Plant Movement Response to Environmental Mechanical Stimulation Toward Understanding Predator Defense

Abstract

Plants are fascinating living systems, possessing starkly different morphology to mammals, yet they have still evolved ways to defend themselves, consume prey, communicate, and in the case of plants like Mimosa pudica even move in response to a variety of stimuli. The complex physiological pathways driving this are of great interest, though many questions remain. In this work, a known responsive plant, M. pudica is mechanically stimulated, in terms of wounding via removal of pinnae, nonwounding mechanical poking, and nonwounding pulses of air through a designed small nozzle approach. Removal of clusters called pinnae resulted in rapid, asymmetric response in the adjacent pinnae, while mechanical poking and air pulse responses are slower and more localized. Additionally, while the response from poking propagated across the plant, wind stimuli consistently resulted in the actuation of only the leaflets directly stimulated, suggesting unique sensing mechanisms. Mechanical damage may imply a potential predator, while mechanical stimulation from airflow may be processed as wind, which is of little danger. These findings demonstrate an intricate, stimulant-dependent mechanical sensing process, which is important in plant physiology, mechanobiology, and future biohybrid soft robotic designs.

Keywords: biohybrid systems; mechanics; mimosa pudica; plants; signal response.

Figure 1

A) Four snapshots of M. pudica during stimulation via poking with blunt AWG23 (American Wire Guage) metal tip, showing a propagation of actuation between T = 18 s and T = 27 s. B) Kinematic coordinate system used. θ_about(blue) is the angle rotated around the rachis. θ_along(red) is the angle rotated along the pinna toward the end of the rachis. θ_fold(green) is the combined angle about both axes. A diagram of plant characteristics is in Figure 2. C) Comparison of the response of selected examples from each of the three modes of stimulation (removal, poke, air pulse) showing the dramatically different shape of the behaviors as well as the average delay between one leaflet achieving 20% normalized actuation and the next leaflet and standard deviation. Each line is a leaflet, with time on the X‐axis and the progression of folding represented on the Y‐axis. Line brightness shows proximity of leaflets to their neighbors. Additional details are presented in Figure 3, 4, 5, and photos demonstrating experimental setup available in Figure S5–S7 (Supporting Information).

Figure 2

Photographs of the considered parts and organs of the Mimosa pudica; left: lateral view, right: top view. The primary (PP), secondary (SP), and tertiary (TP) pulvini are the motor organs of the Mimosa pudica, moving the Petiole (P), Rachis (R), and Leaflet/Pinnule (L) respectively. Also pictured are the Stem (S) and Flower (F).

Figure 3

Mimosa pudica folding response to wounding stimulation via removal of adjacent pinna by means of cutting with scissors, separated into the halves of pinnae divided by the rachis that are proximal(near) and distal(far) to the removed pinnae. A) Four snapshots of an example cutting of a sample of M. pudica, showing the frame immediately following the initial cut, T = 0 s. The reaction occurred very quickly, with most folding complete by T = 1 s, and only small additional changes between T = 1 s and T = 2.8 s. B) Line graphs show the folding of leaflets with respect to time. Time = 0 corresponds to the application of the first stimulus. The Y‐axis has normalized to express the initial folding as “0” and the final folding as “1”, with unresponsive leaflets removed for clarity. Line graphs show rapid, mostly simultaneous response in both sides, with leaflets on the distal half of the rachis of the removed pinna (labeled “Far”) having a slower initial response than leaflets on the proximal half (labeled “Near”). Leaflet 1 is the basal leaflet, with each leaflet moving distally incrementing by 1. C) Heat maps show a total difference in angle between the least and greatest fold values (in degrees) observed in the observational period. The heat maps show that mostly all leaflets responded in samples 1 and 2, with no clear pattern emerging. However, in sample 3 only the leaflets further from the base of the pinna with higher numbers responded, meaning the signal traveled through the basal leaflets without triggering their actuation. Photos demonstrating the experimental setup are in Figure S5 (Supporting Information).

Figure 4

Mimosa pudica folding response to stimulation on back of leaflets via mechanical prodding with blunt AWG23 metal tip. A) Four snapshots of an example poking of a leaf of M. pudica. Frames show the progression of folding with subsequent pokes between T = 0 s and T = 18 s, followed by a cascade of actuation between T = 18 s and T = 27 s. B) Line graphs show the folding of leaflets with respect to time. Time = 0 corresponds to the application of the first stimulus. The Y‐axis has normalized to express the initial folding as “0” and the final folding as “1”, with unresponsive leaflets removed for clarity. Line graphs show organized, regular folding in leaflets, in contrast with air pulse experiments (Figure 5). Leaflet 1 is the basal leaflet, with each leaflet moving distally incrementing by 1. C) Bar charts show the total difference in angle between the least and greatest fold values observed in the observational period. Bar charts show that the signal in sample 2 started near the middle and moved toward the end, and in samples 1 and 3 signal started at the ends and moved toward the base. This propagating, directional behavior suggests a variation potential was produced by non‐wounding stimuli. Photos demonstrating experimental setup available in Figure S5 (Supporting Information).

Figure 5

Mimosa pudica folding response to stimulation on back of leaflets via pulses of air at 6 kPa from a 25Ga nozzle for 50 ms by means of a small nozzle connected to a solenoid valve. A) Four snapshots of an example air pulse on a sample of M. pudica. Frames show numerous local, single leaflet responses between T = 0 s and T = 33 s, but no propagation through the pinna. B) Line graphs show the folding of leaflets with respect to time. Time = 0 corresponds to the application of first stimulus. The Y‐axis has normalized to express the initial folding as “0” and the final folding as “1”, with unresponsive leaflets removed for clarity. Line graphs show nonuniform folding in leaflets with individual leaflets actuating independently, in great contrast with poking experiments (Figure 4). C) Bar charts show the total difference in angle between least and greatest fold values observed in the observational period. Bar charts show total difference in angle between least and greatest fold values observed in the observational period, and show no distinct points where folding signals originated and moved in one direction, as in the poking experiments (Figure 4). Photos demonstrating the experimental setup are in Figure S7 (Supporting Information).

Figure 6

Comparison of the response of selected examples from each of the three modes of stimulation (removal, poke, air pulse) showing the dramatically different shape of the behaviors as well as the average delay between one Mimosa pudica leaflet achieving 20% normalized actuation and the next leaflet and standard deviation. These values are approximately an order of magnitude different between each experiment moving from A) Wounding experiments where a pinna, or leaf cluster, is removed and the adjacent pinna observed, B) non‐wounding prodding of the back of leaflets using a blunt metal tip and C) non‐wounding pulses of air directed through a small nozzle onto the back of the leaflets.