Frontiers | Electrical Signaling, Photosynthesis and Systemic Acquired Acclimation | Physiology
https://www.frontiersin.org/articles/10.3389/fphys.2017.00684/full
One of the most critical functions of each organism is a selective sensing of the environment. Ordered flow of electrical currents between cells and organs allows a given organism for universal, rapid, and efficient communication of the external changes. The steady state of plasma membrane electrical potential defines the electric field of each cell. However, external factors induce rapid changes in the membrane potential, and these changes can be transduced in the form of waves: (1) the movement of ions across of plasma membrane and organelle membranes is a driving mechanism for wavy changes of the electric potential, which propagate along the membrane of one cell or organelle, and in turn, determine intracellular electrical activity of the cell and adjust its local metabolism; (2) the short-distance intercellular electrical signaling to maintain specific behavior of the group of the cells; and (3) the long-distance intercellular electrical signal from the site of stimulus perception to distal organs, where it triggers plant-wide responses.
Despite specific differences, the network of electrical signaling is present at almost each level of complexity, from unicellular bacteria and fungi to multi-cellular organisms like plants and animals. In unicellular organisms, cell-to-cell electrical signaling plays a key role in the reproduction and coordination of colony behavior. For example, bacteria Bacillus subtilis generates electrical signals mediated by potassium ion channels to direct motility in a biofilm of their own community, to stop reproducing bacteria on colony periphery, and to leave core cells with a sufficient nutrient supply (Humphries et al., 2017). A polarization and dynamic coordination of the electrical signals underlies also the ability of plant cell groups to proliferation, proper morphogenesis, regeneration and orientation (Filek et al., 2002; Yan et al., 2009; Nakajima et al., 2015). Similarly, the bioelectric network of each cell and the bioelectric gradients serve as a kind of pattern memory of animal tissues and organs (Durant et al., 2017). The environmental signals, physical (e.g., light, temperature, humidity, electric fields, wounding), chemical (e.g., nutrients and various substances), and biological (e.g., symbiosis, pathogenesis), can alter local and systemic electrical responses and modify cell division and growth. However, once the connectivity patterns of electrical signaling are disrupted, organisms can no longer follow appropriate morphogenetic and functional pathways (Szechyńska-Hebda et al., 2010; Karpiński et al., 2013; Nakajima et al., 2015).
Probably the most spectacular system involving electrical signaling is the organism-to-organism signaling. Among unicellular bacteria, electrical communication enables cross-species interactions. Pseudomonas aeruginosa cells become attracted to the electrical signal released by the B. subtilis biofilm (Humphries et al., 2017). In the plant kingdom, the role of electrical signals in organism-to-organism interactions is still highly speculative and largely phenomenological, but there are several pioneering examples of how plant creates and responds to electrical fields. Flowers exhibit differences in the pattern of the electric field, which can be discriminated by bumblebees. When the bumblebee lands on the flower, the electric field changes within seconds and this facilitates rapid and dynamic signaling between flowers and their pollinators (Clarke et al., 2013). Arabidopsis thaliana respond to biotic stress agents: Spodoptera littoralis, Myzus persicae, Pseudomonas syringae with plasma membrane depolarization and it was correlated to specific regulation of the wide range of defense genes (Bricchi et al., 2012). Similarly, transition zone of the roots is an area with unusually high levels of electrical activity (Baluška, 2010; Baluška and Mancuso, 2013), and it makes the root apex zone an attractive target of pathogenic and symbiotic organisms (Brenner et al., 2006). There is also the possibility that electric field generated by each growing root might allow electrical signaling among roots of the same or another plant (Schenk and Seabloom, 2010; Garzon and Keijzer, 2011). However, the most extremal example among multicellular organisms, is the usage of electric organs by fish in murky environment to navigate, recognize the species and sex, and as a shocking defense (Gallant et al., 2014). The electric field generated for predatory purposes is up to 500 V or higher