Environmental stimuli and physiological responses: The current view on electrical signalling
Introduction
Classic work on action potentials in plants already indicates that all higher plants may use electrical signals to regulate various physiological functions (Pickard, 1973). Within the last few years, focus on plant electrophysiology research has strongly shifted from short-distance, uni-cellular towards long-distance, systemic signalling. Remarkably enough, plants also possess most of the chemistry of the neuromotoric system in animals, i.e. neurotransmitters, such as acetylcholine, or cellular messengers, such as calmodulin, or cellular motors, e.g. actin. Further, voltage-gated ion channels as well as sensors for touch, for light, gravity and temperature, have been manifoldly detected in plant physiology research. And yet, despite the cellular equipment, electrical signalling in plants has not reached the great complexity as in nerves. However, a very simple neural network-like signalling pathway has been formed with the phloem tissue, allowing plants to communicate successfully over long distances. The necessity for plants to having developed networks of electrical signalling is most likely due to enable rapid response to environmental stimuli and stress factors. Various stimulations trigger specific electric responses in living plant cells, which then have the ways and means to transmit the signal to a distant responding region. Contrasting chemical signalling, e.g. by phytohormones, electrical signals are able to transmit information over long distances very rapidly: most of the plant action potentials (AP) investigated so far revealed velocities ranging between 0.005 and 0.2 m s−1 (Fromm and Lautner, 2007).
Despite all the similarities between animal neuronal systems and plant signalling pathways, it appears to be unlikely that latter was actually adopted from the animal system. Rather we would need to look at unicellular ancestors, which have no need for transmitting signals over long distances, when searching for the common evolutionary roots of action potentials in plants and animals. Consequently, the transfer function of electrical signalling over distances most likely has evolved at a later evolutionary stage, assuming, that during the course of evolution development of plants and animals branched off into different directions. It becomes obvious, that both plants and animals inherited their principle neuronal capabilities from their bacterial ancestors, since cellular excitability has been shown to exist in those primitive organisms (Simons, 1992). This has been set out for example for changes in membrane potential during bacterial chemotaxis (Szmelcman and Adler, 1976) or the sensitivity to mechanical touch. Regarding the latter function, pressure-sensitive ion channels are hypothesized to have a principally osmotic function (Martinac et al., 1987). Likewise, for the early formation of action potentials osmotic function might also have been the purpose, as studies on unicellular algae such as Acetabularia indicated (Mummert and Gradmann, 1976). But also characean algae have shown to form action potentials, as was shown at a very early stage of plant electrophysiology for Nitella in the internodal cells (Hörmann, 1898). Here, the functional resemblance of electrical stimulation to the contraction response displayed by skeletal muscle cells after electrical stimulation by nerve cells was illustrated. Once having left aquasphere and taken over dry land during the course of evolution, requirements on the cellular excitability and signalling capability have also altered. The focus shifted towards working out of survival techniques in order to meet the needs of the new environment, e.g. the development of stomatal guard cell’s capacity of prompt responding, or the development of an electrical communication network system, using the phloem tissue to transmit signals and the corresponding information over long distances within the plant body (Fromm and Lautner, 2006, Fromm and Lautner, 2007).
Section snippets
Types of electrical signals
Various types of electrical signals are transmitted along the phloem pathway. In general, two main types of signals occur in plants, rapid action potentials (APs) propagate with velocities of 0.5–20 cm/sec while the velocity of variation potentials (VPs) is in the range of 0.1–1.0 cm/s (Fromm and Lautner, 2007, Stahlberg and Cosgrove, 1997). Moreover, electrical signals are characterized on the basis of amplitude, duration and profile. Composite signals involving both APs and VPs can be evoked by
Pathways of signal transmission
Electrical signals can propagate over short distances via plasmodesmata and electrical coupling via plasmodesmata was shown previously in various species such as Nitella (Spanswick and Costerton, 1967), Elodea and Avena (Spanswick, 1972). While plasmodesmata are relays in the signalling network between neighbouring cells, long distances can only be bridged rapidly via low resistance connections extending throughout the whole plant such as the elongated sieve tubes. Due to the relatively large
Long-distance signalling and plant water status
In response to environmental changes higher plants permanently adjust their metabolic and physiologic processes. External factors such as light intensity, temperature and humidity continuously affect plant water relations and upholding of water status is essential for plant growth. It requires coordinated modulation to regulate water uptake, movement and release via stomata. Regarding the question of how information of plant water status is transmitted to remote sites we will deal with current
Light-induced long-distance signalling
Electrical signals have been found to be induced by variations in light intensity, whereas their role in intra- and intercellular signalling are still not completely understood (Volkov and Ranatunga, 2006, Marten et al., 2010). In fact, dark–light transitions trigger membrane potential changes at the leaf mesophyll (Spalding et al., 1992, Elzenga et al., 1995, Shabala and Newman, 1999) as well as at the root level (Wegner and Zimmermann, 1998, Shabala et al., 2009), thereby modulating ion
Long-distance signalling and photosynthesis
Alteration of leaf gas exchange and in particular of photosynthetic activity in response to electrical signals have been observed in a few studies to date, primarily as a result of heat and wounding stimuli but also after re-irrigation of drought stressed plants (see Table 1). However, our current knowledge about the direct or indirect effect of electrical signals on photosynthesis is still limited. Besides an immediate and transient suppression of photosynthetic activity, the pattern of
Long-distance signalling and respiration
Apart from the electrical signal induced suppression of AN it has been questioned whether (photo-) respiratory processes were enhanced during this drop or not. Moreover, the drop of AN did not always match with reductions in photosynthetic electron transport rate or ΦPSII, thus leading to the assumption that (photo-) respiratory processes were enhanced as a result of electrical signals. A current study on M. pudica provides some evidence for an increase of respiratory CO2 release during
Long-distance signalling in relation to electrical oscillations
Since 1962 when Scott and Martin (Scott and Martin, 1962) discovered bioelectric fields in bean roots, the significant role of electric oscillations in plant life, particularly in root growth and circumnutations was shown (Shabala et al., 1997, Shabala and Newman, 1997). Endogenous currents of roots have been measured in several species, showing that growing plant roots drive ion currents through themselves. Importantly, ultradian oscillations in plant roots have physiological implications and
Concluding remarks
Physiological and molecular plant responses to electrical signals have been shown in several plant species to date, suggesting an important role of electrical signalling in plant defense to abiotic (and biotic) stresses. Electrical signals as derived from a number of environmental stimuli can travel at high speed over long distances throughout the entire plant. Thus, these signals allow to respond quickly to stresses as for instance wounding or re-watering. Moreover, transmission of AP over the
Acknowledgements
JF acknowledges funding from project BFU2011-23294. The authors acknowledge the constructive comments by two anonymous reviewers on an earlier version of this manuscript.
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2022, Advances in Botanical ResearchCitation Excerpt :Although the question of how hydraulic waves are linked to electric, ROS, and ABA remain to be answered, it was proposed that different mechano-sensitive channels could sense hydraulic waves and convert them into Ca2 + signals (Basu & Haswell, 2017). Within the last decade, the research focus on plant electrophysiology has shifted from the short-distance to long-distance or systemic signaling as signaling pathway has been formed in the phloem, allowing plants to communicate over long distances (Galle, Lautner, Flexas, & Fromm, 2015). Contrast to chemical signals electrical signals can transmit signal over long distances with higher speed: most of the action potentials (APs) in plant investigated so far revealed velocities ranging from 0.005 to 0.2 m s− 1 (Fromm & Lautner, 2007).