Kinematic Evidence of Root-to-Shoot Signaling for the Coding of Support Thickness in Pea Plants

Abstract

Plants such as climbers characterized by stems or tendrils need to find a potential support (e.g., pole, stick, other plants or trees) to reach greater light exposure. Since the time when Darwin carried out research on climbing plants, several studies on plants' searching and attachment behaviors have demonstrated their unique ability to process some features of a support to modulate their movements accordingly. Nevertheless, the strategies underlying this ability have yet to be uncovered. The present research tries to fill this gap by investigating how the interaction between above- (i.e., stems, tendrils, …) and below-ground (i.e., the root system) plant organs influences the kinematics of their approach-to-grasp movements. Using three-dimensional (3D) kinematic analysis, we characterized the movements of pea plants (Pisum sativum L.) as they leaned towards supports whose below- and above-ground parts were characterized by different thicknesses (i.e., thin below- thick above-ground, or the opposite). As a control condition, the plants were placed next to supports with the same thickness below and above ground (i.e., either entirely thin or thick). The results suggest that the information regarding below- and above-ground parts of a support appears to be integrated and modulates the reach-to-grasp behavior of the plant. Information about the support conveyed by the root system seems to be particularly important to achieve the end-goal of movement.

Keywords: circumnutation; climbing plants; kinematics; plant behavior; root-to-shoot signaling.

Figure 1

Supports for the: (a) ‘Thin-Below’ condition, (b) the ‘Thick-Below’ condition, (c) the ‘Control-Thin’ condition, and (d) the ‘Control-Thick’ condition. In each case the support was positioned in front of the first plant’s leaf at a distance of 12 cm.

Figure 2

Graphical representation of the experimental set up. The representation illustrates the ‘Thick-Below’ condition.

Figure 3

The landmarks considered and examples of the spatial trajectories. (a) The landmarks considered were the support (1, 2) and the tip of the tendrils (3, 4). The colors of the circles correspond to the colors of the trajectories shown in the right-side panel (i.e., light-blue, and red lines in panel b refer to the individual trajectory for each tendril). (b) represents the trajectories for the tip of the tendrils for the ‘Control-Thin’, ‘Thin-Below’, ‘Control-Thick’ and ‘Thick-Below’ support conditions. The support is a solid vertical line. The axes x and y refer to the sagittal and vertical axis in mm, respectively. Please note that the plant leaned toward the support and the tendrils grasped it for all the conditions.

Figure 4

Bar plots representing movement time during the ‘Control-Thick’ and ‘Thin-Below’ support conditions and during the ‘Control-Thin’ and ‘Thick-Below’ support conditions. The bars refer to the median; the error bars refer to the absolute deviation (MAD). The asterisks indicate when the difference between the perturbed and the control conditions was significant. Please note that movement duration was longer for the ‘Control-Thick’ than for the ‘Control-Thin’ conditions and they were longer for the perturbed (i.e., ‘Thin-Below and ‘Thick-Below’ support) than for the control conditions. * = p < 0.05; *** = p < 0.001.

Figure 5

A graphical representation of the velocity of the tendrils (a) and of their aperture (b) for the ‘Control-Thin’ (i.e., the light blue line) and the ‘Control-Thick’ conditions (i.e., the red line). The arrows indicate the moments when the maximum peak velocity (a) and the maximum peak aperture (b) occurred. Please note that these peaks occurred earlier for the ‘Control-Thick’ than for the ‘Control-Thin’ conditions.

Figure 6

A graphical representation of the velocity (a,c) and the aperture of the tendrils (b,d) during the ‘Control-Thick’ (i.e., the red line) and the ‘Thin-Below’ conditions (i.e., the blue line) and during the ‘Control-Thin’ (i.e., the light blue line) and the Thick-Below conditions (i.e., the orange line). The arrows indicate the time the maximum peak velocity (a,c) and maximum peak aperture of the tendrils (b,d) occurred. Please note that for the perturbed trials (i.e., ‘Thin- and ‘Thick-Below’ condition) the peak velocity of the tendrils was reached earlier with respect to what happened during the control trials (i.e., ‘Control-Thin’ and ‘Control-Thick’ conditions; (a,c)). Further, the peak of the maximum aperture of the tendrils occurred earlier for the ‘Thin-Below’ than for the ‘Control-Thick’ support (b). No differences were found in the maximum aperture of the tendrils and in the peak of the maximum aperture for the ‘Control-Thin’ and ‘Thick-Below’ conditions (d).