Light-induced changes in hydrogen, calcium, potassium, and chloride ion fluxes and concentrations from the mesophyll and epidermal tissues of bean leaves. Understanding the ionic basis of light-induced bioelectrogenesis

Noninvasive, ion-selective vibrating microelectrodes were used to measure the kinetics of H+, Ca2+, K+, and Cl- fluxes and the changes in their concentrations caused by illumination near the mesophyll and attached epidermis of bean (Vicia faba L.). These flux measurements were related to light-induced changes in the plasma membrane potential. The influx of Ca2+ was the main depolarizing agent in electrical responses to light in the mesophyll. Changes in the net fluxes of H+, K+, and Cl- occurred only after a significant delay of about 2 min, whereas light-stimulated influx of Ca2+ began within the time resolution of our measurements (5 s). In the absence of H+ flux, light caused an initial quick rise of external pH near the mesophyll and epidermal tissues. In the mesophyll this fast alkalinization was followed by slower, oscillatory pH changes (5-15 min); in the epidermis the external pH increased steadily and reached a plateau 3 min later. We explain the initial alkalinization of the medium as a result of CO2 uptake by photosynthesizing tissue, whereas activation of the plasma membrane H+ pump occurred 1.5 to 2 min later. The epidermal layer seems to be a substantial barrier for ion fluxes but not for CO2 diffusion into the leaf.

[1]  M. Tazawa,et al.  Effect of intracellular pH on the light-induced potential change and electrogenic activity in tonoplast-free cells of Chora australis , 1979 .

[2]  E. Van Volkenburgh,et al.  Characterization and effect of light on the plasma membrane H(+) -ATPase of bean leaves. , 1990, Plant physiology.

[3]  S. Takagi,et al.  Light-affected ca fluxes in protoplasts from vallisneria mesophyll cells. , 1988, Plant physiology.

[4]  M. Blom-Zandstra,et al.  Transient light-induced changes in ion channel and proton pump activities in the plasma membrane of tobacco mesophyll protoplasts , 1997 .

[5]  D. Ramm,et al.  The Effect of Transthylakoid Proton Uptake on Cytosolic pH and the Imbalance of ATP and NAPDH/H+ Production as Measured by CO2- and Light-Induced Depolarisation of the Plasmalemma , 1993 .

[6]  I. Newman,et al.  Proton and calcium flux oscillations in the elongation region correlate with root nutation. , 1997, Physiologia plantarum.

[7]  R. M. Spanswick,et al.  ELECTROGENIC ION PUMPS , 1981 .

[8]  H. Felle,et al.  The H+/Cl- Symporter in Root-Hair Cells of Sinapis alba (An Electrophysiological Study Using Ion-Selective Microelectrodes) , 1994, Plant physiology.

[9]  M. Tazawa,et al.  Light-induced changes in membrane potential in Spirogyra , 1978 .

[10]  N. Higinbotham,et al.  Membrane potentials of vallisneria leaf cells and their relation to photosynthesis. , 1980, Plant physiology.

[11]  S. Shabala,et al.  Protoplast ion fluxes: their measurement and variation with time, position and osmoticum , 1998, Planta.

[12]  J. Raven.  CO2-concentrating mechanisms: a direct role for thylakoid lumen acidification? , 1997 .

[13]  R. Levine,et al.  Reversible pH Changes in Cells of Chlamydomonas reinhardi Resulting from CO(2) Fixation in the Light and Its Evolution in the Dark. , 1971, Plant physiology.

[14]  M. Tazawa,et al.  Action Spectrum of Light-Induced Membrane Hyperpolarization in Egeria densa , 1986 .

[15]  E. Johannes,et al.  Red light-induced membrane potential transients in the moss Physcomitrella patens: ion channel interaction in phytochrome signalling. , 1997, Journal of experimental botany.

[16]  W. Vredenberg,et al.  On the steady-state electrical potential difference across the thylakoid membranes of chloroplasts in illuminated plant cells. , 1975, Biochimica et biophysica acta.

[17]  A. Moroni,et al.  Light-induced Activation of Electrogenic H+ Extrusion and K+ Uptake in Elodea densa Depends on Photosynthesis and is Mediated by the Plasma membrane H+ ATPase , 1989 .

[18]  C. Atkins,et al.  Light-induced pH changes by cells of Chlamydomonas reinhardii. Dependence on CO2 uptake. , 1971, Biochimica et biophysica acta.

[19]  Noel Keenlyside,et al.  Proton flux measurements from tissues in buffered solution , 1995 .

[20]  S. Shabala,et al.  Oscillations in H+ and Ca2+ Ion Fluxes around the Elongation Region of Corn Roots and Effects of External pH , 1997, Plant physiology.

[21]  H. Gimmler,et al.  Light-induced H+ transport across the plasma membrane of the acid resistant green alga Dunaliella acidophila , 1994 .

[22]  M. Kura-Hotta,et al.  Light-induced H+ Efflux from Intact Cells of Cyanidium caldarium , 1981 .

[23]  U. Lüttge,et al.  Photosynthesis and apparent proton fluxes in Elodea canadensis , 1972 .

[24]  W. J. Lucas,et al.  Inorganic carbon transport in aquatic photosynthetic organisms , 1985 .

[25]  J. Snel,et al.  The mechanism of bicarbonate assimilation by the polar leaves of Potamogeton and Elodea. CO2 concentrations at the leaf surface , 1982 .

[26]  W. Kaiser,et al.  Fast Cytoplasmic pH Regulation in Acid-Stressed Leaves , 1994 .

[27]  H. Dau,et al.  Relationship between Photosynthesis and Plasmalemma Transport , 1987 .

[28]  E. Volkenburgh,et al.  Red and blue light-stimulated proton efflux by epidermal leaf cells of the Argenteum mutant of Pisum sativum , 1994 .

[29]  C. Slayman,et al.  Ion channels in Arabidopsis plasma membrane : transport characteristics and involvement in light-induced voltage changes. , 1992, Plant physiology.