikova, E.P., Ultrastructural organization of chloroplasts in leaves of potato plants transformed with yeast invertase gene in normal conditions and under hypothermia, Dokl. Akad. Nauk, 2003, vol. 389, pp. 842–845.

    Google Scholar 

  17. Dospekhov, B.A., Metodika opytnogo dela (Methodology of Experimental Work), Moscow: Kolos, 1977.

    Google Scholar 

  18. Klimov, S.V., Dubinina, I.M., Burakhanova, E.A., Astakhova, N.V., Popov, V.N., Alieva, G.P., and Trunova, T.I., Association of CO2 exchange with sugar accumulation and invertase activity under winter wheat cold hardening, Dokl. Akad. Nauk, 2004, vol. 398, pp. 135–138.

    Google Scholar 

  19. Ashworth, E.N. and Pearce, R.S., Extracellular freezing in leaves of freezing-sensitive species, Planta, 2002, vol. 214, pp. 798–805.

    Article  PubMed  CAS  Google Scholar 

  20. Klimov, S.V., Pathways for plant low temperature adaptation, Usp. Sovrem. Biol., 2001, vol. 121, pp. 3–22.

    CAS  Google Scholar 

  21. Margesin, R., Neuner, G., and Storey, K.B., Cold-loving microbes, plants, and animals — fundamental and applied aspects, Naturwissenschaften, 2007, vol. 94, pp. 77–99.

    Article  PubMed  CAS  Google Scholar 

  22. Ma, Y., Zhang, Y., Lu, J., and Shao, H., Roles of plant soluble sugars and their responses to plant cold stress, Afr. J. Biotechnol, 2009, vol. 8, p. 2004.

  23. Janska, A., Marsik, P., Zelenkova, S., and Ovesna, J., Cold stress and acclimation — what is important for metabolic adjustment? Plant Biol., 2010, vol. 12, pp. 395–405.

    Article  PubMed  CAS  Google Scholar 

  24. Sowinski, P., Rudzinska-Langwald, A., Adamczyk, J., Kubica, W., and Fronk, J., Recovery of maize seedling growth, development and photosynthetic efficiency after initial growth at low temperature, J. Plant Physiol., 2005, vol. 162, pp. 67–80.

    Article  PubMed  CAS  Google Scholar 

  25. Kutik, J., Hola, D., Kocova, M., Rothova, O., Haisel, D., Wilhelmova, N., and Ticha, I., Ultrastructure and dimensions of chloroplasts in leaves of three maize (Zea mays L.) inbred lines and their F1 hybrids grown under moderate chilling stress, Photosynthetica, 2004, vol. 42, pp. 447–455.

    Article  Google Scholar 

  26. Kratsch, H.A. and Wise, R.R., The ultrastructure of chilling stress, Plant Cell Environ., 2000, vol. 23, pp. 337–350.

    Article  CAS  Google Scholar 

  27. Popov, V.N., Antipina, O.V., Pchelkin, V.P., and Tsydendambaev, V.D., Changes in the content and composition of lipid fatty acids in tobacco leaves and roots at low-temperature hardening, Russ. J. Plant Physiol., 2012, vol. 59, pp. 177–182.

    Article  CAS  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Timiryazev Institute of Plant Physiology, Russian Academy of Sciences, Botanicheskaya ul. 35, Moscow, 127276, Russia

    N. V. Astakhova, V. N. Popov, A. A. Selivanov, E. A. Burakhanova, G. P. Alieva & I. E. Moshkov

Authors
  1. N. V. Astakhova
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. V. N. Popov
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. A. A. Selivanov
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. E. A. Burakhanova
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. G. P. Alieva
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. I. E. Moshkov
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to N. V. Astakhova.

Additional information

Original Russian Text © N.V. Astakhova, V.N. Popov, A.A. Selivanov, E.A. Burakhanova, G.P. Alieva, I.E. Moshkov, 2014, published in Fiziologiya Rastenii, 2014, Vol. 61, No. 6, pp. 790–797.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Astakhova, N.V., Popov, V.N., Selivanov, A.A. et al. Reorganization of chloroplast ultrastructure associated with low-temperature hardening of Arabidopsis plants. Russ J Plant Physiol 61, 744–750 (2014). https://doi.org/10.1134/S102144371406003X

Download citation

  • Received:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1134/S102144371406003X

Keywords

Search

Navigation