Bioelectricity

Polar growth and guidance of pollen tubes (PTs) is regulated by chemical and electrical signaling cues. Central regulators controlling cellular protrusion of PTs tip-focused Ca²⁺ and H⁺ cytosolic gradients and ion fluxes depend, but also feedback, on membrane voltage (V_m). However, the functional relationship between V_m, Ca²⁺, and H⁺ dynamics is largely unclear. We carried out parallel live-cell Ca²⁺ and H⁺-imaging together with V_m recordings followed by cross-correlation analysis to study their interconnection in tobacco PTs. Upon electrode impalement at the tip or shank, PT growth ceased but sustained oscillatory behavior of all three signals continued and remained mostly in phase, although shifted in time. The Ca²⁺ oscillations were largely restricted to the apex, temporally leading the H⁺ increases by ∼18 s, whereas H⁺ tip-focused peaks spread into the shank. Voltage recordings in the shank (50–80 μm behind the tip) revealed transient bell-shaped depolarizations that correlated strongly with H⁺ but not Ca²⁺ oscillations. In contrast, V_m oscillations readout at the tip correlated equally with tip Ca²⁺- and H⁺-signals, having action potential-like appearances that were approximately five times faster compared with those in the shank. Our multiparameter readout approach identified distinct relationships of chemical and electric signals along PTs, where at the tip changes in both Ca²⁺ and H⁺ correlated with V_m dynamics, whereas at the shank only H⁺ correlated with V_m. We propose that spatially confined chemo-electric coupling support the manifestation of propagating voltage and pH waves along nongrowing PTs, which are preceded by short-lasting but high amplitude tip Ca²⁺ spikes.

The ability to generate distinct spatiotemporal patterns of cytosolic calcium concentration (Ca²⁺_cyt) is a fundamental property of eukaryotic cells and underlies responses to external stimuli as well as directing downstream processes involved in morphogenesis, growth, and even developmental fate. In this review, we consider a number of well-studied and less well-studied photosynthetic plant and algal systems from the point of view of the different Ca²⁺ channel types that underlie spatiotemporal Ca²⁺_cyt patterns. These include pollen tubes, root hairs, moss protonema, algal rhizoids, and single-celled algae. We show that similar spatial and temporal Ca²⁺_cyt patterns can be brought about by the coordinated activities of a range of Ca²⁺ channel types. Most significantly, these channel types vary widely between different photosynthetic groups, indicating that the conserved necessity to generate spatiotemporal Ca²⁺ signals is satisfied by divergent underlying mechanisms, likely reflecting the different evolutionary pressures on ion transport mechanisms across the photosynthetic eukaryote clades.

Bioelectricity has been studied since the 18th century in every branch of the tree of life. Bioelectricity is involved in cell growth, proliferation, and behavior, which at a tissue-scale level translates in dramatic tissue rearrangements during embryology and somatic development. Although ion fluxes can be measured in single cells, it is not unanimous that a single cell may create and sustain different bioelectrical states within itself by means of electrochemical nonequilibrium phenomena. We address this possibility, with a focus on the pollen tube as a biological model. Pollen tubes are the subject of intense research given its unique properties, evolutionary streamlined to very fast apical growth and sensitivity to external cues that affect chemotropic responses. Pollen tube's functions rely on conspicuous tip-focused ions dynamics, involving the formation of steep ion gradients, with ion concentration differences over an order of magnitude when compared with the shank cytosol. These gradients are thought to be based on the spatial segregation of ion transporters, channels, and pumps along the cell, creating distinct electrochemical environments at the tip and the shank. But how polarity is generated and maintained is still a matter of debate. In the past we hypothesized that opposing electrochemical forces of depolarization at the tip and hyperpolarization in the shank could create a membrane potential gradient spanning from the tip to the shank that would be part of feedback mechanisms essential to cell polarity in these and likely other cell types. In this study, we review the latest progress on understanding apical growth from the perspective of bioelectricity-driven morphogenesis.

Oxygenic photosynthesis, performed by plants, algae, and cyanobacteria, is the major route by which solar energy is converted into chemical energy on earth. This process provides the essentials (e.g., food and fuels) for humans to survive and is responsible for oxygenating the earth's atmosphere, which allowed the evolution of multicellular life. Photon energy is harvested during the so-called “light reactions” and used to extract electrons from water, which are then transported through an electron transport chain—in a type of bioelectric current—that is coupled to the movement of protons across the thylakoid membrane, storing energy in the form of a proton electrochemical gradient. The net result of the light reactions is the synthesis of adenosine triphosphate and reduced nicotinamide adenine dinucleotide phosphate, which are used by the “dark” or “light-independent” reactions to convert carbon dioxide into carbohydrates in the Calvin–Benson cycle. In this study, we summarize the structure and function of the main redox-active proteins involved in electron transfer and highlight some recent developments aiming to enhance the efficiency and robustness of the light reactions.

One of the major challenges for plant biology research is to elucidate the complex mechanisms involved in the plant response to stress conditions. This is of utmost importance in view of climatic change that affects crop yields, because of exposure of plants to more severe and frequent environmental stresses such as drought, salinity, and high light. The defense response of the plants to stress conditions requires the orchestration among different signaling pathways activated in different subcellular compartments. An increasing knowledge became available about the role of bioenergetics organelles, the sites of energy conversion in eukaryotes by photosynthesis in chloroplasts and respiration in mitochondria. Information is mainly restricted to retrograde signaling between the organelles and the nucleus. The emerging hypothesis discussed in this minireview is that interorganellar cross talk between mitochondria and chloroplasts through Ca²⁺ and reactive oxygen species signaling may also play a role in ensuring an optimized response of plants and algae to environmental stresses.

Plants form mutually beneficial or antagonistic interactions with organisms from various kingdoms of life. A clear understanding of the underlying mechanisms is fundamental for crop protection and environmental preservation. Although historically overlooked, the role of plant bioelectricity in initiating and maintaining biotic interactions is recently emerging as an exciting research topic. In this review, we summarize the state-of-the-art regarding the role of plant bioelectricity in biotic interactions focusing on both shoots and roots. We describe how root bioelectricity mediates interactions with pathogens and symbionts from different phyla, and the role played by flower electric fields in pollination.