PhysiologyVariation potential-induced photosynthetic and respiratory changes 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).
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What do plants need action potentials for?
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