Influence of variation potential on resistance of the photosynthetic machinery to heating in pea.

Electrical signals [action potentials (APs) and variation potentials (VPs)] induced by local stimuli are a mechanism that underlies rapid plant response to environmental factors. Such signals induce a number of functional responses, including changes in photosynthesis. Ultimately, these responses are considered to increase plant resistance to stress factors, but this question has been poorly investigated. We studied the influence of VP on photosynthesis and resistance of the photosynthetic machinery to heating in leaves of pea (Pisum sativum). Localized burning induced a VP that decreased photosynthesis parameters [CO(2) assimilation rate and quantum yields of photosystem I (PSI) and photosystem II (PSII)]. The photosynthetic response was initiated by a decrease in photosynthesis dark-stage activity, which in turn increased resistance of PSI to heating. Three results supported this hypothesized mechanism: (1) the magnitude of VP-induced decrease in CO(2) assimilation and enhanced PSI resistance to heating were highly correlated; (2) the VP influence on PSI resistance to heating was suppressed under a low external CO(2) concentration and (3) decreasing external CO(2) concentration imitated the VP-induced photosynthetic response and increased PSI resistance to heating.

[1]  R. Strasser,et al.  Temperature Effects on Pea Plants Probed by Simultaneous Measurements of the Kinetics of Prompt Fluorescence, Delayed Fluorescence and Modulated 820 nm Reflection , 2013, PloS one.

[2]  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.

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

[4]  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.

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

[6]  Thomas D. Sharkey,et al.  Photosynthetic electron transport and proton flux under moderate heat stress , 2009, Photosynthesis Research.

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

[8]  R. Matyssek,et al.  Involvement of respiratory processes in the transient knockout of net CO2 uptake in Mimosa pudica upon heat stimulation. , 2014, Plant, Cell and Environment.

[9]  G. Johnson,et al.  Physiology of PSI cyclic electron transport in higher plants. , 2011, Biochimica et biophysica acta.

[10]  M. Hajirezaei,et al.  Electrical signaling along the phloem and its physiological responses in the maize leaf , 2013, Front. Plant Sci..

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

[12]  D. Cosgrove,et al.  Rapid alterations in growth rate and electrical potentials upon stem excision in pea seedlings , 1992, Planta.

[13]  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.

[14]  J. Fisahn,et al.  Effects of mechanical wounding, current application and heat treatment on chlorophyll fluorescence and pigment composition in tomato plants , 1999 .

[15]  V. G. Retivin,et al.  Generation of action potential induces preadaptation of Cucurbita pepo L. stem tissues to freezing injury , 1997 .

[16]  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.

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

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

[19]  V. Sukhov,et al.  Analysis of the photosynthetic response induced by variation potential in geranium , 2011, Planta.

[20]  M. Malone,et al.  Wound-induced hydraulic signals and stimulus transmission in Mimosa pudica L. , 1994, The New phytologist.

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

[22]  D. Los,et al.  Heat stress: an overview of molecular responses in photosynthesis , 2008, Photosynthesis Research.

[23]  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.

[24]  J. D. Rhodes,et al.  Evidence for Physically Distinct Systemic Signalling Pathways in the Wounded Tomato Plant , 1999 .

[25]  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.

[26]  J. Komenda,et al.  Heat-induced disassembly and degradation of chlorophyll-containing protein complexes in vivo. , 2010, Biochimica et biophysica acta.

[27]  V. Sukhov,et al.  The role of Ca2+, H+, and Cl− ions in generation of variation potential in pumpkin plants , 2011, Russian Journal of Plant Physiology.

[28]  D. Cosgrove,et al.  Induction and ionic basis of slow wave potentials in seedlings of Pisum sativum L. , 1996, Planta.

[29]  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.

[30]  Stefano Mancuso,et al.  Hydraulic and electrical transmission of wound-induced signals in Vitis vinifera , 1999 .

[31]  É. Hideg,et al.  Production, detection, and signaling of singlet oxygen in photosynthetic organisms. , 2013, Antioxidants & redox signaling.

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

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

[34]  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.

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

[36]  S. Mancuso,et al.  Electrical signaling and photosynthesis , 2011, Plant signaling & behavior.

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

[38]  V. Sukhov,et al.  The mechanism of propagation of variation potentials in wheat leaves. , 2012, Journal of plant physiology.

[39]  A. Laisk,et al.  Partitioning of the Leaf CO2 Exchange into Components Using CO2 Exchange and Fluorescence Measurements , 1994, Plant physiology.

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

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

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

[43]  U. Heber,et al.  Heat sensitivity of chloroplasts and leaves: Leakage of protons from thylakoids and reversible activation of cyclic electron transport , 1999, Photosynthesis Research.

[44]  T. Sharkey,et al.  High temperature effects on electron and proton circuits of photosynthesis. , 2010, Journal of integrative plant biology.

[45]  Lyubov Katicheva,et al.  Simulation of Variation Potential in Higher Plant Cells , 2013, The Journal of Membrane Biology.

[46]  K. Tomizawa,et al.  Enhancement of cyclic electron flow around PSI at high light and its contribution to the induction of non-photochemical quenching of chl fluorescence in intact leaves of tobacco plants. , 2004, Plant & cell physiology.

[47]  Bratislav Stankovic,et al.  Surface potentials and hydraulic signals in wheat leaves following localized wounding by heat , 1991 .

[48]  V. Sukhov,et al.  Influence of a variation potential on photosynthesis in pumpkin seedlings (Cucurbita pepo L.) , 2013, Biofizika.

[49]  V. Vodeneev,et al.  Reversible changes of extracellular pH during action potential generation in a higher plant Cucurbita pepo , 2006, Russian Journal of Plant Physiology.

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

[51]  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 .

[52]  O. Popova,et al.  NAD- AND NADP-ISOCITRATE DEHYDROGENASES AND GLUTAMATE DECARBOXYLASE OF PEASEEDLINGS AS AFFECTED BY SALINITY STRESS , 1999 .

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

[54]  A. Gilmore,et al.  Quantitative analysis of the effects of intrathylakoid pH and xanthophyll cycle pigments on chlorophyll a fluorescence lifetime distributions and intensity in thylakoids. , 1998, Biochemistry.

[55]  V. Sukhov,et al.  A Mathematical Model of Action Potential in Cells of Vascular Plants , 2009, Journal of Membrane Biology.

[56]  A. Portis,et al.  Oxygen‐dependent H2O2 production by Rubisco , 2004, FEBS letters.

[57]  Jian-Kang Zhu,et al.  Rapid phosphatidic acid accumulation in response to low temperature stress in Arabidopsis is generated through diacylglycerol kinase , 2013, Front. Plant Sci..

[58]  C. Foyer,et al.  Redox regulation in photosynthetic organisms: signaling, acclimation, and practical implications. , 2009, Antioxidants & redox signaling.