Herbivore-Triggered Electrophysiological Reactions: Candidates for Systemic Signals in Higher Plants and the Challenge of Their Identification

Abstract

In stressed plants, electrophysiological reactions (elRs) are presumed to contribute to long-distance intercellular communication between distant plant parts. Because of the focus on abiotic stress-induced elRs in recent decades, biotic stress-triggered elRs have been widely ignored. It is likely that the challenge to identify the particular elR types (action potential [AP], variation potential, and system potential [SP]) was responsible for this course of action. Thus, this survey focused on insect larva feeding (Spodoptera littoralis and Manduca sexta) that triggers distant APs, variation potentials, and SPs in monocotyledonous and dicotyledonous plant species (Hordeum vulgare, Vicia faba, and Nicotiana tabacum). APs were detected only after feeding on the stem/culm, whereas SPs were observed systemically following damage to both stem/culm and leaves. This was attributed to the unequal vascular innervation of the plant and a selective electrophysiological connectivity of the plant tissue. However, striking variations in voltage patterns were detected for each elR type. Further analyses (also in Brassica napus and Cucurbita maxima) employing complementary electrophysiological approaches in response to different stimuli revealed various reasons for these voltage pattern variations: an intrinsic plasticity of elRs, a plant-specific signature of elRs, a specific influence of the applied (a)biotic trigger, the impact of the technical approach, and/or the experimental setup. As a consequence, voltage pattern variations, which are not irregular but rather common, need to be included in electrophysiological signaling analysis. Due to their widespread occurrence, systemic propagation, and respective triggers, elRs should be considered as candidates for longdistance communication in higher plants.

Are plants sentient?

“…Numerous modern investigations (e.g., Favre & Agosti, ; Fromm & Lautner, ; Pickard, ; van Bel et al, ; Volkov & Ranatunga, ; Yan et al, ; Zimmermann, Mithöfer, Will, Felle, & Furch, ; and references therein) have confirmed the validity of some of these early claims of electrical communication by Bose. Because the phloem is to be found throughout any higher plant, the potential for very long distance communication in large plants exists, incidentally, at considerable speeds (Fromm & Bauer, ; Fromm & Lautner, ; Galle, Lautner, Flexas, & Fromm, ; Yan et al, ; Zimmermann et al, ). Action potentials in plants can move from 0.5 to 40 cm/sec, and the distance covered may be helped by the recently described system potentials (Choi, Hilleary, Swanson, Kim, & Gilroy, ; Zimmermann et al, ).…”

Triggering a false alarm: wounding mimics prey capture in the carnivorous Venus flytrap (Dionaea muscipula)

“…d). Such restricted propagation of typical APs, in contrast to VPs, was also recently documented in noncarnivorous plants (Zimmermann et al ., ) and is also known in sensitive plant ( Mimosa pudica ; Fromm & Lautner, ). But Escalante‐Pérez et al .…”

The role of electrical and jasmonate signalling in the recognition of captured prey in the carnivorous sundew plant Drosera capensis

“…It has been hypothesized that VPs are induced by hydraulic waves in the xylem that affect mechanosensitive ion channels (Mancuso, ) or, if a chemical is transported, via ligand‐activated channels (Malone, ). The SPs were recognized only recently as signals with reverse polarity with all‐or‐nothing character and are not caused by a hydraulic pressure surge (Zimmermann et al ., , ).…”