Flexible control of movement in plants

Abstract

Although plants are essentially sessile in nature, these organisms are very much in tune with their environment and are capable of a variety of movements. This may come as a surprise to many non-botanists, but not to Charles Darwin, who reported that plants do produce movements. Following Darwin's specific interest on climbing plants, this paper will focus on the attachment mechanisms by the tendrils. We draw attention to an unsolved problem in available literature: whether during the approach phase the tendrils of climbing plants consider the structure of the support they intend to grasp and plan the movement accordingly ahead of time. Here we report the first empirical evidence that this might be the case. The three-dimensional (3D) kinematic analysis of a climbing plant (Pisum sativum L.) demonstrates that the plant not only perceives the support, but it scales the kinematics of tendrils' aperture according to its thickness. When the same support is represented in two-dimensions (2D), and thus unclimbable, there is no evidence for such scaling. In these circumstances the tendrils' kinematics resemble those observed for the condition in which no support was offered. We discuss these data in light of the evidence suggesting that plants are equipped with sensory mechanisms able to provide the necessary information to plan and control a movement.

Figure 1

Graphical depiction of the experimental set up and the experimental conditions considered in the three experiments. (a) ‘No stimulus’ condition; (b) ‘3D Stimulus’ condition (Experiment 1) in which a wooden pole (i.e., the 3D stimulus) of 60 cm height of 1.2 cm in diameter (Experiment 1) or either 1.2. or 3 cm in diameter for Experiment 2 was positioned at a distance of 12 cm in front of the first unifoliate leaf for each plant; (c) ‘2D Stimulus’ condition in which the 2D representation (picture) of the 3D stimuli was attached to one of the walls of the growth chamber.

Figure 2

The considered landmarks of the plants and representative examples of their spatial trajectories. (a) Landmarks that were tracked in time through video digitalization procedures: the internode (1), the apex (2), the node below the tendrils (3), and the tips of the tendrils (4 and 5). Markers 6 and 7 were positioned upon the stimulus and served as reference points. The colours of the circles correspond to the colour of the trajectories represented in the other panels for the corresponding landmark. The projected trajectories on the vertical plane of the considered landmarks for the no stimulus (b), the 3D stimulus (c) and the 2D stimulus (d) conditions. The vertical line represents the 3D (solid line) and the 2D (dashed line) stimulus. Circumnutation is particularly evident for the landmark corresponding to the node below the tendrils (green line) and for the tendrils (light blue and red lines). For the apex (yellow line) circumnutation is less pronounced and directed towards the light source. When the stimulus is 3D the tendrils veered towards the stimulus and stopped at the time grasping occurred (c). When there is no stimulus (b) or the stimulus is 2D (d) the tendrils stop to circumnutate and remain far apart. Axis x = sagittal axis in mm; axis y = vertical axis in mm.

Figure 3

Representative examples of spatial trajectories exhibited by the apex for the different experiments. Panel (a) depicts the comparison between the 3D stimulus versus the no stimulus condition. Note that for the 3D stimulus condition the apex veered towards the support whereas for the no stimulus condition the apex grew up to a certain stage and then fell down. Panel (b) depicts the comparison between the thin and the thick 3D stimulus. For both conditions the apex veered towards the stimulus. The vertical solid line represents the 3D stimulus. Panel (c) depicts the comparison between the thin and the thick stimulus presented in 2D. For both conditions the apex grew up to a certain point and then fell down. The vertical dashed line represents the 2D stimulus. Axis x = sagittal axis in mm; axis y = vertical axis in mm.

Figure 4

Tendrils’ kinematics is scaled with respect to the size of the stimulus. Velocity (a) and tendrils aperture (b) profiles for movements performed towards either the thick or the thin stimulus for Experiment 2. Arrows indicate the occurrence of maximum peak velocity (a) and maximum grip aperture (b) depending on stimulus thickness. Please note that when the stimulus is thicker peak velocity is anticipated and the maximum aperture of the tendrils is reached earlier for the thicker than the thinner stimulus.