Electrical Signaling, Photosynthesis and Systemic Acquired Acclimation

Abstract

Electrical signaling in higher plants is required for the appropriate intracellular and intercellular communication, stress responses, growth and development. In this review, we have focus on recent findings regarding the electrical signaling, as a major regulator of the systemic acquired acclimation (SAA) and the systemic acquired resistance (SAR). The electric signaling on its own cannot confer the required specificity of information to trigger SAA and SAR, therefore, we have also discussed a number of other mechanisms and signaling systems that can operate in combination with electric signaling. We have emphasized the interrelation between ionic mechanism of electrical activity and regulation of photosynthesis, which is intrinsic to a proper induction of SAA and SAR. In a special way, we have summarized the role of non-photochemical quenching and its regulator PsbS. Further, redox status of the cell, calcium and hydraulic waves, hormonal circuits and stomatal aperture regulation have been considered as components of the signaling. Finally, a model of light-dependent mechanisms of electrical signaling propagation has been presented together with the systemic regulation of light-responsive genes encoding both, ion channels and proteins involved in regulation of their activity. Due to space limitations, we have not addressed many other important aspects of hormonal and ROS signaling, which were presented in a number of recent excellent reviews.

Keywords: PsbS overexpression and npq-4; electrical signal; ion channel activity; photosynthesis; plasma membrane.

Figure 1

Scheme of the signaling pathways triggered by electrical signals, that are possibly involved in long-term adjustment of photosynthesis, SAA and SAR. The blue solid lines indicate the induction of the calcium wave; blue dotted lines—fast pathways influencing photosynthesis; purple lines - the pathways for long-term inactivation of photosynthesis; red lines—ROS- and NPQ-dependent pathways, sinus-like wave—the electric signals, black solid lines—electron flow. Abbreviations in the alphabetical order: ABA, abscisic acid; APX, ascorbate peroxidase; arrows, increase (green) and decrease (red) of a process; ATPase, ATP synthase; C/C-C, Ca²⁺- dependent protein kinases (CPK/CBL-CIPKs); Ca, potential-dependent, mechano-sensitive and (or) ligand-dependent Ca²⁺ channels; CEF, cyclic electron flow; Cl, Ca²⁺- dependent Cl⁻ channels; Cyt b₆f, cytochrome b₆f complex; EL, excess light; FD, ferredoxin; FNR, ferredoxin-NADP⁺ reductase; GLR, Glue receptor-like channels; JA, jasmonic acid; K, potential-dependent K⁺ channels; LHCII and LHCI, Light-harvesting complex II and I; LL, low light; NPQ, non-photochemical quenching; Pd, plasmodesma; PQ and PQH₂, oxidized and reduced plastoquinone; PsbS, Photosystem II Subunit S; PSII and PSI, photosystems II and I; PSucS, phloem sucrose symporter; RBOH, Respiratory oxidase homolog; SAA, systemic acquired acclimation; Suc, sucrose; TPC1, vacuolar TWO PORE CHANNEL1 calcium channels; ΦPSI and ΦPSII, the photochemical quantum yield of PSI and PSII.

Figure 2

The electrical signals generated on the leaf surface in variable light conditions. Relative changes in the plasma membrane electrical potential were recorded for genotypes differing in PsbS protein content: red line, recessive mutant npq4 devoid of PsbS; black line, WT ecotype Col-0; blue line, overexpressing line of oePsbS. Generally, the pattern of electrical signal detected on the leaf surface is reversed, when measured intracellularly. The recording by surface contact electrode detects a mixture of the signals from the three types of cells: guard, epidermal and mesophyll cells, and they can differ in their responses to light.

Figure 3

Co-expression of light-responsive genes involved in the flow of ions across the membranes and in the non-photochemical quenching. Multiple microarray and RNAseq experiments, as well as NCBI database were searched to select genes which respond to the excess light (induction of SAA and SAR) and are involved in ion transport across biological membranes in Arabidopsis. 273 genes with query “ion channel” and 10 genes for query “nonphotochemical quenching” were verified in the AmiGO 2 database. Finally, the Similarity Search Tool and Hierarchical Clustering of the Genevestigator were used to select 45 genes with the most closely correlated expression profiles during defined light conditions (Exp ID: AT-00467 and AT-00682). The transfer of the plant from low light (LL, 65 μmol photons m⁻² s⁻¹) to excess light (EL, 1300 μmol photons m⁻² s⁻¹), from moderate light (ML, 150 μmol photons m⁻² s⁻¹) to darkness (D), from ML to LL; and from ML to high light (HL, 400 μmol photons m⁻² s⁻¹) was compared. Left panel represents relative expression data of experimental vs control values. GO class was assigned to each gene according to NCBI and Gene Set Enrichment tool of Genevestigetor and the results is indicated in the right panel as: - anion channel activity; + cation channel activity; Cl⁻, K⁺, Ca²⁺ Na⁺, H⁺, chloride, potassium, calcium, sodium and hydrogen ions channel activity; V, pH, M - voltage-, pH-, mechanically-gated ion channel activity; PL, CP, VC, protein localization in plasma membrane, chloroplast, vacuole.