Chemical agents transported by xylem mass flow propagate variation potentials

Abstract

SummaryLong‐distance signalling is important for coordinating plant responses to the environment. Variation potentials (VPs) are a type of long‐distance electrical signal that are generated in plants in response to wounding or flaming. Unlike self‐propagating action potentials, VPs can be measured beyond regions of dead or chemically treated tissue that block signal generation, suggesting a different mode of propagation. Two alternative propagation mechanisms have been proposed: movement of a chemical agent and a pressure wave through the vasculature. Variants of these two signalling mechanisms have been suggested. Here, we use simple models of the underlying physical processes to evaluate and compare these predictions against independent data. Our models suggest that chemical diffusion and pressure waves are unlikely to capture existing data with parameters that are known from other sources. The previously discarded hypothesis of mass flow in the xylem transporting a chemical agent, however, is able to reproduce experimental propagation speeds for VPs. We therefore suggest that chemical agents transported by mass flow within the xylem are more likely than a pressure wave or chemical diffusion as a VP propagation mechanism. Understanding this mode of long‐distance signalling within plants is important for unravelling how plants coordinate physiological responses via cell‐to‐cell communication.

Wound‐ and mechanostimulated electrical signals control hormone responses

“…Hydraulic pressure models for SWP initiation by wounding are not universally accepted because a release of xylem tension upon wounding should, in theory, travel at speeds orders of magnitude faster than the cm min -1 apparent velocities measured for SWPs (e.g. Evans & Morris, 2017). It is notable that many models for SWP initiation have been based on the use of leaf or stem burning as a wound stimulus (e.g.…”

Identification of cell populations necessary for leaf-to-leaf electrical signaling in a wounded plant

“…This mechanism is thought to occur in other species (e.g., ref. 13 ). Alternatively, hydraulic signals in the xylem have been proposed to underlie SWP propagation ( 14 ).…”

Spatial and Temporal Dynamics of Electrical and Photosynthetic Activity and the Content of Phytohormones Induced by Local Stimulation of Pea Plants

“…In pea externally measured distances between the stimulated leaf and the first, the second, and the third leaves amount to 10.9 ± 1.1 cm, 15.2 ± 1.2 cm, and 19.7 ± 1.5 cm, respectively. Since the VP propagation is associated with vascular bundles, in particular with xylem [ 3 , 28 ], VP-covered distances differ from the externally measured distances. According to the scheme ( Figure 6 ) signal-covered distances (pointed with arrows on the scheme) amount to ~20 cm, 15 cm, and 28 cm for the first, the second, and the third leaves, respectively.…”

“…Propagation of the electrical signals in plants is known to be mainly related to the vascular bundles [ 2 , 3 , 4 ], in particular to xylem [ 3 , 28 ]; it can be expected that parameters of VP and investigated physiological responses should be dependent on lengths of the vascular bundles between the burned and analyzed zones. Analysis of dependence of investigated parameters on these lengths ( Figure 7 ) supports this supposition: the typical dependences of parameters of signals and responses on distance from the burned zone are observed.…”