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Electrogenic biofilms, which have attracted considerable attention in simultaneous wastewater treatment and energy recovery in bioelectrochemical systems, are regulated by chemical communication and potassium channel-mediated electrical signaling. However, how these two communication pathways interact with each other has not been thoroughly investigated. This study first explored the roles of chemical communication, including intracellular bis-(3'-5')-cyclic dimeric guanosine monophosphate (c-di-GMP) and extracellular N-acyl-homoserine lactone (AHL)-mediated quorum sensing, in electrogenic biofilm formation through an integrated analysis of transcriptomics and metabolomics. Electrical signaling disruption inhibited the formation and electroactivity of Geobacter sulfurreducens biofilm, which was mainly ascribed to the reduction in biofilm viability and extracellular protein/polysaccharide ratio. The upregulation of expression levels of genes encoding c-di-GMP and AHL synthesis by transcriptomic analysis, and the increased secretion of N-butanoyl-L-homoserine lactone by metabolomic analysis confirmed the enhancement of chemical communication under electrical signaling disruption, thus indicating a compensatory mechanism among different signaling pathways. Furthermore, protein-protein interaction network showed the convergence of different signaling pathways, with c-di-GMP-related genes acting as central bridges. This study highlights the interaction of different signaling pathways, especially the resilience of c-di-GMP signaling to adverse external stresses, thereby laying the foundation for facilitating electrogenic biofilm formation under adverse conditions in practical applications.

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Leaf wounding triggers rapid long-range electrical signaling that initiates systemic defense responses to protect the plants from further attack. In Arabidopsis, this process largely depends on clade three GLUTAMATE RECEPTOR-LIKE (GLR) genes GLR3.3 and GLR3.6. In the cellular context, phloem sieve elements and xylem contact cells where GLRs were mostly present are implicated in the signaling events. In spite of that, the spatial requirements of different leaf cell types for leaf-to-leaf signaling remain poorly investigated. In this study, we dissected cell-type-specific long-distance wound signaling mediated by GLR3s and showed that phloem companion cells are critical in shaping the functions of GLR3.3 and GLR3.6 in the signaling pathway. GLR3.3-mediated response is phloem-specific, during which, GLR3.3 has to be renewed from companion cells to allow its function in sieve elements. GLR3.6 functions dually in ectopic phloem companion cells, in addition to xylem contact cells. Furthermore, the action of GLR3.6 in phloem is independent of its paralog GLR3.3 and probably requires synthesis of GLR3.6 from xylem contact cells. Overall, our work highlights that the phloem companion cell is crucial for both GLRs in controlling leaf-to-leaf electrical signaling.

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Jasmonic acid (JA) plays crucial functions in plant stress response, and the synergistic interaction between JA and abscisic acid (ABA) signaling is implicated to help plants adapt to environmental challenges, whereas the underlying molecular mechanism still needs to be revealed. Here, we report that OsJAZ10, a repressor in the JA signaling, represses rice drought tolerance via inhibition of JA and ABA biosynthesis. Function loss of OsJAZ10 markedly enhances, while overexpression of OsJAZ10ΔJas reduces rice drought tolerance. The osjaz10 mutant is more sensitive to exogenous ABA and MeJA, and produces higher levels of ABA and JA after drought treatment, indicating OsJAZ10 represses the biosynthesis of these two hormones. Mechanistic study demonstrated that OsJAZ10 physically interacts with OsMYC2. Transient transcriptional regulation assays showed that OsMYC2 activates the expression of ABA-biosynthetic gene OsNCED2, JA-biosynthetic gene OsAOC, and drought-responsive genes OsRAB21 and OsLEA3, while OsJAZ10 prevents OsMYC2 transactivation of these genes. Further, the electrophoretic mobility shift assay (EMSA) confirmed that OsMYC2 directly binds to the promoters of OsNCED2 and OsRAB21. Electrical activity has been proposed to activate JA biosynthesis. Interestingly, OsJAZ10 inhibits the propagation of osmotic stress-elicited systemic electrical signals, indicated by the significantly increased PEG-elicited slow wave potentials (SWPs) in osjaz10 mutant, which is in accordance with the elevated JA levels. Collectively, our findings establish that OsJAZ10 functions as a negative regulator in rice drought tolerance by repressing JA and ABA biosynthesis, and reveal an important mechanism that plants integrate electrical events with hormone signaling to enhance the adaption to environmental stress.

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Spinal cord injury (SCI), caused by significant physical trauma, as well as other pathological conditions, results in electrical signaling disruption and loss of bodily functional control below the injury site. Conductive biomaterials have been considered a promising approach for treating SCI, owing to their ability to restore electrical connections between intact spinal cord portions across the injury site. In this study, we evaluated the ability of a conductive hydrogel, poly-3-amino-4-methoxybenzoic acid-gelatin (PAMB-G), to restore electrical signaling and improve neuronal regeneration in a rat SCI model generated using the compression clip method. Gelatin or PAMB-G was injected at the SCI site, yielding three groups: Control (saline), Gelatin, and PAMB-G. During the 8-week study, PAMB-G, compared to Control, had significantly lower proinflammatory factor expression, such as for tumor necrosis factor -α (0.388 ± 0.276 for PAMB-G vs. 1.027 ± 0.431 for Control) and monocyte chemoattractant protein (MCP)-1 (0.443 ± 0.201 for PAMB-G vs. 1.662 ± 0.912 for Control). In addition, PAMB-G had lower astrocyte and microglia numbers (35.75 ± 4.349 and 40.75 ± 7.890, respectively) compared to Control (50.75 ± 6.5 and 64.75 ± 10.72) and Gelatin (48.75 ± 4.787 and 71.75 ± 7.411). PAMB-G-treated rats also had significantly greater preservation and regeneration of remaining intact neuronal tissue (0.523 ± 0.059% mean white matter in PAMB-G vs 0.377 ± 0.044% in Control and 0.385 ± 0.051% in Gelatin) caused by reduced apoptosis and increased neuronal growth-associated gene expression. All these processes stemmed from PAMB-G facilitating increased electrical signaling conduction, leading to locomotive functional improvements, in the form of increased Basso-Beattie-Bresnahan scores and steeper angles in the slope test (76.667 ± 5.164 for PAMB-G, vs. 59.167 ± 4.916 for Control and 58.333 ± 4.082 for Gelatin), as well as reduced gastrocnemius muscle atrophy (0.345 ± 0.085 for PAMB-G, vs. 0.244 ± 0.021 for Control and 0.210 ± 0.058 for Gelatin). In conclusion, PAMB-G injection post-SCI resulted in improved electrical signaling conduction, which contributed to lowered inflammation and apoptosis, increased neuronal growth, and greater bodily functional control, suggesting its potential as a viable treatment for SCI.

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The functioning of the human heart relies on complex electrical and communication systems that coordinate cardiac contractions and sustain rhythmicity. One of the key players contributing to this intricate system is the KIR2.1 potassium ion channel, which is encoded by the KCNJ2 gene. KIR2.1 channels exhibit abundant expression in both ventricular myocytes and Purkinje fibers, exerting an important role in maintaining the balance of intracellular potassium ion levels within the heart. And by stabilizing the resting membrane potential and contributing to action potential repolarization, these channels have an important role in cardiac excitability also. Either gain- or loss-of-function mutations, but also acquired impairments of their function, are implicated in the pathogenesis of diverse types of cardiac arrhythmias. In this review, we aim to elucidate the system functions of KIR2.1 channels related to cellular electrical signaling, communication, and their contributions to cardiovascular disease. Based on this knowledge, we will discuss existing and new pharmacological avenues to modulate their function.

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Higher plants efficiently orchestrate rapid systemic responses to diverse environmental stimuli through electric signaling. This review explores the mechanisms underlying two main types of electric signals in plants, action potentials (APs) and slow wave potentials (SWPs), and how new discoveries challenge conventional neurophysiological paradigms traditionally forming their theoretical foundations. Animal APs are biophysically well-defined, whereas plant APs are often classified based on their shape, lacking thorough characterization. SWPs are depolarizing electric signals deviating from this shape, leading to an oversimplified classification of plant electric signals. Indeed, investigating the generation and propagation of plant APs and SWPs showcases a complex interplay of mechanisms that sustain self-propagating signals and internally propagating stimuli, resulting in membrane depolarization, cytosolic calcium increase, and alterations in reactive oxygen species and pH. A holistic understanding of plant electric signaling will rely on unraveling the network of ion-conducting proteins, signaling molecules, and mechanisms for signal generation and propagation.

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Bioelectronic medicine is a multidisciplinary field that combines molecular medicine, neurology, engineering, and computer science to design devices for diagnosing and treating diseases. The advancements in bioelectronic medicine can improve the precision and personalization of illness treatment. Bioelectronic medicine can produce, suppress, and measure electrical activity in excitable tissue. Bioelectronic devices modify specific neural circuits using electrons rather than pharmaceuticals and use bioelectronic processes to regulate the biological processes underlining various diseases. This promotes the potential to address the underlying causes of illnesses, reduce adverse effects, and lower costs compared to conventional medication. The current review presents different important aspects of bioelectronic medicines with recent advancements. The area of bioelectronic medicine has a lot of potential for treating diseases, enabling non-invasive therapeutic intervention by regulating brain impulses. Bioelectronic medicine uses electricity to control biological processes, treat illnesses, or regain lost capability. These new classes of medicines are designed by the technological developments in the detection and regulation of electrical signaling methods in the nervous system. Peripheral nervous system regulates a wide range of processes in chronic diseases; it involves implanting small devices onto specific peripheral nerves, which read and regulate the brain signaling patterns to achieve therapeutic effects specific to the signal capacity of a particular organ. The potential for bioelectronic medicine field is vast, as it investigates for treatment of various diseases, including rheumatoid arthritis, diabetes, hypertension, paralysis, chronic illnesses, blindness, etc.

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Action potentials of plant cells are engaged in the regulation of many cell processes, including photosynthesis and cytoplasmic streaming. Excitable cells of characean algae submerged in a medium with an elevated K+ content are capable of generating hyperpolarizing electrical responses. These active responses of plasma membrane originate upon the passage of inward electric current comparable in strength to natural currents circulating in illuminated Chara internodes. So far, it remained unknown whether the hyperpolarizing electrical signals in Chara affect the photosynthetic activity. Here, we showed that the negative shift of cell membrane potential, which drives K+ influx into the cytoplasm, is accompanied by a delayed decrease in the actual yield of chlorophyll fluorescence F' and the maximal fluorescence yield Fm' under low background light (12.5 µmol m-2 s-1). The transient changes in F' and Fm' were evident only under illumination, which suggests their close relation to the photosynthetic energy conversion in chloroplasts. Passing the inward current caused an increase in pH at the cell surface (pHo), which reflected high H+/OH- conductance of the plasmalemma and indicated a decrease in cytoplasmic pH due to the H+ entry into the cell. The shifts in pHo arising in response to the first hyperpolarizing pulse disappeared upon repeated stimulation, thus indicating the long-term inactivation of plasmalemmal H+/OH- conductance. Suppression of plasmalemmal H+ fluxes did not abolish the hyperpolarizing responses and the analyzed changes in chlorophyll fluorescence. These results suggest that K+ fluxes between the extracellular medium, cytoplasm, and stroma are involved in the functional changes of chloroplasts reflected by transients of F' and Fm'.

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Electrogenic biofilms in microbial electrochemical systems have played significant roles in simultaneous wastewater treatment and energy recovery owing to their unique extracellular electron transfer. Their formation has been shown to be regulated by electrical and chemical communication, but the interaction between these signal communication pathways has not been studied. This research investigated the coordination between intracellular c-di-GMP signaling and reinforced quorum sensing with or without exogenous HSL (a common quorum sensing molecule), on the formation of mixed-cultured electrogenic biofilm under electrical signaling disruption by tetraethylammonium (TEA, a broad-range potassium channel blocker). Intracellular c-di-GMP was spontaneously reinforced in response to TEA stress, and metagenomic analysis revealed that the dominant DGC (the genes for producing c-di-GMP) induced the eventual biofilm formation by mediating exopolysaccharide synthesis. Meanwhile, reinforced quorum sensing by exogenous HSL could also benefit the biofilm restoration, however, it alleviated the TEA-induced communication stress, resulting in the weakening of c-di-GMP dominance. Interestingly, suppressing electrical communication with or without HSL addition both induced selective enrichment of Geobacter of 85.5% or 30.1% respectively. Functional contribution analysis revealed the significant roles of Geobacter and Thauera in c-di-GMP signaling, especially Thauera in resistance to TEA stress. This study proposed a potential strategy for electrogenic biofilm regulation from the perspectives of cell-to-cell communication.

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Signaling pathways in plant cells often comprise electrical phenomena developing at the plasma membrane. The action potentials in excitable plants like characean algae have a marked influence on photosynthetic electron transport and CO2 assimilation. The internodal cells of Characeae can also generate active electrical signals of a different type. The so called hyperpolarizing response develops under the passage of electric current whose strength is comparable to physiological currents circulating between nonuniform cell regions. The plasma membrane hyperpolarization is involved in multiple physiological events in aquatic and terrestrial plants. The hyperpolarizing response may represent an unexplored tool for studying the plasma membrane-chloroplast interactions in vivo. This study shows that the hyperpolarizing response of Chara australis internodes whose plasmalemma was preliminary converted into the K+-conductive state induces transient changes in maximal (Fm') and actual (F') fluorescence yields of chloroplasts in vivo. These fluorescence transients were light dependent, suggesting their relation to photosynthetic electron and H+ transport. The cell hyperpolarization promoted H+ influx that was inactivated after a single electric stimulus. The results indicate that the plasma membrane hyperpolarization drives transmembrane ion fluxes and modifies the ionic composition of cytoplasm, which indirectly (via envelope transporters) affects the pH of chloroplast stroma and chlorophyll fluorescence. Remarkably, the functioning of envelope ion transporters can be revealed in short-term experiments in vivo, without growing plants on solutions with various mineral compositions.

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Recent studies have shown that bacterial membrane potential is dynamic and plays signaling roles. Yet, little is still known about the mechanisms of membrane potential dynamics regulation-owing to a scarcity of appropriate research tools. Optical modulation of bacterial membrane potential could fill this gap and provide a new approach for studying and controlling bacterial physiology and electrical signaling. Here, the authors show that a membrane-targeted azobenzene (Ziapin2) can be used to photo-modulate the membrane potential in cells of the Gram-positive bacterium Bacillus subtilis. It is found that upon exposure to blue-green light (λ = 470 nm), isomerization of Ziapin2 in the bacteria membrane induces hyperpolarization of the potential. To investigate the origin of this phenomenon, ion-channel-deletion strains and ion channel blockers are examined. The authors found that in presence of the chloride channel blocker idanyloxyacetic acid-94 (IAA-94) or in absence of KtrAB potassium transporter, the hyperpolarization response is attenuated. These results reveal that the Ziapin2 isomerization can induce ion channel opening in the bacterial membrane and suggest that Ziapin2 can be used for studying and controlling bacterial electrical signaling. This new optical tool could contribute to better understand various microbial phenomena, such as biofilm electric signaling and antimicrobial resistance.

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Glutamate receptor-like (GLR) 3.3 and 3.6 proteins are required for mediating wound-induced leaf-to-leaf electrical signaling. In the previous study, we found that the carboxy-terminal tail of GLR3.3 contains key residues that are indispensable for its action in electrical signaling. In the present work, we generated plants that expressed the truncated C-tail fraction of GLR3.3. To our expectation, the truncated C-tail itself was not functional in propagating leaf-to-leaf signals. However, we identified that the C-tail-mVENUS fusion proteins had dual localization patterns in sieve elements and companion cells. In companion cells, the fusion proteins overlapped largely with the nucleus. We speculated that a possible nuclear localization signal is present in the C-tail of GLR3.3, paralleling the C-tails of the ionotropic glutamate receptors in animal cells. Our further findings on the C-tail of GLR3.3 open up new possibilities for the regulatory roles of the C-tails to GLR proteins.

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Arabidopsis Clade 3 GLUTAMATE RECEPTOR-LIKEs (GLRs) are primary players in wound-induced systemic signaling. Previous studies focused on dissecting their ligand-activated channel properties involving extracellular and membrane-related domains. Here, we report that the carboxy-terminal tails (C-tails) of GLRs contain key elements controlling their function in wound signaling. GLR3.3 without its C-tail failed to rescue the glr3.3a mutant. We carried out a yeast two-hybrid screen to identify the C-tail interactors. We performed functional studies of the interactor by measuring electrical signals and defense responses. Then we mapped their binding sites and evaluated the impact of the sites on GLR functions. IMPAIRED SUCROSE INDUCTION 1 (ISI1) interacted with GLR3.3. Enhanced electrical activity was detected in reduced function isi1 mutants in a GLR3.3-dependent manner. isi1 mutants were slightly more resistant to insect feeding than the wild-type. Furthermore, a triresidue motif RFL in the GLR3.3 C-tail binds to ISI1 in yeast. Finally, we demonstrated that FL residues were conserved across GLRs and functionally required. Our study provides new insights into the functions of GLR C-tails, reveals parallels with the ionotropic glutamate receptor regulation in animal cells, and may enable rational design of strategies to engineer GLRs for future practical applications.

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Since the 19th century, it has been known that the carnivorous Venus flytrap is electrically excitable. Nevertheless, the mechanism and the molecular entities of the flytrap action potential (AP) remain unknown. When entering the electrically excitable stage, the trap expressed a characteristic inventory of ion transporters, among which the increase in glutamate receptor GLR3.6 RNA was most pronounced. Trigger hair stimulation or glutamate application evoked an AP and a cytoplasmic Ca2+ transient that both propagated at the same speed from the site of induction along the entire trap lobe surface. A priming Ca2+ moiety entering the cytoplasm in the context of the AP was further potentiated by an organelle-localized calcium-induced calcium release (CICR)-like system prolonging the Ca2+ signal. While the Ca2+ transient persisted, SKOR K+ channels and AHA H+-ATPases repolarized the AP already. By counting the number of APs and long-lasting Ca2+ transients, the trap directs the different steps in the carnivorous plant's hunting cycle. VIDEO ABSTRACT.

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Potassium (K+)-channel-based electrical signaling can coordinate microbial actions at a distance that provides an evolutionary advantage to cell communities. Electroactive cells are usually cultured surrounded by an electric field which provided stronger electrical signaling than the K+-mediated electrical signaling. Whether the K+ signaling also plays a role in coordinating the behavior of electroactive microorganisms has not been accurately demonstrated. Thus, we constructed a K+-channel-deficient strain ΔgsuK of Geobacter sulfurreducens to directly investigate roles of K+ signaling in electroactive biofilm formation for the first time. The ΔgsuK strain exhibited significantly inferior biofilm formation (i.e., biomass, thickness and component) and consequently showed weaker electrical performance (i.e., start-up time, current output, electrochemical catalytic behavior and charge transfer resistance) than the wild-type strain. Individual electric generation capacity and the expression of genes involved in biofilm formation and electrical performance in the single cell did not significantly change with the deletion of gsuK, indicating that K+ signaling indeed influenced the recruiting behavior of planktonic cell but not the functioning of the single cell related to biofilm formation or electric generation. This study is intended to provide an in-depth understanding of electroactive biofilm formation and serve as a basis for optimizing its electrical performance via strengthening the recruitment behavior.

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Rapid systemic signals travel within the first seconds and minutes after herbivore infestation to mount defense responses in distal tissues. Recent studies have revealed that wound-induced hydraulic pressure changes play an important role in systemic electrical signaling and subsequent calcium and reactive oxygen species waves. These insights raise new questions about signal specificity, the role of insect feeding guild and feeding style and the impact on longer term plant defenses. Here, we integrate the current molecular understanding of wound-induced rapid systemic signaling in the framework of insect-plant interactions.

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PURPOSE: The purpose of this study was to examine the effect of plasma rich in growth factors (PRGFs) under blue light conditions in an in vivo model of retinal degeneration. METHODS: Male Wistar rats were exposed to dark/blue light conditions for 9 days. On day 7, right eyes were injected with saline and left eyes with PRGF. Electroretinography (ERG) and intraocular pressure (IoP) measurements were performed before and after the experiment. After sacrifice, retinal samples were collected. Hematoxylin and eosin staining was performed to analyze the structure of retinal sections. Immunofluorescence for brain-specific homeobox/POU domain protein 3A (Brn3a), choline acetyltransferase (ChAT), rhodopsin, heme oxygenase-1 (HO-1), and glial fibrillary acidic protein (GFAP) was performed to study the retinal conditions. RESULTS: Retinal signaling measured by ERG was reduced by blue light and recovered with PRGF; however, IoP measurements did not show significant differences among treatments. Blue light reduced the expression for Brn3a, ChAT, and rhodopsin. Treatment with PRGF showed a recovery in their expressions. HO-1 and GFAP results showed that blue light increased their expression but the use of PRGF reduced the effect of light. CONCLUSIONS: Blue light causes retinal degeneration. PRGF mitigated the injury, restoring the functionality of these cells and maintaining the tissue integrity.

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In plants, environmental stressors trigger plasma membrane depolarizations. Being electrically interconnected via plasmodesmata, proper functional dissection of electrical signaling by electrophysiology is basically impossible. The green alga Chlamydomonas reinhardtii evolved blue light-excited channelrhodopsins (ChR1, 2) to navigate. When expressed in excitable nerve and muscle cells, ChRs can be used to control the membrane potential via illumination. In Arabidopsis plants, we used the algal ChR2-light switches as tools to stimulate plasmodesmata-interconnected photosynthetic cell networks by blue light and monitor the subsequent plasma membrane electrical responses. Blue-dependent stimulations of ChR2 expressing mesophyll cells, resting around -160 to -180 mV, reproducibly depolarized the membrane potential by 95 mV on average. Following excitation, mesophyll cells recovered their prestimulus potential not without transiently passing a hyperpolarization state. By combining optogenetics with voltage-sensing microelectrodes, we demonstrate that plant plasma membrane AHA-type H+-ATPase governs the gross repolarization process. AHA2 protein biochemistry and functional expression analysis in Xenopus oocytes indicates that the capacity of this H+ pump to recharge the membrane potential is rooted in its voltage- and pH-dependent functional anatomy. Thus, ChR2 optogenetics appears well suited to noninvasively expose plant cells to signal specific depolarization signatures. From the responses we learn about the molecular processes, plants employ to channel stress-associated membrane excitations into physiological responses.

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Bacteria in biofilms are able to utilize potassium ion channel-mediated electrical signaling to achieve cell-cell communication. However, it remains unclear whether these signals play a role in Geobacter sp. when surrounded by an intense electric field. This study used a potassium channel blocker (tetraethylammonium, TEA) that interfered with the release of K+ but not bacterial growth to demonstrate that potassium ion channel-mediated electrical signaling affected the formation and electroactivity of Geobacter sulfurreducens. The results showed that 5 mM TEA slowed the formation of Geobacter sulfurreducens biofilm, and the current density was ~50% lower than in the control. The electrochemical analyses showed that the electroactivity of the biofilms with TEA addition was inferior. In particular, the micrometer- scale biofilm with TEA exhibited fewer high current peaks, and the species of outermost groups that participated in the electron transfer in Geobacter sulfurreducens biofilms was different from the control. This work provides initial evidence to reveal the role of potassium channels in Geobacter sulfurreducens electroactive biofilms.

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A variation potential (VP) is an electrical signal unique to plants that occurs in response to wounding or flaming. The propagation mechanism itself, however, is known not to be electrical. Here we examine the hypothesis that VP transmission occurs via the transport of a chemical agent in the xylem. We assume the electrical signal is generated locally by the activation of an ion channel at the plasma membrane of cells adjacent to the xylem. We work on the assumption that the ion channels are triggered when the chemical concentration exceeds a threshold value. We use numerical computations to demonstrate the combined effect of advection and diffusion on chemical transport in a tube flow, and propose shear-enhanced Taylor-Aris dispersion as a candidate mechanism to explain VP rates observed in experiments.