Abstract
In Chara corallina cells exposed to continuous light, external pH (pHo) and photosystem II (PSII) photochemical yield show correlated banding patterns. Photosynthetic activity is low in cell regions producing alkaline zones and high in the acid regions. We addressed the question whether (and how) photosynthetic activity and plasma membrane (PM) H+-pumping and H+-conductance are coupled in the different bands. First, PM H+-pump activity was stimulated with fusicoccin. This resulted in a more acidic pH in the acid bands without disturbing the correlation of photosynthetic electron transport and H+ fluxes across the PM. Next, H+-pump activity was reduced through microinjection of a phosphorylated peptide matching the canonical 14-3-3 binding motif RSTpSTP in the acid cell region. Microinjection induced a rapid (~5 min) rise in pHo by ca. 1.0 unit near the injection site, whereas the injection of the non-phosphorylated peptide had no effect. This pH rise confirms the supposed inhibition of the H+-pump upon the detachment of 14-3-3 proteins from the H+-ATPase. However, the PSII yield in the cell regions corresponding to the new alkaline peak remained high, which violated the normal inverse relations between the pHo and PSII photochemical yield. We conclude that the injection of the competitive inhibitor of the H+ATPase disrupts the balanced operation of PM H+-transport and photosynthetic electron flow and promotes electron flow through alternative pathways.
Similar content being viewed by others
Abbreviations
- NR:
-
nitrate reductase
- NR-C:
-
non-phosphorylated peptide matching the 14-3-3 interaction domain in barley nitrate reductase
- NR-P:
-
a similar peptide containing phosphorylated serine
- pHo :
-
external pH near the cell surface
- PM:
-
plasma membrane
- PSII:
-
photosystem II
- ΔF/F ’m :
-
effective quantum yield of PS II photochemistry
REFERENCES
Tominaga, M., Kinoshita, T., and Shimazaki, K. (2001) Plant Cell Physiol., 42, 795–802.
Goh, C.-H., Dietrich, P., Steinmeyer, R., Schreiber, U., Nam, H.-G., and Hedrich, R. (2002) Plant J., 32, 623–630.
Serrano, E. E., Zeiger, E., and Hagiwara, S. (1988) Proc. Natl. Acad. Sci. USA, 85, 436–440.
Vanselow, K. H., and Hansen, U.-P. (1989) J. Membr. Biol., 110, 175–187.
Bulychev, A. A., and Vredenberg, W. J. (1995) Physiol. Plant., 94, 64–70.
Plieth, C., Sattelmacher, B., and Hansen, U.-P. (1998) Planta, 207, 52–59.
Plieth, C., Tabrizi, H., and Hansen, U.-P. (1994) Physiol. Plant., 91, 205–211.
Van Ginkel, L. C., and Prins, H. B.A. (1998) Can. J. Bot., 76, 1018–1024.
Baker, N. R., Oxborough, R., Lawson, T., and Morison, J. I. L. (2001) J. Exp. Bot., 52, 615–621.
Lucas, W. J., and Nuccitelli, R. (1980) Planta, 150, 120–131.
Fisahn, J. M., and Lucas, W. J. (1995) J. Membr. Biol., 147, 275–281.
Bulychev, A. A., Polezhaev, A. A., Zykov, S. V., Pljusnina, T. Yu., Riznichenko, G. Yu., Rubin, A. B., Jantoss, W., Zykov, V. S., and Mull er, S. C. (2001) J. Theor. Biol., 212, 275–294.
Bulychev, A. A., Cherkashin, A. A., Rubin, A. B., Vredenberg, W. J., Zykov, V. S., and Muller, S. C. (2001) Bioelectrochemistry, 53, 225–232.
Bulychev, A. A., and Vredenberg, W. J. (2003) Planta, 218, 143–151.
Hansen, U.-P., Moldaenke, C., Tabrizi, H., and Ramm, D. (1993) Plant Cell Physiol., 34, 681–695.
Smith, P. J. S., and Walker, N. A. (1985) J. Membr. Biol., 83, 193–205.
Yao, X., and Bisson, M. A. (1993) Plant Physiol., 103, 197–203.
Baunsgaard, L., Fuglsang, A. T., Jahn, T., Korthout, H., De Boer, A. H., and Palmgren, M. G. (1998) Plant J., 13, 661–671.
Kerkeb, L., Venema, K., Donaire, J. P., and Rodriguez-Rosales, M. P. (2002) Physiol. Plant., 116, 37–41.
Sehnke, P. C., DeLille, J. M., and Ferl, R. J. (2002) Plant Cell, 14, S339-S354.
Bunney, T. D., van den Wijngaard, P. W. J., and De Boer, A. H. (2002) Plant Mol. Biol., 50, 1041–1051.
Tzivion, G., and Avruch, J. (2002) J. Biol. Chem., 277, 3061–3064s.
Fuglsang, A. T., Visconti, S., Drumm, K., Jahn, T., Stensballe, A., Mattei, B., Jensen, O. N., Aducci, P., and Palmgren, M. G. (1999) J. Biol. Chem., 274, 36774–36780.
Kinoshita, T., and Shimazaki, K. (1999) EMBO J., 18, 5548–5558.
Kinoshita, T., and Shimazaki, K. (2001) Plant Cell Physiol., 42, 424–432.
Moorhead, G., Douglas, P., Cotelle, V., Harthill, J., Morrice, N., Meek, S., Deiting, U., Stitt, M., Scarabel, M., Aitken, A., and MacKintosh, C. (1999) Plant J., 18, 1–12.
Ichimura, T., Wakamiya-Tsuruta, A., Itagaki, C., Taoka, M., Hayano, T., Natsume, T., and Isobe, T. (2002) Biochemistry, 41, 5566–5572.
Bunney, T. D., van Walraven, H. S., and De Boer, A. H. (2001) Proc. Natl. Acad. Sci. USA, 98, 4249–4254.
Booij, P. P., Roberts, M. R., Vogelzang, S. A., Kraayenhof, R., and De Boer, A. H. (1999) Plant J., 20, 673–683.
Goh, C.-H., Schreiber, U., and Hedrich, R. (1999) Plant Cell Environ., 22, 1057–1070.
Shimmen, T., and Yamamoto, A. (2002) Plant Cell Physiol., 43, 980–983.
De Boer, A. H. (1997) Trends Plant Sci., 2, 60–66.
Rajan, S., Preisig-Muller, R., Wischmeyer, E., Nehring, R., Hanley, P. J., Renigunta, V., Musset, B., Schlichthorl, G., Derst, C., Karschin, A., and Daut, J. (2002) J. Physiol., 545, 13–26.
MacKintosh, C., Douglas, P., and Lillo, C. (1995) Plant Physiol., 107, 1–457
Huber, S. C., MacKintosh, C., and Kaiser, W. M. (2002) Plant Mol. Biol., 50, 53–1063
Author information
Authors and Affiliations
Corresponding author
Additional information
Translated from Biokhimiya, Vol. 70, No. 1, 2005, pp. 68–76. Original Russian Text Copyright © 2005 by Bulychev, van den Wijngaard, de Boer. Originally published in Biochemistry (Moscow) On-Line Papers in Press, as Manuscript BM04-068, October 31, 2004.
Rights and permissions
About this article
Cite this article
Bulychev, A.A., van den Wijngaard, P.W.J. & de Boer, A.H. Spatial Coordination of Chloroplast and Plasma Membrane Activities in Chara Cells and Its Disruption through Inactivation of 14-3-3 Proteins. Biochemistry (Moscow) 70, 55–61 (2005). https://doi.org/10.1007/PL00021756
Received:
Revised:
Issue Date:
DOI: https://doi.org/10.1007/PL00021756