Advertisement

Lateral transport of photosynthetically active intermediate at rest and after excitation of Chara cells

  • A. A. Bulychev
  • A. V. Komarova
Articles
  • 45 Downloads

Abstract

Cytoplasmic streaming is vital for plant cells; however, its relation to cell functions remains largely undisclosed. Microfluorometry of chloroplasts in vivo and measurements of cell surface pH under localized illumination of cell regions located upstream the cytoplasmic flow, at a distance of few millimeters from the analyzed area, is a new means to reveal the role of liquid flow for signal transmission in large cells, such as internodes of characean algae. Properties of photoinduced signals transmitted along the cell can be clarified by comparing the effects of pointed illumination under conditions of continuous and briefly arrested cytoplasmic flow. Chlorophyll fluorescence measurements with the use of saturation pulse method showed that excitation-induced cessation of cytoplasmic streaming, concomitant with the period of localized illumination, caused a significant delay and deceleration of the lateral transmission of the photoinduced signal and, in addition, diminished the peak of maximal fluorescence F m′ in the cell response to propagated signals. The relative extent of the peak suppression was small in cell regions producing light-dependent external alkaline zones and increased substantially for cell regions with slightly acidic external pH. These and other results indicate the possible role of cytoplasmic pH in controlling chlorophyll fluorescence and photosynthetic activity in vivo. When the period of streaming cessation coincided with localized illumination, the velocity of cytoplasmic flow recovered slower than after arrest of the flow without additional illumination. The results are promising for further analysis of regulatory and protective functions of cytoplasmic streaming in photosynthesizing plant cells.

Keywords

Characeae cytoplasmic streaming action potential chlorophyll fluorescence alkaline and acid zones proton transport 

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References

  1. 1.
    Pickard W.F. 2003. The role of cytoplasmic streaming in symplastic transport. Plant, Cell Environ. 26, 1–15.CrossRefGoogle Scholar
  2. 2.
    Verchot-Lubicz J., Goldstein R.E. 2010. Cytoplasmic streaming enables the distribution of molecules and vesicles in large plant cells. Protoplasma. 240, 99–107.PubMedCrossRefGoogle Scholar
  3. 3.
    Goldstein R.E., Tuval I., van de Meent J.W. 2008. Microfluidics of cytoplasmic streaming and its implications for intracellular transport. Proc. Natl. Acad. Sci. USA. 105, 3663–3667.PubMedCentralPubMedCrossRefGoogle Scholar
  4. 4.
    Bulychev A.A., Dodonova S.O. 2011. Effects of cyclosis on chloroplast-cytoplasm interactions revealed with localized lighting in Characean cells at rest and after electrical excitation. Biochim. Biophys. Acta. 1807, 1221–1230.PubMedCrossRefGoogle Scholar
  5. 5.
    Dodonova S.O., Bulychev A.A. 2011. Cyclosis-related asymmetry of chloroplast-plasma membrane interactions at the margins of illuminated area in Chara corallina cells. Protoplasma. 248, 737–749.PubMedCrossRefGoogle Scholar
  6. 6.
    Eremin A., Bulychev A.A., Hauser M.J.B. 2013. Cyclosis-mediated transfer of H2O2 elicited by localized illumination of Chara cells and its relevance to the formation of pH bands. Protoplasma. 250, 1339–1349.PubMedCrossRefGoogle Scholar
  7. 7.
    Bulychev A.A., Alova A.V., Rubin A.B. 2013. Propagation of photoinduced signals with the cytoplasmic flow along Characean internodes: Evidence from changes in chloroplast fluorescence and surface pH. Eur. Biophys. J. 42, 441–453.PubMedCrossRefGoogle Scholar
  8. 8.
    Bulychev A.A., Alova A.V., Rubin A.B. 2013. Fluorescence transients in chloroplasts of Chara corallina cells during transmission of photoinduced signal with the streaming cytoplasm. Russ. J. Plant Physiol. 60, 33–40.CrossRefGoogle Scholar
  9. 9.
    Harada A., Shimazaki K. 2009. Measurement of changes in cytosolic Ca2+ in Arabidopsis guard cells and mesophyll cells in response to blue light. Plant Cell Physiol. 50, 360–373.PubMedCrossRefGoogle Scholar
  10. 10.
    Miller A.J., Sanders D. 1987. Depletion of cytosolic free calcium induced by photosynthesis. Nature. 326, 397–400.CrossRefGoogle Scholar
  11. 11.
    Remiš D., Bulychev A.A., Kurella G.A. 1988. Photoinduced pH changes in the vicinity of isolated Peperomia metallica chloroplasts. J. Exp. Bot. 39, 633–640.CrossRefGoogle Scholar
  12. 12.
    Naydov I.A., Mubarakshina M.M., Ivanov B.N. 2012. Formation kinetics and H2O2 distribution in chloroplasts and protoplasts of photosynthetic leaf cells of higher plants under illumination. Biochemistry (Moscow). 77, 143–151.PubMedCrossRefGoogle Scholar
  13. 13.
    Felle H., Bertl A. 1986. Light-induced cytoplasmic pH changes and their interrelation to the activity of the electrogenic proton pump in Riccia fluitans. Biochim. Biophys. Acta. 848, 176–182.CrossRefGoogle Scholar
  14. 14.
    Kamiya N. 1959. Protoplasmic streaming. Wien: Springer.CrossRefGoogle Scholar
  15. 15.
    Williamson R.E., Ashley C.C. 1982. Free Ca2+ and cytoplasmic streaming in the alga Chara. Nature. 296, 647–651.PubMedCrossRefGoogle Scholar
  16. 16.
    Tominaga Y., Shimmen T., Tazawa M. 1983. Control of cytoplasmic streaming by extracellular Ca2+ in permeabilized Nitella cells. Protoplasma. 116, 75–77.CrossRefGoogle Scholar
  17. 17.
    Yokota E., Muto S., Shimmen T. 1999. Inhibitory regulation of higher-plant myosin by Ca2+ ions. Plant Physiol. 119, 231–239.PubMedCentralPubMedCrossRefGoogle Scholar
  18. 18.
    Shimmen T. 2007. The sliding theory of cytoplasmic streaming: Fifty years of progress. J. Plant Res. 120, 31–43.PubMedCrossRefGoogle Scholar
  19. 19.
    Awata J., Saitoh K., Shimada K., Kashiyama T., Yamamoto K. 2001. Effects of Ca2+ and calmodulin on the motile activity of characean myosin in vitro. Plant Cell Physiol. 42, 828–834.PubMedCrossRefGoogle Scholar
  20. 20.
    Tsuchiya Y., Yamazaki H., Aoki T. 1991. Steady and transient behaviors of protoplasmic streaming in Nitella internodal cell. Biophys. J. 59, 249–251.PubMedCentralPubMedCrossRefGoogle Scholar
  21. 21.
    Bulychev A.A., Kamzolkina N.A. 2006. Differential effects of plasma membrane electric excitation on H+ fluxes and photosynthesis in characean cells. Bioelectrochemistry. 69, 209–215.PubMedCrossRefGoogle Scholar
  22. 22.
    Bulychev A.A., Kamzolkina N.A. 2006. Effect of action potential on photosynthesis and spatially distributed H+ fluxes in cells and chloroplasts of Chara corallina. Russ. J. Plant Physiol. 53, 1–9.CrossRefGoogle Scholar
  23. 23.
    Bulychev A.A., Kamzolkina N.A., Luengviriya J., Rubin A.B., Mueller S.C. 2004. Effect of a single excitation stimulus on photosynthetic activity and lightdependent pH banding in Chara cells. J. Membr. Biol. 202, 11–19.PubMedCrossRefGoogle Scholar
  24. 24.
    Krupenina N.A., Bulychev A.A. 2007. Action potential in a plant cell lowers the light requirement for non-photochemical energy-dependent quenching of chlorophyll fluorescence. Biochim. Biophys. Acta. 1767, 781–788.PubMedCrossRefGoogle Scholar
  25. 25.
    Bulychev A.A. 2012. Membrane excitation and cytoplasmic streaming as modulators of photosynthesis and proton flows in Characean cells. In: Plant electrophysiology: Methods and cell electrophysiology. Ed. Volkov A.G. Berlin: Springer, p. 273–300.CrossRefGoogle Scholar
  26. 26.
    van de Meent J.W., Sederman A.J., Gladden L.F., Goldstein R.E. 2010. Measurement of cytoplasmic streaming in single plant cells by magnetic resonance velocimetry. J. Fluid Mech. 642, 5–14.CrossRefGoogle Scholar
  27. 27.
    Krupenina N.A., Bulychev A.A., Roelfsema M.B.G., Schreiber U. 2008. Action potential in Chara cells intensifies spatial patterns of photosynthetic electron flow and non-photochemical quenching in parallel with inhibition of pH banding. Photochem. Photobiol. Sci. 7, 681–688.PubMedCrossRefGoogle Scholar
  28. 28.
    Bulychev A.A., Krupenina N.A. 2009. Transient removal of alkaline zones after excitation of Chara cells is associated with inactivation of high conductance in the plasmalemma. Plant Signal. Behav. 4, 24–31.CrossRefGoogle Scholar

Copyright information

© Pleiades Publishing, Ltd. 2014

Authors and Affiliations

  1. 1.Department of Biophysics, Faculty of BiologyMoscow Lomonosov State UniversityMoscowRussia

Personalised recommendations