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Age-dependent changes of photosynthetic responses induced by electrical signals in wheat seedlings

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Abstract

Electrical signals in plants, namely, the action potential (AP) and variation potential (VP) alter the activity of many processes, including photosynthesis. The functional responses induced by electrical signals vary in direction and amplitude, which might be determined by variable conditions of plants prior to stimulation, by the development stage in particular. In this work, the parameters of VP-induced photosynthetic responses were analyzed at various stages of wheat seedling development. Local wounding of the second leaf in wheat plants induced the propagation of VP and altered the activity of photosynthesis at a distance from the wound location. The amplitude of VP was enlarged when the seedling age increased from 11 to 18 days. The VP-induced photosynthetic response changed with age both qualitatively and quantitatively. The amplitude of VP-induced changes in CO2 assimilation and nonphotochemical quenching (NPQ) increased with age, which might be due to the increase in VP amplitude and associated changes in Ca2+ and H+ concentrations. The quantum yield of photosystem II photoreaction was subject to age-dependent changes: the photochemical quantum yield (γ(PSII)) was found to increase after VP in young leaves, whereas the decline in γ(PSII) was observed after the VP propagation in mature leaves. The results may explain the diversity of photosynthetic responses caused by the electrical signals.

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Abbreviations

A:

assimilation of CO2

AP:

action potential

ES:

electrical signal

NPQ:

nonphotochemical quenching

PSI and PSII:

photosystems I and II

γ(PSI) and γ(PSII):

quantum yields of PSI and PSII photoreactions

VP:

variation potential

References

  1. Opritov, V.A., Pyatygin, S.S., and Retivin, V.G., Bioelektrogenez u vysshikh rastenii (Bioelectrogenesis in Higher Plants), Moscow: Nauka, 1991.

    Google Scholar 

  2. Fromm, J. and Lautner, S., Electrical signals and their physiological significance in plants, Plant Cell Environ., 2007, vol. 30, pp. 249–257.

    Article  CAS  PubMed  Google Scholar 

  3. Sibaoka, T., Rapid plant movements triggered by action potentials, Bot. Mag., 1991, vol. 104, pp. 73–95.

    Article  Google Scholar 

  4. Trebacz, K., Dziubinska, H., and Krol, E., Electrical signals in long-distance communication in plants, Communication in Plants. Neuronal Aspects of Plant Life, Baluška, F., Mancuso, S., and Volkmann, D., Eds., Berlin-Heidelberg: Springer-Verlag, 2006, pp. 277–290.

  5. Felle, H., Systemic signalling in barley through action potentials, Planta, 2007, vol. 226, pp. 203–214.

    Article  CAS  PubMed  Google Scholar 

  6. Stahlberg, R., Cleland, R.E., and Volkenburgh, E., Slow wave potentials–a propagating electrical signal unique to higher plants, Communication in Plants. Neuronal Aspects of Plant Life, Baluška, F., Mancuso, S., and Volkmann, D., Eds., Berlin: Springer-Verlag, 2006, pp. 291–309.

  7. Vodeneev, V., Akinchits, E., and Sukhov, V., Variation potential in higher plants: mechanisms of generation and propagation, Plant Signal Behav., 2015, vol. 10, p. e1057365. doi 10.1080/15592324.2015.1057365

    Article  PubMed  PubMed Central  Google Scholar 

  8. Rhodes, J.D., Thain, J.F., and Wildon, D.C., Evidence for physically distinct systemic signalling pathways in the wounded tomato plant, Ann. Bot., 1999, vol. 84, pp. 109–116.

    Article  CAS  Google Scholar 

  9. Julien, J.L., Desbiez, M.O., De Jaegher, G., and Frachisse, J.M., Characteristics of the wave of depolarization induced by wounding in Bidens pilosa L., J. Exp. Bot., 1991, vol. 42, pp. 131–137.

    Article  Google Scholar 

  10. Vodeneev, V.A., Akinchits, E.K., Orlova, L.A., and Sukhov, V.S., The role of Ca2+,H+,and Clions in generation of variation potential in pumpkin plants, Russ. J. Plant Physiol., 2011, vol. 58, pp. 974–981.

    Article  CAS  Google Scholar 

  11. Katicheva, L., Sukhov, V., Akinchits, E., and Vodeneev, V., Ionic nature of burn-induced variation potential in wheat leaves, Plant Cell Physiol., 2014, vol. 55, pp. 1511–1519.

    Article  CAS  PubMed  Google Scholar 

  12. Lautner, S., Stummer, M., Matyssek, R., Fromm, J., and Grams, T.E.E., Involvement of respiratory processes in the transient knockout of net CO2 uptake in Mimosa pudica upon heat stimulation, Plant Cell Environ., 2014, vol. 37, pp. 254–260.

    Article  CAS  PubMed  Google Scholar 

  13. Krupenina, N.A. and Bulychev, A.A., Action potential in a plant cell lowers the light requirement for non-photochemical energy-dependent quenching of chlorophyll fluorescence, Biochim. Biophys. Acta, 2007, vol. 1767, pp. 781–788.

    Article  CAS  PubMed  Google Scholar 

  14. Grams, T.E.E., Lautner, S., Felle, H.H., Matyssek, R., and Fromm, J., Heat-induced electrical signals affect cytoplasmic and apoplastic pH as well as photosynthesis during propagation through the maize leaf, Plant Cell Environ., 2009, vol. 32, pp. 319–326.

    Article  CAS  PubMed  Google Scholar 

  15. Pavlovic, A., Slováková, L., Pandolfi, C., and Mancuso, S., On the mechanism underlying photosynthetic limitation upon trigger hair irritation in the carnivorous plant Venus flytrap (Dionaea muscipula Ellis), J. Exp. Bot., 2011, vol. 62, pp. 1991–2000.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  16. Sukhov, V., Orlova, L., Mysyagin, S., Sinitsina, J., and Vodeneev, V., Analysis of the photosynthetic response induced by variation potential in geranium, Planta, 2012, vol. 235, pp. 703–712.

    Article  CAS  PubMed  Google Scholar 

  17. Sukhov, V., Sherstneva, O., Surova, L., Katicheva, L., and Vodeneev, V., Proton cellular influx as a probable mechanism of variation potential influence on photosynthesis in pea, Plant Cell Environ., 2014, vol. 37, pp. 2532–2541.

    Article  CAS  PubMed  Google Scholar 

  18. Sukhov, V., Surova, L., Sherstneva, O., Katicheva, L., and Vodeneev, V., Variation potential influence on photosynthetic cyclic electron flow in pea, Front. Plant Sci., 2015, vol. 5, p. 766. doi 10.3389/fpls.2014.00766

    Article  PubMed  PubMed Central  Google Scholar 

  19. Gallé, A., Lautner, S., Flexas, J., Ribas-Carbo, M., Hanson, D., Roesgen, J., and Fromm, J., Photosynthetic responses of soybean (Glycine max L.) to heatinduced electrical signalling are predominantly governed by modifications of mesophyll conductance for CO2, Plant Cell Environ., 2013, vol. 36, pp. 542–552.

    Article  PubMed  Google Scholar 

  20. Sherstneva, O.N., Vodeneev, V.A., Katicheva, L.A., Surova, L.M., and Sukhov, V.S., Participation of intracellular and extracellular pH changes in photosynthetic response development induced by variation potential in pumpkin seedlings, Biochemistry (Moscow), 2015, vol. 80, pp. 776–784.

    Article  CAS  Google Scholar 

  21. Sherstneva, O.N., Surova, L.M., Vodeneev, V.A., Plotnikova, Yu.I., Bushueva, A.V., and Sukhov, V.S., Biochemistry (Moscow), Suppl. Ser. A: Membr. Cell Biol., 2016, vol. 10, pp. 60–67.

    Google Scholar 

  22. Krupenina, N.A., Bulychev, A.A., Roelfsema, M.R.G., and Schreiber, U., Action potential in Chara cells intensifies spatial patterns of photosynthetic electron flow and non-photochemical quenching in parallel with inhibition of pH banding, Photochem. Photobiol. Sci., 2008, vol. 7, pp. 681–688.

    Article  CAS  PubMed  Google Scholar 

  23. Sukhov, V.S., Surova, L.M., Sherstneva, O.N., Rumyantsev, E.A., and Vodeneev, V.A., Influence of a variation potential on photosynthesis in pumpkin seedlings (Cucurbita pepo L.), Biophysics, 2013, vol. 58, pp. 361–365.

    Article  CAS  Google Scholar 

  24. Fromm, J. and Fei, H., Electrical signaling and gas exchange in maize plants of drying soil, Plant Sci., 1998, vol. 132, pp. 203–213.

    Article  CAS  Google Scholar 

  25. Grams, T.E.E., Koziolek, C., Lautner, S., Matyssek, R., and Fromm, J., Distinct roles of electric and hydraulic signals on the reaction of leaf gas exchange upon re-irrigation in Zea mays L., Plant Cell Environ., 2007, vol. 30, pp. 79–85.

    Article  PubMed  Google Scholar 

  26. Lawlor, D.W., Boyle, F.A., Young, A.T., Key, A.J., and Kendall, A.C., Nitrate nutrition and temperature effects on wheat: photosynthesis and photorespiration of leaves, J. Exp. Bot., 1987, vol. 38, no. 188, pp. 393–408.

    Article  Google Scholar 

  27. Suzuki, S., Nakamoto, H., Ku, M., and Edwards, G., Influence of leaf age on photosynthesis, enzyme activity, and metabolite levels in wheat, Plant Physiol., 1987, vol. 84, pp. 1244–1248.

    CAS  PubMed  Google Scholar 

  28. Vodeneev, V., Orlova, A., Morozova, E., Orlova, L., Akinchits, E., Orlova, O., and Sukhov, V., The mechanism of propagation of variation potentials in wheat leaves, J. Plant Physiol., 2012, vol. 169, pp. 949–954.

    Article  CAS  PubMed  Google Scholar 

  29. Von Caemmerer, S. and Farquhar, G.D., Some relationships between the biochemistry of photosynthesis and the gas exchange of leaves, Planta, 1981, vol. 153, pp. 376–387.

    Article  Google Scholar 

  30. Maxwell, K. and Johnson, G.N., Chlorophyll fluorescence—a practical guide, J. Exp. Bot., 2000, vol. 51, pp. 659–668.

    Article  CAS  PubMed  Google Scholar 

  31. Sukhov, V., Surova, L., Sherstneva, O., Bushueva, A., and Vodeneev, V., Variation potential induces decreased PSI damage and increased PSII damage under high external temperatures in pea, Funct. Plant Biol., 2015, vol. 42, pp. 727–736.

    Article  Google Scholar 

  32. Polyakova, I.B., Karavaev, V.A., Solntsev, M.K., and Chechulina, A.A., Luminescence indices of different parts of the wheat leaf during ontogeny, Biophysics, 2003, vol. 48, pp. 1025–1031.

    Google Scholar 

  33. Šestak, Z., Changes in electron transport chain composition and activities of photosystems and photophosphorylation during leaf ontogeny, in Photosynthesis during Leaf Development, Šestak, Z., Ed., Lancaster: Dr. W. Junk Publ., 1985, pp. 128–144.

    Google Scholar 

  34. Stiles, K.A. and Van Volkenburgh, E., Light-regulated leaf expansion in two Populus species: dependence on developmentally controlled ion transport, J. Exp. Bot., 2002, vol. 53, pp. 1651–1657.

    Article  CAS  PubMed  Google Scholar 

  35. Retivin, V.G., Opritov, V.A., and Fedulina, S.B., Generation of action potential induces preadaptation of Cucurbita pepo L. stem tissues to freezing injury, Russ. J. Plant Physiol., 1997, vol. 44, pp. 432–442.

    CAS  Google Scholar 

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Correspondence to V. A. Vodeneev.

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Original Russian Text © V.A. Vodeneev, O.N. Sherstneva, L.M. Surova, M.M. Semina, L.A. Katicheva, V.S. Sukhov, 2016, published in Fiziologiya Rastenii, 2016, Vol. 63, No. 6, pp. 873–880.

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Vodeneev, V.A., Sherstneva, O.N., Surova, L.M. et al. Age-dependent changes of photosynthetic responses induced by electrical signals in wheat seedlings. Russ J Plant Physiol 63, 861–868 (2016). https://doi.org/10.1134/S1021443716050162

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  • DOI: https://doi.org/10.1134/S1021443716050162

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