Elsevier

Journal of Plant Physiology

Volume 202, 1 September 2016, Pages 57-64
Journal of Plant Physiology

Physiology
Variation potential-induced photosynthetic and respiratory changes increase ATP content in pea leaves

https://doi.org/10.1016/j.jplph.2016.05.024Get rights and content

Abstract

Local damage induces a physiological response in higher plants by means of generation and propagation of variation potential (VP). The response includes changes in photosynthesis and respiration. The aim of the present study was to investigate the effect of these changes on adenosine triphosphate (ATP) content in pea leaves. VP was induced by local heating of the first mature leaf and registered using extracellular and intracellular electrodes. Photosynthesis and respiration were measured using Dual-PAM-100 and GFS-3000. ATP content was determined using a bioluminescence-based ATP determination kit. Two non-stimulated leaves (second and fourth) were investigated. We showed that heating induced VP that propagated into the second mature leaf, but only a slight electrical reaction was registered in the fourth mature leaf. VP-induced inactivation of photosynthesis developed in the second leaf and included two stages: short- and long-term inactivation. Local heating also caused a two-stage increase in ATP content in the second leaf, which was connected with the photosynthetic responses. Changes in photosynthesis and ATP content were not observed in the fourth leaf. The effect of VP on respiration was investigated under dark conditions. We found that variation potential induced short-term activation of respiration in the second leaf. Local heating induced ATP content increase which included only one stage under dark conditions. Changes in ATP and respiration were absent in the fourth leaf under dark conditions. Thus, VP-induced photosynthetic and respiratory changes are likely to increase ATP content in pea leaves.

Introduction

Environmental stressors induce physiological responses that can develop under the influence of systemic and local factors. The influence of local stressors on plant functions requires rapid signal development and response to connect the stimulated zone with the non-stimulated plant tissues. Electrical signals, including action potential (AP) and variation potential (VP), can play this role (Volkov, 2000, Dziubinska, 2003, Brenner et al., 2006, Stahlberg et al., 2006, Fromm and Lautner, 2007, Pyatygin et al., 2008, Król et al., 2010). Non-damaging stimuli induce self-propagated AP, which is based mainly on activation of Ca2+, Cl, and K+ channels (Felle and Zimmermann, 2007). Damaging stimuli cause hydraulic wave propagation and/or wound substance transmission that induces VP in undamaged plant parts (Malone, 1994, Mancuso, 1999, Stahlberg et al., 2006, Vodeneev et al., 2012, Sukhov et al., 2013). VP generation is based mainly on inactivation of H+-ATPase in the plasma membrane (Julien et al., 1991, Stahlberg and Cosgrove, 1996), but ion channels also participate in this process (Vodeneev et al., 2011, Sukhov et al., 2013, Katicheva et al., 2014).

It is known that electrical signals influence gene expression (Stanković and Davies, 1996, Fisahn et al., 2004, Mousavi et al., 2013), phytohormone synthesis (Fisahn et al., 2004, Hlaváčková et al., 2006, Mousavi et al., 2013), phloem transport (Fromm and Bauer, 1994), and plant resistance to stressors (Retivin et al., 1997, Retivin et al., 1999, Mousavi et al., 2013, Sukhov et al., 2014b, Sukhov et al., 2015b). In particular, AP and VP inactivate photosynthesis (Hlaváčková et al., 2006, Krupenina and Bulychev, 2007, Krupenina et al., 2008, Grams et al., 2009, Pavlovič et al., 2011, Sukhov et al., 2012, Sukhov et al., 2014a, Sukhov et al., 2014b, Sukhov et al., 2014a, Sukhov et al., 2014b, Bulychev and Komarova, 2014, Sherstneva et al., 2015) and activate respiration (Dziubinska et al., 1989, Filek and Kościelniak, 1997, Pavlovič et al., 2011, Sukhov et al., 2014a, Sherstneva et al., 2015) in plants. Photosynthesis dark stage inactivation is likely the primary stage of photosynthetic response induced by AP and VP (Krupenina and Bulychev, 2007, Pavlovič et al., 2011, Sukhov et al., 2012, Sukhov et al., 2014a, Sukhov et al., 2014b, Sukhov et al., 2015a, Sherstneva et al., 2015). Changes in light stage reactions are mainly connected with this inactivation. However, a direct influence of electrical signals on photosystems I (PSI) and II (PSII) is also possible (Sukhov et al., 2012, Sukhov et al., 2014a, Sukhov et al., 2015a, Vredenberg and Pavlovič, 2013). There are two potential ways that electrical signals initiate the photosynthetic response in plants. Investigation of AP influence on photosynthesis in Chara showed that Ca2+ influx is the potential initiator of photosynthetic changes (Krupenina and Bulychev, 2007). Analysis of VP influence on photosynthesis on higher plants has shown that the VP effect is associated with H+ influx (Grams et al., 2009, Sukhov et al., 2014a, Sherstneva et al., 2015). Additionally, the slow influence of VP on photosynthesis (tens of minutes) could be connected with increase of abscisic and jasmonic acids concentrations (Hlaváčková et al., 2006, Hlavinka et al., 2012). The mechanisms of electrical signal-induced activation of respiration are unclear.

Both photosynthesis electrical signals induced dark stage inactivation, which contributes to decreased ATP consumption in chloroplasts (Pavlovič et al., 2011), and respiration activation can potentially increase ATP content in leaves. Increased ATP may play an important role in plant adaptation to stress (Sukhov et al., 2014b). However, experimental data on the influence of electrical signals on ATP content in plants are contradictory. According to Pyatygin et al. (2008), AP induced multiphase changes in ATP content in phloem. However, leaf stimulation by ice water and cutting of the leaf tip did not induce significant differences in ATP concentration 15 min after the stress was applied (Fromm et al., 2013). These results may be caused by different dynamics of photosynthetic and respiratory responses, but connection of these responses with ATP content has not been investigated previously. The aim of the present work was to investigate the influence of variation potential-induced photosynthetic and respiratory changes on ATP content in pea leaves.

Section snippets

Plant material

Pea (Pisum sativum L.) seedlings were cultivated hydroponically in a Binder KBW 240 plant growth chamber (Binder GmbH, Tuttlingen, Germany) at 24 °C under a 16/8 h (light/dark) photoperiod. Seedlings used in experiments were 14–21 days old.

Stimulation and electrical measurements

Stimulation and electrical measurements were carried out according to our previous work with pea seedlings (Sukhov et al., 2014a). VP was induced by heating ∼1 cm2 of a first mature leaf tip over a flame for 3–4 s (Fig. 1).

The surface electrical potential was

Propagation of variation potential induced by local heating

Local heating of the first mature leaf induced VP generation in pea seedlings (Fig. 2), which has been shown using measurements of surface membrane potential. In stems, VP amplitudes were about 67 mV near the second leaf and about 43 mV near the fourth leaf; therefore, decrement of variation potential was about 6.4% cm−1. However, the moderate decrease of VP amplitude in stems is likely to strongly influence VP in leaves located proximal to the induction site. VP amplitude in the second leaf was

Discussion

Our results showed that local heating can induce changes in ATP content in the undamaged leaves. The changes have first and second maximums that are in accordance with the multiphase dynamics of ATP content in phloem exudate observed after electrical signal induction (Pyatygin et al., 2008).

It is likely that local heating-induced photosynthetic inactivation, which was observed in the present work as well as in other experiments (Sukhov et al., 2014a, Sukhov et al., 2014b) is the main mechanism

Conclusion

Our results show that local heating of the leaf can induce an increase in ATP content in undamaged peas leaves. The increase is caused by photosynthesis inactivation and respiratory activation, which are induced by local heating. Variation potential, which is induced by local heating and can propagate through plant, is the likely mechanism of induction of photosynthetic and respiratory responses. Thus, variation potential-induced photosynthetic and respiratory changes increase ATP content in

Acknowledgments

Investigation of electrical activity using intracellular electrodes was supported by the Russian Science Foundation (Project No. 14-26-00098). Investigations of electrical activity using extracellular electrodes, ATP content, respiration and photosynthetic responses were supported by the Russian Foundation for Basic Research (Project No. 14-04-01899 А).

References (52)

  • S.I. Allakhverdiev et al.

    Heat stress: an overview of molecular responses in photosynthesis

    Photosynth. Res.

    (2008)
  • A.A. Bulychev et al.

    Long-distance signal transmission and regulation of photosynthesis in characean cells

    Biochemistry (Moscow)

    (2014)
  • H. Dziubinska et al.

    The effect of excitation on the rate of respiration in the liverwort Conocephalum conicum

    Physiol. Plant.

    (1989)
  • H. Dziubinska

    Ways of signal transmission and physiological role of electrical potential in plants

    Acta Soc. Bot. Pol.

    (2003)
  • H.H. Felle et al.

    Systemic signaling in barley through action potentials

    Planta

    (2007)
  • 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

    Plant Cell Physiol.

    (2004)
  • J. Fromm et al.

    Action potentials in maize sieve tubes change phloem translocation

    J. Exp. Bot.

    (1994)
  • J. Fromm et al.

    Electrical signals and their physiological significance in plants

    Plant Cell Environ.

    (2007)
  • J. Fromm et al.

    Electrical signaling along the phloem and its physiological responses in the maize leaf

    Front. Plant Sci.

    (2013)
  • D.F. Gaff et al.

    ATP and ADP contents in leaves of drying and rehydrating desiccation tolerant plants

    Oecologia

    (1989)
  • T.E.E. Grams et al.

    Heat-induced electrical signals affect cytoplasmic and apoplastic pH as well as photosynthesis during propagation through the maize leaf

    Plant Cell Environ.

    (2009)
  • V. Hlaváčková et al.

    Electrical and chemical signals involved in short-term systemic photosynthetic responses of tobacco plants to local burning

    Planta

    (2006)
  • J.L. Julien et al.

    Characteristics of the wave of depolarization induced by wounding in Bidens pilosa L

    J. Exp. Bot.

    (1991)
  • L. Katicheva et al.

    Ionic nature of burn-induced variation potential in wheat leaves

    Plant Cell Physiol.

    (2014)
  • C. Klughammer et al.

    Saturation pulse method for assessment of energy conversion in PS I

    PAM Appl. Notes

    (2008)
  • E. Król et al.

    What do plants need action potentials for?

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