Register      Login
Functional Plant Biology Functional Plant Biology Society
Plant function and evolutionary biology
RESEARCH ARTICLE

Cyclosis-mediated long distance communications of chloroplasts in giant cells of Characeae

Anna V. Komarova A B C , Vladimir S. Sukhov B and Alexander A. Bulychev A
+ Author Affiliations
- Author Affiliations

A Department of Biophysics, Faculty of Biology, Lomonosov Moscow State University, 119992 Moscow, Russia.

B Department of Biophysics, Lobachevsky State University of Nizhny Novgorod, Gagarin Avenue 23, 603950 Nizhny Novgorod, Russia.

C Corresponding author. Email: ava1945@mail.ru

This paper originates from a presentation at the Fourth International Symposium on Plant Signaling and Behavior, Komarov Botanical Institute RAS/Russian Science Foundation, Saint Petersburg, Russia, 1923 June 2016.

Functional Plant Biology 45(2) 236-246 https://doi.org/10.1071/FP16283
Submitted: 8 August 2016  Accepted: 21 February 2017   Published: 24 March 2017

Abstract

Long-distance communications in giant characean internodal cells involve cytoplasmic streaming as an effective means for transportation of regulatory substances. The local illumination of Chara corallina Klein ex C.L.Willdenow internodal cells with an intense 30 s pulse of white light caused a transient increase of modulated chlorophyll fluorescence in cell regions positioned downstream the cytoplasmic flow after a delay whose duration increased with the axial distance from the light source. No changes in fluorescence were observed in cell regions residing upstream of the light spot. The transient increase in actual fluorescence Fʹ in cell areas exposed to constant dim illumination at large distances from the brightly lit area indicates the transmission of photosynthetically active metabolite between chloroplasts separated by 1–5 mm distances. The shapes of fluorescence transients were sensitive to retardation of cytoplasmic streaming by cytochalasin D and to variations in cyclosis velocity during gradual recovery of streaming after an instant arrest of cyclosis by elicitation of the action potential. Furthermore, the analysed fluorescence transients were skewed on the ascending or descending fronts depending on the position of light-modulated cytoplasmic package at the moment of streaming cessation with respect to the point of measurements. The observations are simulated in qualitative terms with a simplified streaming–diffusion model.

Additional keywords: advection, Chara corallina, cytoplasmic streaming, diffusion, modulated chlorophyll microfluorometry, plasma membrane excitation.


References

Bulychev AA (2012) Membrane excitation and cytoplasmic streaming as modulators of photosynthesis and proton flows in Characean cells. In ‘Plant electrophysiology: methods and cell electrophysiology.’ (Ed. AG Volkov) pp. 273–300. (Springer: Berlin)

Bulychev AA, Dodonova SO (2011) Effects of cyclosis on chloroplast–cytoplasm interactions revealed with localized lighting in Characean cells at rest and after electrical excitation. Biochimica et Biophysica Acta 1807, 1221–1230.
Effects of cyclosis on chloroplast–cytoplasm interactions revealed with localized lighting in Characean cells at rest and after electrical excitation.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXptV2jsrs%3D&md5=71dbd8bd419ac537e5feffc94db06d72CAS |

Bulychev AA, Komarova AV (2015) Photoinduction of cyclosis-mediated interactions between distant chloroplasts. Biochimica et Biophysica Acta 1847, 379–389.
Photoinduction of cyclosis-mediated interactions between distant chloroplasts.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2MXhtlWgs7Y%3D&md5=4e62cc6efeb9f6929f5603411b0879fcCAS |

Bulychev AA, Komarova AV (2017) Implication of long-distance cytoplasmic transport into dynamics of local pH on the surface of microinjured Chara cells. Protoplasma 254, 557–567.
Implication of long-distance cytoplasmic transport into dynamics of local pH on the surface of microinjured Chara cells.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC28Xms12ktL8%3D&md5=4f566cacc4f3b77774312f76febbc7a5CAS |

Bulychev AA, Alova AV, Rubin AB (2013) Propagation of photoinduced signals with the cytoplasmic flow along Characean internodes: evidence from changes in chloroplast fluorescence and surface pH. European Biophysics Journal 42, 441–453.
Propagation of photoinduced signals with the cytoplasmic flow along Characean internodes: evidence from changes in chloroplast fluorescence and surface pH.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXnvFyrtrs%3D&md5=0a4e23b1a78ed41107e547d09a37182fCAS |

Carrillo N, Lucero HA, Vallejos RH (1981) Light modulation of chloroplast membrane-bound ferredoxin-NADP+ oxidoreductase. Journal of Biological Chemistry 256, 1058–1059.

Corneille S, Cournac L, Guedeney G, Havaux M, Peltier G (1998) Reduction of the plastoquinone pool by exogenous NADH and NADPH in higher plant chloroplasts: characterization of a NAD(P)H–plastoquinone oxidoreductase activity. Biochimica et Biophysica Acta (BBA) – Bioenergetics 1363, 59–69.
Reduction of the plastoquinone pool by exogenous NADH and NADPH in higher plant chloroplasts: characterization of a NAD(P)H–plastoquinone oxidoreductase activity.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1cXhtlOjs7Y%3D&md5=e82726dd5803fa18108445d11e88fd9bCAS |

Dodonova SO, Bulychev AA (2011) Cyclosis-related asymmetry of chloroplast–plasma membrane interactions at the margins of illuminated area in Chara corallina cells. Protoplasma 248, 737–749.
Cyclosis-related asymmetry of chloroplast–plasma membrane interactions at the margins of illuminated area in Chara corallina cells.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXhsVaht73J&md5=604070152900a78bff3e77669756be2eCAS |

Endo T, Mi H, Shikanai T, Asada K (1997) Donation of electrons to plastoquinone by NAD(P)H dehydrogenase and by ferredoxin-quinone reductase in spinach chloroplasts. Plant & Cell Physiology 38, 1272–1277.
Donation of electrons to plastoquinone by NAD(P)H dehydrogenase and by ferredoxin-quinone reductase in spinach chloroplasts.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2sXnsFWqsbk%3D&md5=febacd227c93e8d54719cef7a39b4badCAS |

Eremin A, Bulychev AA, Hauser MJB (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.
Cyclosis-mediated transfer of H2O2 elicited by localized illumination of Chara cells and its relevance to the formation of pH bands.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXhvVehsLbE&md5=bcde16ea70abd69e9520246315f3257aCAS |

Flügge U-I, Heldt HW (1991) Metabolite translocators of the chloroplast envelope. Annual Review of Plant Physiology and Plant Molecular Biology 42, 129–144.
Metabolite translocators of the chloroplast envelope.Crossref | GoogleScholarGoogle Scholar |

Foissner I, Wasteneys GO (2012) The characean internodal cell as a model system for studying wound healing. Journal of Microscopy 247, 10–22.
The characean internodal cell as a model system for studying wound healing.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38XhtlWgsLjJ&md5=0e21e1d089d0bd5755167ec540e7ef01CAS |

Foyer CH, Noctor G (2009) Redox regulation in photosynthetic organisms: signaling, acclimation, and practical implications. Antioxidants & Redox Signalling 11, 861–905.
Redox regulation in photosynthetic organisms: signaling, acclimation, and practical implications.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXitlWhsr0%3D&md5=edff1e61eb09d385c483b1131a201038CAS |

Goldstein RE, van de Meent J-W (2015) A physical perspective on cytoplasmic streaming. Interface Focus 5, 20150030
A physical perspective on cytoplasmic streaming.Crossref | GoogleScholarGoogle Scholar |

Hauser M, Eichelmann H, Oja V, Heber U, Laisk A (1995) Stimulation by light of rapid pH regulation in the chloroplast stroma in vivo as indicated by CO2 solubilization in leaves. Plant Physiology 108, 1059–1066.
Stimulation by light of rapid pH regulation in the chloroplast stroma in vivo as indicated by CO2 solubilization in leaves.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2MXmvFGmtb4%3D&md5=f3d8c3dd1b91f3bb24420c712554ac85CAS |

Hochachka PW (1999) The metabolic implications of intracellular circulation. Proceedings of the National Academy of Sciences of the United States of America 96, 12233–12239.
The metabolic implications of intracellular circulation.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1MXnt1yrtrs%3D&md5=adab134f91d7d49f51e22ae1a90c9d1fCAS |

Kalwarczyk T, Tabaka M, Holyst R (2012) Biologistics – diffusion coefficients for complete proteome of Escherichia coli. Bioinformatics 28, 2971–2978.
Biologistics – diffusion coefficients for complete proteome of Escherichia coli.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38Xhs1Glt7fK&md5=5a54fcd96f077ac308587d10e49d0e17CAS |

Kamiya N (1959) ‘ Protoplasmic streaming.’ (Springer: Wien, Germany)

Kamiya N (1981) Physical and chemical basis of cytoplasmic streaming. Annual Review of Plant Physiology 32, 205–236.
Physical and chemical basis of cytoplasmic streaming.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL3MXkt1WhsL0%3D&md5=abdd94fdcc2adb2a663d688d531b4aadCAS |

Mano J, Miyake C, Schreiber U, Asada K (1995) Photoactivation of the electron flow from NADPH to plastoquinone in spinach chloroplasts. Plant & Cell Physiology 36, 1589–1598.

Montroll E, Shlesinger M (1984) On the wonderful world of random walks. In ‘Nonequilibrium phenomena II: from stochastics to hydrodynamics. Studies in statistical mechanics. Vol. XI’. (Eds J Lebowitz, E Montroll) pp. 1–121. (Elsevier: Amsterdam)

Nothnagel EA, Webb WW (1982) Hydrodynamic models of viscous coupling between motile myosin and endoplams in characean algae. Journal of Cell Biology 94, 444–454.
Hydrodynamic models of viscous coupling between motile myosin and endoplams in characean algae.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DyaL383msF2htA%3D%3D&md5=c83fc083fe9c1bcac9f86c284ff656b9CAS |

Pearcy RW, Krall JP, Sassenrath-Cole GF (1996) Photosynthesis in fluctuating light environments. In ‘Photosynthesis and the environment’. (Ed. NR Baker) pp. 321–346. (Kluwer: Dordrecht, The Netherlands)

Pickard WF (2003) The role of cytoplasmic streaming in symplastic transport. Plant, Cell & Environment 26, 1–15.
The role of cytoplasmic streaming in symplastic transport.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXhtlKrtLo%3D&md5=4939c31997533749353ca890cd4dc57dCAS |

Raghavendra AS, Padmasree K (2003) Beneficial interactions of mitochondrial metabolism with photosynthetic carbon assimilation. Trends in Plant Science 8, 546–553.
Beneficial interactions of mitochondrial metabolism with photosynthetic carbon assimilation.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXos1CnsrY%3D&md5=1f3f36483cc7ac6f23f3d1c09dca6b01CAS |

Ruban AV (2016) Nonphotochemical chlorophyll fluorescence quenching: mechanism and effectiveness in protecting plants from photodamage. Plant Physiology 170, 1903–1916.
Nonphotochemical chlorophyll fluorescence quenching: mechanism and effectiveness in protecting plants from photodamage.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC28XhsVOgsrbI&md5=2f25490c93873c6edf499d0020846d99CAS |

Sassenrath-Cole GF, Pearcy RW (1994) Regulation of photosynthetic induction state by the magnitude and duration of low light exposure. Plant Physiology 105, 1115–1123.
Regulation of photosynthetic induction state by the magnitude and duration of low light exposure.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2cXlsFemtLg%3D&md5=19bb00da94b9c91b7bda75c227327102CAS |

Scheibe R (1991) Redox-modulation of chloroplast enzymes. Plant Physiology 96, 1–3.
Redox-modulation of chloroplast enzymes.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK3MXkt1Gqt7g%3D&md5=8d40a01c8a62e9775e34bf8707b98758CAS |

Shimmen T (2007) The sliding theory of cytoplasmic streaming: fifty years of progress. Journal of Plant Research 120, 31–43.
The sliding theory of cytoplasmic streaming: fifty years of progress.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXhs1Ckurw%3D&md5=c698daf9475d6cafdec0eaaa0ca876f4CAS |

Shimmen T, Yokota E (2004) Cytoplasmic streaming in plants. Current Opinion in Cell Biology 16, 68–72.
Cytoplasmic streaming in plants.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXitlSms7s%3D&md5=8d6313090f6a4486751b75096ce2b1a9CAS |

Stael S, Wurzinger B, Mair A, Mehlmer N, Vothknecht UC, Teige M (2012) Plant organellar calcium signalling: an emerging field. Journal of Experimental Botany 63, 1525–1542.
Plant organellar calcium signalling: an emerging field.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38XjtlKhsb0%3D&md5=16cff8b129b95613f5a9ee9ce5066b8cCAS |

Taniguchi M, Miyake H (2012) Redox-shuttling between chloroplast and cytosol: integration of intra-chloroplast and extra-chloroplast metabolism. Current Opinion in Plant Biology 15, 252–260.
Redox-shuttling between chloroplast and cytosol: integration of intra-chloroplast and extra-chloroplast metabolism.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38Xnsl2rsrs%3D&md5=d3723850acaa95d32856890d399f1a88CAS |

Tazawa M (2003) Cell physiological aspects of the plasma membrane electrogenic H+ pump. Journal of Plant Research 116, 419–442.
Cell physiological aspects of the plasma membrane electrogenic H+ pump.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXptFahsrY%3D&md5=41a72aea79eea01f5db051d4ca55d12cCAS |

Tazawa M, Kishimoto U (1968) Cessation of cytoplasmic streaming of Chara internodes during action potential. Plant & Cell Physiology 9, 361–368.

Tsuchiya Y, Yamazaki H, Aoki T (1991) Steady and transient behaviors of protoplasmic streaming in Nitella internodal cell. Biophysical Journal 59, 249–251.
Steady and transient behaviors of protoplasmic streaming in Nitella internodal cell.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BC3croslCltg%3D%3D&md5=71f071a5ed4df31eb2c412eacfdca346CAS |

van de Meent J-W, Tuval I, Goldstein RE (2008) Nature’s microfluidic transporter: rotational cytoplasmic streaming at high Peclet numbers. Physical Review Letters 101, 178102
Nature’s microfluidic transporter: rotational cytoplasmic streaming at high Peclet numbers.Crossref | GoogleScholarGoogle Scholar |

Vodeneev V, Orlova A, Morozova E, Orlova L, Akinchits E, Orlova O, Sukhov V (2012) The mechanism of propagation of variation potentials in wheat leaves. Journal of Plant Physiology 169, 949–954.
The mechanism of propagation of variation potentials in wheat leaves.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38XlvFynt7g%3D&md5=2e55f9d627159a124661c33b7479ee87CAS |

Williamson RE, Ashley CC (1982) Free Ca2+ and cytoplasmic streaming in the alga Chara. Nature 296, 647–651.
Free Ca2+ and cytoplasmic streaming in the alga Chara.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL38XktlKgsbo%3D&md5=9dec749d72e829ce4be2e8fe44297589CAS |

Wolff K, Marenduzzo D, Cates ME (2012) Cytoplasmic streaming in plant cells: the role of wall slip. Journal of the Royal Society, Interface 9, 1398–1408.
Cytoplasmic streaming in plant cells: the role of wall slip.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BC38vjtFCltw%3D%3D&md5=f61f8bf472c522050c72a39ab6de3cdaCAS |