Skip to main content
SpringerLink
Log in

Cytoplasmic Streaming as an Intracellular Conveyer: Effect on Photosynthesis and H+ Fluxes in Chara Cells

  • CELL BIOPHYSICS
  • Published:
Biophysics Aims and scope Submit manuscript

Abstract

Giant-sized cells, such as the internodes of characean algae, demonstrate rapid (up to 100 μm/s) rotational cytoplasmic streaming that participates in long-distance intracellular interactions and coordinates the functional activity of organelles under a nonuniform light environment. The specific functions of intense cytoplasmic streaming remain poorly investigated. The lateral transport of photometabolites can be detected by combining pinhole illumination with measurements of chlorophyll fluorescence and external pH on microscopic cell regions located downstream of the locally illuminated area. The involvement of cyclosis in regulation of photosynthesis and plasmalemmal H+ transport was revealed by this means. In regions exposed to bright local light, the chloroplasts export reducing equivalents and triose phosphates into the streaming cytoplasm that spread over the cell and induce a transient rise of chlorophyll fluorescence in shaded cell areas located far from the site of photostimulus application. This review highlights the properties of cyclosis-mediated fluorescence changes, including the photoinduction of long-distance transmission, sensitivity to metabolic inhibitors, its nonuniform spatial distribution in illuminated cells, and gradual (1–5 min) inactivation of long-range signaling after transferring the cell to darkness. A stimulatory influence of the action potential on long-distance signal transmission is shown. The new method is suitable for studying the intercellular transport of metabolites and the permeability of plasmodesmata.

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

Fig. 1.
Fig. 2.
Fig. 3.

Similar content being viewed by others

REFERENCES

  1. M. Tominaga and K. Ito, Curr. Opin. Plant Biol. 27, 104 (2015).

    Google Scholar 

  2. T. Shimmen, J. Plant Res. 120, 31 (2007).

    Google Scholar 

  3. R. E. Goldstein and J.-W. van de Meent, Interface Focus 5, 20150030 (2015).

    Google Scholar 

  4. W. F. Pickard, Plant, Cell Environ. 26, 1 (2003).

    Google Scholar 

  5. K. J. Oparka and D. A. M. Prior, Plant J. 2 (5), 741 (1992).

    Google Scholar 

  6. E. B. Tucker and J. E. Tucker, Protoplasma 174, 36 (1993).

    Google Scholar 

  7. T. Nishiyama et al., Cell 174, 448 (2018).

    Google Scholar 

  8. V. Z. Lunevsky, O. M. Zherelova, I. Ya. Vostrikov, et al., J. Membr. Biol. 72 (1), 43 (1983).

    Google Scholar 

  9. G. N. Berestovsky and A. A. Kataev, Eur. Biophys. J. 34, 973 (2005).

    Google Scholar 

  10. W. J. Lucas and R. Nuccitelli, Planta 150, 120 (1980).

    Google Scholar 

  11. M. J. Beilby, T. Mimura, and T. Shimmen, Protoplasma 175, 144 (1993).

    Google Scholar 

  12. A. A. Bulychev, A. A. Cherkashin, A. B. Rubin, et al., Bioelectrochemistry 53, 225 (2001).

    Google Scholar 

  13. A. A. Bulychev, A. A. Polezhaev, S. V. Zykov, et al. J. Theor. Biol. 212, 275 (2001).

    Google Scholar 

  14. N. A. Krupenina, A. A. Bulychev, M. R. G. Roelfsema, et al., Photochem. Photobiol. Sci. 7, 681 (2008).

    Google Scholar 

  15. N. A. Krupenina, A. A. Bulychev, and U. Schreiber, Protoplasma 248, 513 (2011).

    Google Scholar 

  16. N. S. Allen and R. D. Allen, Ann. Rev. Biophys. Bioeng. 7, 497 (1978).

    Google Scholar 

  17. T. Shimmen and E. Yokota, Curr. Opin. Cell Biol. 16, 68 (2004).

    Google Scholar 

  18. T. McConnaughey, Limnol. Oceanogr. 36, 619 (1991).

    ADS  Google Scholar 

  19. D. Menzel, Protoplasma 144, 73 (1988).

    Google Scholar 

  20. I. Foissner and G. O. Wasteneys, J. Microsc. 247 (1), 10 (2012).

    Google Scholar 

  21. M. J. Beilby, Front. Plant Sci. 7, 1052 (2016).

    Google Scholar 

  22. N. Kamiya, Protoplasmic Streaming (Springer, Wien, 1959).

    Google Scholar 

  23. R. Scheibe, Plant Physiol. 96 (1), 1 (1991).

    ADS  Google Scholar 

  24. M. Taniguchi and H. Miyake, Curr. Opin. Plant Biol. 15, 252 (2012).

    Google Scholar 

  25. A. A. Bulychev, A. V. Alova, and A. B. Rubin, Eur. Biophys. J. 42, 441 (2013).

    Google Scholar 

  26. A. A. Bulychev and A. A. Rybina, Protoplasma 255 (6), 1621 (2018).

    Google Scholar 

  27. A. V. Komarova, V. S. Sukhov, and A. A. Bulychev, Funct. Plant Biol. 45 (1–2), 236 (2018).

  28. A. A. Bulychev and S. O. Dodonova, Russ. J. Plant Physiol. 58 (2), 233 (2011).

    Google Scholar 

  29. A. A. Bulychev and S. O. Dodonova, Biochim. Biophys. Acta 1807, 1221 (2011).

    Google Scholar 

  30. A. A. Bulychev and A. V. Komarova, Protoplasma 251 (6), 1481 (2014).

    Google Scholar 

  31. A. A. Bulychev, in Plant Electrophysiology: Methods and Cell Electrophysiology, Ed. by A. G. Volkov (Springer, Berlin, 2012), pp. 273–300.

    Google Scholar 

  32. A. A. Bulychev and A. V. Komarova, Biochemistry (Moscow) 79 (3), 273 (2014).

    Google Scholar 

  33. A. A. Bulychev, Long-distance Interactions and Signal Transmission in Chara Algae Cells: Timiryazev Memorial Lectures–76 (Nauka, Moscow, 2017) [in Russian].

    Google Scholar 

  34. S. O. Dodonova and A. A. Bulychev, Protoplasma 248, 737 (2011).

    Google Scholar 

  35. A. A. Bulychev and A. V. Komarova, Biochim. Biophys. Acta 1847, 379 (2015).

    Google Scholar 

  36. I. Foissner and G. O. Wasteneys, Plant Cell Physiol. 48 (4), 585 (2007).

    Google Scholar 

  37. A. A. Bulychev and I. Foissner, Plant Signal. Behav. 12 (9), e1362518 (2017).

    Google Scholar 

  38. A. A. Bulychev and A. V. Komarova, Protoplasma 254 (1), 557 (2017).

    Google Scholar 

  39. A. A. Bulychev, A. A. Rybina, and I. Foissner, in Chloroplasts and Cytoplasm: Structure and Functions, Ed. by C. Dejesus and L. Trask (Nova Science, New York, 2018), pp. 1–24.

    Google Scholar 

  40. A. A. Bulychev and N. A. Krupenina, Biochemistry (Moscow) Suppl. Ser. A: Membr. Cell Biol. 2 (4), 387 (2008).

    Google Scholar 

  41. C. H. Foyer and G. Noctor, Antioxid. Redox Signal. 11 (4), 861 (2009).

    Google Scholar 

  42. 42. A. A. Bulychev and A. V. Komarova, Biochim. Biophys. Acta 1858 (5), 386 (2017).

    Google Scholar 

  43. A. A. Bulychev and N. A. Krupenina, Bioelectrochemistry 129, 62 (2019).

    Google Scholar 

  44. Y. N. Antonenko and A. A. Bulychev, Biochim. Biophys. Acta 1070, 279 (1991).

    Google Scholar 

  45. J. A. Feijo, J. Saihas, J. R. Hackett, et al. J. Cell Biol. 144 (3), 483 (1999).

    Google Scholar 

  46. A. A. Bulychev and N. A. Kamzolkina, Bioelectrochemistry 69, 209 (2006).

    Google Scholar 

  47. A. A. Bulychev, N. A. Kamzolkina, J. Luengviriya, et al., J. Membr. Biol. 202 (1), 11 (2004).

    Google Scholar 

  48. A. A. Bulychev and N. A. Krupenina, Plant Signal. Behav. 4 (8), 24 (2009).

    Google Scholar 

  49. N. A. Krupenina and A. A. Bulychev, Biochim. Biophys. Acta 1767, 781 (2007).

    Google Scholar 

  50. A. A. Bulychev, Protoplasma 256 (3), 815 (2019).

    Google Scholar 

  51. V. Hernandez-Hernandez, M. Benitez, and A. Boudaoud, J. Exp. Bot. 71 (3), 768 (2020). https://doi.org/10.1093/jxb/erz434

    Article  Google Scholar 

Download references

Funding

This study was supported by the Russian Foundation for Basic Research (projects nos. 16-04-00318 and 20-54-12015).

Author information

Authors and Affiliations

  1. Department of Biology, Moscow State University, 119991, Moscow, Russia

    A. A. Bulychev, A. V. Alova, N. A. Krupenina & A. B. Rubin

Authors
  1. A. A. Bulychev
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. A. V. Alova
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. N. A. Krupenina
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. A. B. Rubin
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to A. A. Bulychev.

Ethics declarations

This article does not contain any studies with human participants or animals performed by any of the authors.

Conflict of Interest. The authors declare that they have no conflicts of interest.

Additional information

Translated by A. Bulychev

Abbreviations: QA, primary quinone acceptor of photosystem II, PSII, photosystem II, PSI, photosystem I.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Bulychev, A.A., Alova, A.V., Krupenina, N.A. et al. Cytoplasmic Streaming as an Intracellular Conveyer: Effect on Photosynthesis and H+ Fluxes in Chara Cells. BIOPHYSICS 65, 250–258 (2020). https://doi.org/10.1134/S0006350920020037

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1134/S0006350920020037

Keywords:

Search

Navigation