Analysis of the photosynthetic response induced by variation potential in geranium

Electrical signals (action and variation potentials) caused by environmental stimuli induce a number of physiological responses in plants including changes in photosynthesis; however, mechanisms of these changes remain unclear. We investigated the influence of the variation potential on photosynthesis in geranium (Pelargonium zonale) under different conditions (control, low external CO2 concentration, and actinic light absence). The variation potential caused by lamina burning induced a reduction in photosynthesis (decreases in effective quantum yields of photosystem I and II, CO2 assimilation rate, and stomatal conductance) in unstimulated leaves under control conditions. Changes in the majority of light-stage parameters (photosystem I and II quantum yields, coefficients of photochemical and non-photochemical quenching, quantum yield of non-photochemical energy dissipation in photosystem I due to donor-side limitation) were correlated with a decrease in CO2 assimilation rate. The changes were similar to those caused by lowering [CO2]; their magnitudes decreased both under low external CO2 concentration and without actinic light. These results support the hypothesis that Calvin cycle inactivation plays a key role in photosynthetic response induced by electrical signals. However, a decrease in electron transport through the PSI acceptor side also induced by variation potential was not correlated with a decrease in the CO2 assimilation rate and did not depend on the external CO2 concentration or actinic light intensity. Thus, we suggest that there are two different mechanisms of light-stage inactivation induced by the variation potential in geranium: one strongly dependent on dark-stage inactivation and one weakly dependent on dark-stage inactivation.

[1]  J. Fromm,et al.  Control of phloem unloading by action potentials in Mimosa , 1991 .

[2]  Jean-Marie Frachisse,et al.  Characteristics of the Wave of Depolarization Induced by Wounding in Bidens pilosa L. , 1991 .

[3]  Jörg Fromm,et al.  Electric Signals Released from Roots of Willow (Salix viminalis L.) Change Transpiration and Photosynthesis , 1993 .

[4]  Jörg Fromm,et al.  Action potentials in maize sieve tubes change phloem translocation , 1994 .

[5]  A. Jagendorf,et al.  Signals involved in wound-induced proteinase inhibitor II gene expression in tomato and potato plants. , 1995, Proceedings of the National Academy of Sciences of the United States of America.

[6]  U. Heber,et al.  Relationship between photosynthetic electron transport and pH gradient across the thylakoid membrane in intact leaves. , 1995, Proceedings of the National Academy of Sciences of the United States of America.

[7]  B. Stanković,et al.  Both action potentials and variation potentials induce proteinase inhibitor gene expression in tomato , 1996, FEBS letters.

[8]  M. Filek,et al.  The effect of wounding the roots by high temperature on the respiration rate of the shoot and propagation of electric signal in horse bean seedlings (Vicia faba L. minor) , 1997 .

[9]  J. Fromm,et al.  Electrical signaling and gas exchange in maize plants of drying soil , 1998 .

[10]  K. Asada,et al.  THE WATER-WATER CYCLE IN CHLOROPLASTS: Scavenging of Active Oxygens and Dissipation of Excess Photons. , 1999, Annual review of plant physiology and plant molecular biology.

[11]  C. Foyer,et al.  Homeostasis of adenylate status during photosynthesis in a fluctuating environment. , 2000, Journal of experimental botany.

[12]  K Maxwell,et al.  Chlorophyll fluorescence--a practical guide. , 2000, Journal of experimental botany.

[13]  K. Niyogi,et al.  Non-photochemical quenching. A response to excess light energy. , 2001, Plant physiology.

[14]  V. Hurry,et al.  Cold acclimation of Arabidopsis thaliana results in incomplete recovery of photosynthetic capacity, associated with an increased reduction of the chloroplast stroma , 2001, Planta.

[15]  J. Flexas,et al.  Regulation of photosynthesis of C3 plants in response to progressive drought: stomatal conductance as a reference parameter. , 2002, Annals of botany.

[16]  J. Allen.  Cyclic, pseudocyclic and noncyclic photophosphorylation: new links in the chain. , 2003, Trends in plant science.

[17]  Janusz Koscielniak,et al.  Variation and action potentials evoked by thermal stimuli accompany enhancement of ethylene emission in distant non-stimulated leaves of Vicia faba minor seedlings. , 2003, Journal of plant physiology.

[18]  S. Müller,et al.  Effect of a Single Excitation Stimulus on Photosynthetic Activity and Light-dependent pH Banding in Chara Cells , 2004, The Journal of Membrane Biology.

[19]  G. Farquhar,et al.  Some relationships between the biochemistry of photosynthesis and the gas exchange of leaves , 1981, Planta.

[20]  N. Baker,et al.  Resolving chlorophyll a fluorescence images of photosynthetic efficiency into photochemical and non-photochemical components – calculation of qP and Fv-/Fm-; without measuring Fo-; , 1997, Photosynthesis Research.

[21]  Rainer Matyssek,et al.  Transient knockout of photosynthesis mediated by electrical signals. , 2004, The New phytologist.

[22]  N. Bukhov.  Dynamic Light Regulation of Photosynthesis (A Review) , 2004, Russian Journal of Plant Physiology.

[23]  J. Fisahn,et al.  Analysis of the transient increase in cytosolic Ca2+ during the action potential of higher plants with high temporal resolution: requirement of Ca2+ transients for induction of jasmonic acid biosynthesis and PINII gene expression. , 2004, Plant & cell physiology.

[24]  C. Buschmann.  Photochemical and Non-Photochemical Quenching Coefficients of the Chlorophyll Fluorescence: Comparison of Variation and Limits , 1999, Photosynthetica.

[25]  Rainer Matyssek,et al.  Characteristics of Electrical Signals in Poplar and Responses in Photosynthesis1 , 2005, Plant Physiology.

[26]  H. Kaiser,et al.  Rapid hydropassive opening and subsequent active stomatal closure follow heat-induced electrical signals in Mimosa pudica. , 2006, Journal of experimental botany.

[27]  T. Sibaoka,et al.  Rapid plant movements triggered by action potentials , 1991, The botanical magazine = Shokubutsu-gaku-zasshi.

[28]  František Baluška,et al.  Communication in Plants , 2006 .

[29]  E. Davies,et al.  Electrical Signals, the Cytoskeleton, and Gene Expression: a Hypothesis on the Coherence of the Cellular Responses to Environmental Insult , 2006 .

[30]  E. Król,et al.  Electrical Signals in Long-Distance Communication in Plants , 2006 .

[31]  P. Joliot,et al.  Cyclic electron flow in C3 plants. , 2006, Biochimica et biophysica acta.

[32]  Ondřej Novák,et al.  Electrical and chemical signals involved in short-term systemic photosynthetic responses of tobacco plants to local burning , 2006, Planta.

[33]  Hubert H. Felle,et al.  Systemic signalling in barley through action potentials , 2007, Planta.

[34]  E. Davies,et al.  Electrical Signals in Plants: Facts and Hypotheses , 2006 .

[35]  Rainer Stahlberg,et al.  Slow Wave Potentials — a Propagating Electrical Signal Unique to Higher Plants , 2006 .

[36]  A. Bulychev,et al.  Action potential in a plant cell lowers the light requirement for non-photochemical energy-dependent quenching of chlorophyll fluorescence. , 2007, Biochimica et biophysica acta.

[37]  Alexander G. Volkov,et al.  Plant Electrophysiology: Theory and Methods , 2007 .

[38]  J. Fromm,et al.  Electrical signals and their physiological significance in plants. , 2007, Plant, cell & environment.

[39]  Rainer Matyssek,et al.  Distinct roles of electric and hydraulic signals on the reaction of leaf gas exchange upon re-irrigation in Zea mays L. , 2007, Plant, cell & environment.

[40]  G. Peltier,et al.  Chlororespiration and cyclic electron flow around PSI during photosynthesis and plant stress response. , 2007, Plant, cell & environment.

[41]  V. Sukhov,et al.  Influence of propagating electrical signals on delayed luminescence in pelargonium leaves: Experimental analysis , 2008 .

[42]  U. Schreiber,et al.  Saturation Pulse method for assessment of energy conversion in PS I , 2008 .

[43]  V. Sukhov,et al.  Influence of propagating electrical signals on delayed luminescence in pelargonium leaves: Theoretical analysis , 2008 .

[44]  M. Roelfsema,et al.  Action potential in Chara cells intensifies spatial patterns of photosynthetic electron flow and non-photochemical quenching in parallel with inhibition of pH banding , 2008, Photochemical and Photobiological Sciences.

[45]  J. Reinitz,et al.  Dynamic filtration of the expression pattern variability of Drosophila zygotic segmentation genes , 2008 .

[46]  H. Felle,et al.  Dissection of heat-induced systemic signals: superiority of ion fluxes to voltage changes in substomatal cavities , 2009, Planta.

[47]  V. Vodeneev,et al.  Signaling role of action potential in higher plants , 2008, Russian Journal of Plant Physiology.

[48]  R. Matyssek,et al.  Heat-induced electrical signals affect cytoplasmic and apoplastic pH as well as photosynthesis during propagation through the maize leaf. , 2009, Plant, cell & environment.

[49]  J. Ward,et al.  Tansley review Plant responses to low [ CO 2 ] of the past , 2010 .

[50]  J. Ward,et al.  Plant responses to low [CO2] of the past. , 2010, The New phytologist.

[51]  Stefano Mancuso,et al.  On the mechanism underlying photosynthetic limitation upon trigger hair irritation in the carnivorous plant Venus flytrap (Dionaea muscipula Ellis) , 2011, Journal of experimental botany.