Advertisement

Biochemistry (Moscow)

, Volume 79, Issue 3, pp 273–281 | Cite as

Long-distance signal transmission and regulation of photosynthesis in characean cells

  • A. A. BulychevEmail author
  • A. V. Komarova
Review

Abstract

Photosynthetic electron transport in an intact cell is finely regulated by the structural flexibility of thylakoid membranes, existence of alternative electron-transport pathways, generation of electrochemical proton gradient, and continuous exchange of ions and metabolites between cell organelles and the cytoplasm. Long-distance interactions underlying reversible transitions of photosynthetic activity between uniform and spatially heterogeneous distributions are of particular interest. Microfluorometric studies of characean cells with the use of saturating light pulses and in combination with electrode micromethods revealed three mechanisms of distant regulation ensuring functional coordination of cell domains and signal transmission over long distances. These include: (1) circulation of electric currents between functionally distinct cell domains, (2) propagation of action potential along the cell length, and (3) continuous cyclical cytoplasmic streaming. This review considers how photosynthetic activity depends on membrane transport of protons and cytoplasmic pH, on ion fluxes associated with the electrical excitation of the plasmalemma, and on the transmission of photoinduced signals with streaming cytoplasm. Because of signal transmission with cytoplasmic flow, dynamic changes in photosynthetic activity can develop far from the point of photostimulus application and with a long delay (up to 100 s) after a light pulse stimulus is extinguished.

Key words

Chara corallina transmembrane H+ fluxes chlorophyll fluorescence photosynthetic electron transport intracellular diffusion action potential cytoplasmic streaming 

Abbreviations

AP

action potential

NPQ

non-photochemical quenching

pHc

cytoplasmic pH

pHo

pH on the outer cell surface

PSII

photosystem II

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References

  1. 1.
    Allen, J. F., and Forsberg, J. (2001) Trends Plant Sci., 6, 317–326.PubMedCrossRefGoogle Scholar
  2. 2.
    Bulychev, A. A., and Vredenberg, W. J. (1999) Physiol. Plant., 105, 577–584.CrossRefGoogle Scholar
  3. 3.
    Kramer, D. M., Avenson, T. J., Kanazawa, A., Cruz, J. A., Ivanov, B., and Edwards, G. E. (2004) in Chlorophyll a Fluorescence: A Signature of Photosynthesis (Papageorgiou, G. C., and Govindjee, eds.) Springer, Dordrecht, pp. 251–278.Google Scholar
  4. 4.
    Flügge, U.-N., and Heldt, H. W. (1991) Annu. Rev. Plant Physiol. Plant Mol. Biol., 42, 129–144.CrossRefGoogle Scholar
  5. 5.
    Siebke, K., and Weis, E. (1995) Photosynth. Res., 45, 225–237.PubMedCrossRefGoogle Scholar
  6. 6.
    Schurr, U., Walter, A., and Rascher, U. (2006) Plant Cell Environ., 29, 340–352.PubMedCrossRefGoogle Scholar
  7. 7.
    Baker, N. R. (2008) Annu. Rev. Plant Biol., 59, 89–113.PubMedCrossRefGoogle Scholar
  8. 8.
    Bulychev, A. A., Cherkashin, A. A., Rubin, A. B., Vredenberg, W. J., Zykov, V. S., and Müller, S. C. (2001) Bioelectrochemistry, 53, 225–232.PubMedCrossRefGoogle Scholar
  9. 9.
    Krupenina, N. A., Bulychev, A. A., Roelfsema, M. B. G., and Schreiber, U. (2008) Photochem. Photobiol. Sci., 7, 681–688.PubMedCrossRefGoogle Scholar
  10. 10.
    Krupenina, N. A., and Bulychev, A. A. (2007) Biochim. Biophys. Acta, 1767, 781–788.PubMedCrossRefGoogle Scholar
  11. 11.
    Bulychev, A. A., Polezhaev, A. A., Zykov, S. V., Pljusnina, T. Y., Riznichenko, G. Y., Rubin, A. B., Jantoss, W., Zykov, V. S., and Müller, S. C. (2001) J. Theor. Biol., 212, 275–294.PubMedCrossRefGoogle Scholar
  12. 12.
    Verchot-Lubicz, J., and Goldstein, R. E. (2010) Protoplasma, 240, 99–107.PubMedCrossRefGoogle Scholar
  13. 13.
    Lucas, W. J., Keifer, D. W., and Sanders, D. (1983) J. Membr. Biol., 73, 263–274.CrossRefGoogle Scholar
  14. 14.
    Lucas, W. J., and Nuccitelli, R. (1980) Planta, 150, 120–131.PubMedCrossRefGoogle Scholar
  15. 15.
    Beilby, M. J., and Bisson, M. A. (2012) in Plant Electrophysiology: Methods and Cell Electrophysiology (Volkov, A. G., ed.) Springer, Berlin, pp. 247–271.Google Scholar
  16. 16.
    Schmölzer, P. M., Höftberger, M., and Foissner, I. (2011) Plant Cell Physiol., 52, 1274–1288PubMedCentralPubMedCrossRefGoogle Scholar
  17. 17.
    Bulychev, A. A., Wijngaard, P. W. J., and de Boer, A. H. (2005) Biochemistry (Moscow), 70, 55–61.CrossRefGoogle Scholar
  18. 18.
    Bisson, M. A., and Walker, N. A. (1980) J. Membr. Biol., 56, 1–7.CrossRefGoogle Scholar
  19. 19.
    Smith, J. R., and Walker, N. A. (1983) J. Membr. Biol., 73, 193–202.CrossRefGoogle Scholar
  20. 20.
    Foissner, I. (2004) Protoplasma, 224, 145–157.PubMedCrossRefGoogle Scholar
  21. 21.
    Antonenko, Y. N., and Bulychev, A. A. (1991) Biochim. Biophys. Acta, 1070, 279–282.CrossRefGoogle Scholar
  22. 22.
    Feijó, J. A., Sainhas, J., Hackett, G. R., Kunkel, J. G., and Hepler, P. K. (1999) J. Cell Biol., 144, 483–496.PubMedCentralPubMedCrossRefGoogle Scholar
  23. 23.
    Takeshige, K., and Tazawa, M. (1989) Plant Physiol., 89, 1049–1052.PubMedCentralPubMedCrossRefGoogle Scholar
  24. 24.
    Hou, G., Kramer, V. L., Wang, Y.-S., Chen, R., Perbal, G., Gilroy, S., and Blancaflor, E. B. (2004) Plant J., 39, 113–125.PubMedCrossRefGoogle Scholar
  25. 25.
    Felle, H., and Bertl, A. (1986) Biochim. Biophys. Acta, 848, 176–182.CrossRefGoogle Scholar
  26. 26.
    Bulychev, A. A., Alova, A. V., and Rubin, A. B. (2013) Eur. Biophys. J., 42, 441–453.PubMedCrossRefGoogle Scholar
  27. 27.
    Johnson, M. P., Zia, A., and Ruban, A. V. (2012) Planta, 235, 193–204.PubMedCrossRefGoogle Scholar
  28. 28.
    Beilby, M. J. (2007) Int. Rev. Cytol., 257, 43–82.PubMedCrossRefGoogle Scholar
  29. 29.
    Bulychev, A. A., and Kamzolkina, N. A. (2006) Bioelectrochemistry, 69, 209–215.PubMedCrossRefGoogle Scholar
  30. 30.
    Bulychev, A. A., and Krupenina, N. A. (2009) Plant Signal. Behav., 4, 24–31.CrossRefGoogle Scholar
  31. 31.
    Eremin, A., Bulychev, A. A., Krupenina, N. A., Mair, T., Hauser, M. J. B., Stannarius, R., Müller, S. C., and Rubin, A. B. (2007) Photochem. Photobiol. Sci., 6, 103–109.PubMedCrossRefGoogle Scholar
  32. 32.
    Berestovsky, G. N., and Kataev, A. A. (2005) Eur. Biophys. J., 34, 973–986.PubMedCrossRefGoogle Scholar
  33. 33.
    Hepler, P. K. (2005) Plant Cell, 17, 2142–2155.PubMedCentralPubMedCrossRefGoogle Scholar
  34. 34.
    Dodonova, S. O., Krupenina, N. A., and Bulychev, A. A. (2010) Biochemistry (Moscow), Suppl. Series A: Membr. Cell Biol., 4, 389–396.CrossRefGoogle Scholar
  35. 35.
    De Nisi, P., Dell’Orto, M., Pirovano, L., and Zocchi, G. (1999) Planta, 209, 187–194.PubMedCrossRefGoogle Scholar
  36. 36.
    Kinoshita, T., Nishimura, M., and Shimazaki, K. (1995) Plant Cell, 7, 1333–1342.PubMedCentralPubMedGoogle Scholar
  37. 37.
    Lino, B., Baizabal-Aguirre, V. M., and De la Vara, L. E. G. (1998) Planta, 204, 352–359.PubMedCrossRefGoogle Scholar
  38. 38.
    Muto, S., Izawa, S., and Miyachi, S. (1982) FEBS Lett., 139, 250–254.CrossRefGoogle Scholar
  39. 39.
    Johnson, C. H., Shingles, R., and Ettinger, W. F. (2006) in The Structure and Function of Plastids (Wise, R. R., and Hoober, J. K., eds.) Springer, Dordrecht, The Netherlands, pp. 403–416.Google Scholar
  40. 40.
    Plieth, C., Sattelmacher, B., and Hansen, U.-P. (1997) Protoplasma, 198, 107–124.CrossRefGoogle Scholar
  41. 41.
    Krupenina, N. A., Bulychev, A. A., and Schreiber, U. (2011) Protoplasma, 248, 513–522.PubMedCrossRefGoogle Scholar
  42. 42.
    Shimmen, T., and Yokota, E. (2004) Curr. Opin. Cell Biol., 16, 68–72.PubMedCrossRefGoogle Scholar
  43. 43.
    Kimura, Y., Toyoshima, N., Hirakawa, N., Okamoto, K., and Ishijima, A. (2003) J. Mol. Biol., 328, 939–950.PubMedCrossRefGoogle Scholar
  44. 44.
    Pickard, W. F. (2003) Plant Cell Environ., 26, 1–15.CrossRefGoogle Scholar
  45. 45.
    Bulychev, A. A., and Dodonova, S. O. (2011) Russ. J. Plant Physiol., 58, 233–237.CrossRefGoogle Scholar
  46. 46.
    Dodonova, S. O., and Bulychev, A. A. (2011) Protoplasma, 248, 737–749.PubMedCrossRefGoogle Scholar
  47. 47.
    Bulychev, A. A. (2012) in Plant Electrophysiology: Methods and Cell Electrophysiology (Volkov, A. G., ed.) Springer, Berlin, pp. 273–300.Google Scholar
  48. 48.
    Shimmen, T., and Yamamoto, A. (2002) Plant Cell Physiol., 43, 980–983.PubMedCrossRefGoogle Scholar
  49. 49.
    Bulychev, A. A., Alova, A. V., and Bibikova, T. N. (2013) Biochim. Biophys. Acta, 1828, 2359–2369.PubMedCrossRefGoogle Scholar
  50. 50.
    Bulychev, A. A., and Dodonova, S. O. (2011) Biochim. Biophys. Acta, 1807, 1221–1230.PubMedCrossRefGoogle Scholar
  51. 51.
    Dodonova, S. O., and Bulychev, A. A. (2012) Russ. J. Plant Physiol., 59, 35–41.CrossRefGoogle Scholar
  52. 52.
    Remiš, D., Bulychev, A. A., and Kurella, G. A. (1988) J. Exp. Bot., 39, 633–640.CrossRefGoogle Scholar
  53. 53.
    Eremin, A., Bulychev, A. A., and Hauser, M. J. B. (2013) Protoplasma, 250, 1339–1349.PubMedCrossRefGoogle Scholar
  54. 54.
    Kreimer, G., Melkonian, M., and Latzko, E. (1985) FEBS Lett., 180, 253–258.CrossRefGoogle Scholar

Copyright information

© Pleiades Publishing, Ltd. 2014

Authors and Affiliations

  1. 1.Department of Biophysics, Faculty of BiologyLomonosov Moscow State UniversityMoscowRussia

Personalised recommendations