Environmental stimuli and physiological responses: The current view on electrical signalling

https://doi.org/10.1016/j.envexpbot.2014.06.013Get rights and content

Highlights

  • Environmental cues like heat, cold and wounding induce electrical signals.

  • Electrical signals can travel over long distances across organs and affect several physiological processes.

  • Long distance signals modulate plant water status, photosynthesis and respiration.

Abstract

Electrical signals have been studied in numerous species so far. It appears that two main types of such signals occur in plants, rapid action potentials (APs) and slower variation potentials (VPs). While APs are generally evoked by non-invasive stimuli and follow the all-or-nothing principle as in neurons, VPs are mostly triggered by wounding and do not follow the all-or-nothing law. They are correlated to the stimulus strength and last longer than APs. The transmission of both, APs and VPs, occurs via the phloem over long distances and via plasmodesmata over short distances from cell to cell. Regarding physiological functions of electrical signals, numerous examples exist. They regulate rapid leaf movements in order to catch insects and for instance, affect nutrient uptake, gene expression and phloem transport. Recently, it was shown that apart from hydraulic signals, electric signals also play a significant role in root-to-shoot communication of drought-stressed plants. Re-irrigation of plants after soil drying initiates rapid hydraulic as well as electric signalling which affects the gas exchange of leaves. In addition, evidence was found for a link between electrical signals and photosynthesis as well as respiration. Wound-induced VPs cause a transient suppression in photosynthetic activity and an increase in respiratory CO2 release. The results led us to conclude that different stimulation types trigger characteristic electrical signals each with specific influence on physiological processes.

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.

References (104)

  • M.E. Alves et al.

    The role of ion fluxes in polarized cell growth and morphogenesis: the pollen tube as an experimental paradigm

    Int. J. Dev. Biol.

    (2009)
  • L. Bai et al.

    Plasma membrane-associated proline-rich extension-like receptor kinase 4, a novel regulator of Ca2+ signalling, is required for abscisic acid responses in Arabidopsis thaliana

    Plant J.

    (2009)
  • L.C. Boavida et al.

    Gametophyte interaction and sexual reproduction: how plants make a zygote

    Int. J. Dev. Biol.

    (2005)
  • M.J.P. Canny

    Mass transfer

  • O. Chazen et al.

    Hydraulic signals from the roots and rapid cell-wall hardening in growing maize (Zea mays L.) leaves are primary responses to polyethylene glycol-induced water deficits

    Plant Physiol.

    (1994)
  • W.-G. Choi et al.

    Salt stress-induced Ca2+ waves are associated with rapid long-distance root-to-shoot signaling in plants

    PNAS

    (2014)
  • A. Christmann et al.

    A hydraulic signal in root-to-shoot signalling of water shortage

    Plant J.

    (2007)
  • E. Davies

    New functions for electrical signals in plants

    New Phytol.

    (2004)
  • E. Davies et al.

    Electrical signals, the cytoskeleton and gene expression: a hypothesis on the coherence of the cellular responses to environmental insult

  • E. Davies et al.

    Wounding inhibits protein synthesis yet stimulates polysome formation in aged, excised pea epicotyls

    Plant Cell Physiol.

    (1986)
  • H. Dziubinska et al.

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

    Physiol. Plant.

    (1989)
  • J.T.M. Elzenga et al.

    Light-induced membrane-potential changes of epidermal and mesophyll-cells in growing leaves of Pisum sativum

    Planta

    (1995)
  • J.A. Feijo

    The mathematics of sexual attraction

    J. Biol.

    (2010)
  • H.H. Felle et al.

    Systemic signalling in barley through action potentials

    Planta

    (2007)
  • J. Fisahn et al.

    Analysis of a transient increase of cytosoloc Ca2+ during the action potential of higher plants with high temporal resolution: requirement of Ca2+ transients for induction of jasmonic acis synthesis and PINII gene expression

    Plant Cell Physiol.

    (2004)
  • Y. Forterre et al.

    How the Venus flytrap snaps

    Nature

    (2005)
  • J. Fromm et al.

    Transport processes in stimulated and non-stimulated leaves of Mimosa pudica

    Trees – Struct. Funct.

    (1988)
  • J. Fromm

    Control of phloem unloading by action potentials in Mimosa

    Physiol. Plant.

    (1991)
  • J. Fromm et al.

    Characteristics of action potentials in willow (Salix viminalis L.)

    J. Exp. Bot.

    (1993)
  • J. Fromm et al.

    Action potentials in maize sieve tubes change phloem translocation

    J. Exp. Bot.

    (1994)
  • J. Fromm et al.

    The biochemical response of electrical signaling in the reproductive system of Hibiscus plants

    Plant Physiol.

    (1995)
  • J. Fromm et al.

    Characteristics and functions of phloem-transmitted electrical signals in higher plants

  • 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 ist physiological responses in the maize leaf

    Front. Plant Sci.

    (2013)
  • A.C.U. Furch et al.

    Ca2+-mediated remote control of reversible sieve tube occlusion in Vicia faba

    J. Exp. Bot.

    (2007)
  • A.C.U. Furch et al.

    Sieve element Ca2+ channels as relay stations between remote stimulus and sieve tube occlusion

    Plant Cell

    (2009)
  • A.C.U. Furch et al.

    Remote-controlled stop of mass flow by biphasic occlusion in Cucurbita maxima

    J. Exp. Bot.

    (2010)
  • A. Gallé et al.

    Photosynthetic responses of soybean (Glycine max L.) to heat-induced electrical signalling are predominantly governed by modifications of mesophyll conductance for CO2

    Plant Cell Environ.

    (2013)
  • T.E.E. Grams et al.

    Distinct roles of electric and hydraulic signals on the reaction of leaf gas exchange upon re-irrigation in Zea mays

    Plant Cell Environ.

    (2007)
  • 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)
  • J.B. Hafke et al.

    Forisome dispersion in Vicia faba is triggered by Ca2+ hotspots created by concerted action of diverse Ca2+ channels in sieve elements

    Plant Signal. Behav.

    (2009)
  • T. Hayama et al.

    Participation of Ca2+ in cessation of cytoplasmic streaming induced by membrane excitation in Characeae internodal cells

    Protoplasma

    (1979)
  • R. Hedrich

    Ion channels in plants

    Physiol. Rev.

    (2012)
  • O. Herde et al.

    Proteinase inhibitor II gene expression induced by electrical stimulation and control of photosynthetic activity in tomato plants

    Plant Cell Physiol.

    (1995)
  • O. Herde et al.

    Localized wounding by heat initiates the accumulation of proteinase inhibitor II in abscisic acid deficient tomato plants by triggering jasmonic acid biosynthesis

    Plant Physiol.

    (1996)
  • O. Herde et al.

    Effects of mechanical wounding, current application and heat treatment on chlorophyll fluorescence and pigment composition in tomato plants

    Physiol. Plant.

    (1999)
  • V. Hlavackova et al.

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

    Planta

    (2006)
  • D. Hodick et al.

    On the mechanism of trap closure of Venus flytrap (Dionaea muscipula Ellis.)

    Planta

    (1989)
  • G. Hörmann

    Studien über die Protoplasmaströmung bei den Characaean

    (1898)
  • N.M. Holbrook et al.

    Stomatal control in tomato with ABA-deficient roots: response of grafted plants to soil drying

    J. Exp. Bot.

    (2002)
  • Cited by (93)

    • Do plants pay attention? A possible phenomenological-empirical approach

      2022, Progress in Biophysics and Molecular Biology
    • Root-borne signals and their control of guard cell operation under saline conditions: The role of root signals in stomata regulation

      2022, Advances in Botanical Research
      Citation 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).

    View all citing articles on Scopus
    View full text