Protoplasma

, Volume 251, Issue 6, pp 1481–1490 | Cite as

Proton flows across the plasma membrane in microperforated characean internodes: tonoplast injury and involvement of cytoplasmic streaming

Original Article

Abstract

Microperforation of characean cell wall with a glass micropipette in the absence of the tonoplast impalement was found to cause rapid alkalinization of the apoplast by 2–3 pH units, which may rigidify the cell wall structure, thus protecting the cell from further injury. A similar but a deeper insertion of a microneedle, associated with piercing the tonoplast and with an action potential generation, led to a considerable delay in the apoplast alkalinization without affecting the amplitude of the eventual increase in pH. The retardation by the mechanically elicited action potential of the incision-mediated pH transients in the apoplast contrasted sharply to the enhancement of these pH transients by the action potential triggered electrically before the microperforation. Hence, the delay of the apoplast alkalinization was not related to basic ionic mechanisms of plant action potentials. Measurements of the vacuolar pH after mechanical elicitation of an action potential indicate that the tonoplast piercing was accompanied by leakage of protons from the vacuole into the cytoplasm, which may strongly acidify the cytoplasm around the wounded area, thus collapsing the driving force for H+ influx from the medium into the cytoplasm. The lag period preceding the onset of external alkalinization was found linearly related to the duration of temporal cessation of cytoplasmic streaming. The results suggest that the delayed alkalinization of the apoplast in the region of tonoplast wounding reflects the localized recovery of the proton motive force across the plasmalemma during replacement of the acidic cytoplasm with fresh portions of unimpaired cytoplasm upon restoration of cytoplasmic streaming.

Keywords

Chara corallina Cyclosis Cytoplasmic acidification Cell wounding Action potential Proton flows 

References

  1. Allen NS, Allen RD (1978) Cytoplasmic streaming in green plants. Annu Rev Biophys Bioenerg 7:497–526CrossRefGoogle Scholar
  2. Andrianov VK, Bulychev AA, Kurella GA, Litvin FF (1971) Effect of light on resting potential and cation (K+, H+, Na+) activity in the vacuolar sap of Nitella cells. Biofizika 16:1031–1036Google Scholar
  3. Beilby MJ, Bisson MA (2012) pH banding in charophyte algae. In: Volkov AG (ed) Plant electrophysiology: methods and cell electrophysiology. Springer, Berlin, pp 247–271CrossRefGoogle Scholar
  4. Berestovsky GN, Kataev AA (2005) Voltage-gated calcium and Ca2+-activated chloride channels and Ca2+ transients: voltage-clamp studies of perfused and intact cells of Chara. Eur Biophys J 34:973–986Google Scholar
  5. Berestovsky GN, Ternovsky VI, Kataev AA (2001) Through pore diameter in the cell wall of Chara corallina. J Exp Bot 52:1173–1177Google Scholar
  6. Bisson MA, Walker NA (1981) The hyperpolarization of the Chara membrane at high pH: effects of external potassium, internal pH, and DCCD. J Exp Bot 32:951–971Google Scholar
  7. Bobrov VA, Vostrikov IY, Kurella GA, Yaglova LG (1973) Photoinduced changes of electric potential difference across the tonoplast and plasmalemma as a criterion for localization of the microelectrode tip. Tsitologiya 15:1165–1168Google Scholar
  8. Bolwell GP, Bindschedler LV, Blee KA, Butt VS, Davies DR, G SL, Gerrish C, Minibaeva F (2002) The apoplastic oxidative burst in response to biotic stress in plants: a three-component system. J Exp Bot 53:1367–1376PubMedCrossRefGoogle Scholar
  9. Bulychev AA, Komarova AV (2014) Long-distance signal transmission and regulation of photosynthesis in characean cells. Biochemistry (Mosc) 79:273–281CrossRefGoogle Scholar
  10. Bulychev AA, Alova AV, Bibikova TN (2013a) Strong alkalinization of Chara cell surface in the area of cell wall incision as an early event in mechanoperception. Biochim Biophys Acta 1828:2359–2369Google Scholar
  11. Bulychev AA, Alova AV, Rubin AB (2013b) Fluorescence transients in chloroplasts of Chara corallina cells during transmission of photoinduced signal with the streaming cytoplasm. Russ J Plant Physiol 60:33–40Google Scholar
  12. Bulychev AA, Alova AV, Rubin AB (2013c) Propagation of photoinduced signals with the cytoplasmic flow along Characean internodes: evidence from changes in chloroplast fluorescence and surface pH. Eur Biophys J 42:441–453PubMedCrossRefGoogle Scholar
  13. Cosgrove DJ (1998) Molecular regulation of plant cell wall extensibility. Gravit Space Biol Bull 11:61–70PubMedGoogle Scholar
  14. Dodonova SO, Krupenina NA, Bulychev AA (2010) Suppression of the plasma membrane H+-conductance on the background of high H+-pump activity in dithiothreitol-treated Chara cells. Biochemistry (Mosc) Suppl Series A: Membr Cell Biol 4:389–396Google Scholar
  15. Feijó JA, Sainhas J, Hackett GR, Kunkel JG, Hepler PK (1999) Growing pollen tubes possess a constitutive alkaline band in the clear zone and a growth-dependent acidic tip. J Cell Biol 144:483–496PubMedCrossRefPubMedCentralGoogle Scholar
  16. Fleischer A, O’Neil MA, Ehwald R (1999) The pore size of non-graminaceous plant cell walls is rapidly decreased by borate ester cross-linking of the pectic polysaccharide rhamnogalacturonan II. Plant Physiol 121:829–838PubMedCrossRefPubMedCentralGoogle Scholar
  17. Foissner I (1988) The relationship of echinate inclusions and coated vesicles on wound healing in Nitella flexilis (Characeae). Protoplasma 142:164–175Google Scholar
  18. Foissner I, Wasteneys GO (2012) The characean internodal cell as a model system for studying wound healing. J Microsc 247:10–22PubMedCrossRefPubMedCentralGoogle Scholar
  19. Gyenes M, Saxena R, Kurella GA (1981) H+ transport across the plasmalemma and tonoplast of Nitellopsis obtusa during excitation. J Exp Bot 32:973–977Google Scholar
  20. Hardham AR, Jones DA, D. T (2007) Cytoskeleton and cell wall function in penetration resistance. Curr Opin Plant Biol 10:342–348PubMedCrossRefGoogle Scholar
  21. Hepler PK (2005) Calcium: a central regulator of plant growth and development. Plant Cell 17:2142–2155PubMedCrossRefPubMedCentralGoogle Scholar
  22. Iwabuchi K, Kaneko T, Kikuyama M (2008) Mechanosensitive ion channels in Chara: Influence of water channel inhibitors, HgCl2 and ZnCl2, on generation of receptor potential. J Membr Biol 221:27–37Google Scholar
  23. Kaneko T, Takahashi N, Kikuyama M (2009) Membrane stretching triggers mechanosensitive Ca2+ channel activation in Chara. J Membr Biol 228:33–42Google Scholar
  24. Kobayashi Y, Kobayashi I (2013) Microwounding is a pivotal factor for the induction of actin-dependent penetration resistance against fungal attack. Planta 237:1187–1198PubMedCrossRefGoogle Scholar
  25. Menzel D (1988) How do giant plant cells cope with injury?—The wound response in siphonous green algae. Protoplasma 144:73–91CrossRefGoogle Scholar
  26. Metraux JP, Richmond PA, Taiz L (1980) Control of cell elongation in Nitella by endogeneous cell wall pH gradients. Multiaxial extensibility and growth studies. Plant Physiol 65:204–210Google Scholar
  27. Monshausen GB, Bibikova TN, Weisenseel MH, Gilroy S (2009) Ca2+ regulates reactive oxygen species production and pH during mechanosensing in arabidopsis roots. Plant Cell 21:2341–2356PubMedCrossRefPubMedCentralGoogle Scholar
  28. Shepherd VA, Beilby MJ, Shimmen T (2002) Mechanosensory ion channels in charophyte cells: the response to touch and salinity stress. Eur Biophys J 31:341–355PubMedCrossRefGoogle Scholar
  29. Shepherd VA, Beilby MJ, Al Khazaali SAS, Shimmen T (2008) Mechano-perception in Chara cells: the influence of salinity and calcium on touch-activated receptor potentials, action potentials and ion transport. Plant Cell Environ 31:1575–1591Google Scholar
  30. Shimmen T, Nishikawa S (1988) Studies on the tonoplast action potential of Nitella flexilis. J Membr Biol 101:133–140Google Scholar
  31. Shimmen T, Yamamoto A (2002) Induction of a new alkaline band at a target position in internodal cells of Chara corallina. Plant Cell Physiol 43:980–983Google Scholar
  32. Skobeleva OV, Ktitorova IN, Lyalin OO (1996) Cell burst as a mechanism of plant cell injury. Russ J Plant Physiol 43:439–447Google Scholar
  33. Takeshige K, Tazawa M (1989) Measurement of the cytoplasmic and vacuolar buffer capacities in Chara corallina. Plant Physiol 89:1049–1052Google Scholar
  34. Tsuchiya Y, Yamazaki H, Aoki T (1991) Steady and transient behaviors of protoplasmic streaming in Nitella internodal cell. Biophys J 59:249–251Google Scholar
  35. Wijesinghe D, Arachchige MCM, Lu A, Reshetnyak YK, Andreev OA (2013) pH dependent transfer of nano-pores into membrane of cancer cells to induce apoptosis. Sci Rep 3:3560. doi:10.1038/srep03560 PubMedCrossRefPubMedCentralGoogle Scholar
  36. Williamson RE, Ashley CC (1982) Free Ca2+ and cytoplasmic streaming in the alga Chara. Nature 296:647–651Google Scholar

Copyright information

© Springer-Verlag Wien 2014

Authors and Affiliations

  1. 1.Faculty of BiologyLomonosov Moscow State UniversityMoscowRussia

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