Humidity-dependent wound sealing in succulent leaves of Delosperma cooperi – An adaptation to seasonal drought stress

Abstract

During evolution, plants evolved various reactions to wounding. Fast wound sealing and subsequent healing represent a selective advantage of particular importance for plants growing in arid habitats. An effective self-sealing function by internal deformation has been found in the succulent leaves of Delosperma cooperi. After a transversal incision, the entire leaf bends until the wound is closed. Our results indicate that the underlying sealing principle is a combination of hydraulic shrinking and swelling as the main driving forces and growth-induced mechanical pre-stresses in the tissues. Hydraulic effects were measured in terms of the relative bending angle over 55 minutes under various humidity conditions. The higher the relative air humidity, the lower the bending angle. Negative bending angles were found when a droplet of liquid water was applied to the wound. The statistical analysis revealed highly significant differences of the single main effects such as “humidity conditions in the wound region” and “time after wounding” and their interaction effect. The centripetal arrangement of five tissue layers with various thicknesses and significantly different mechanical properties might play an additional role with regard to mechanically driven effects. Injury disturbs the mechanical equilibrium, with pre-stresses leading to internal deformation until a new equilibrium is reached. In the context of self-sealing by internal deformation, the highly flexible wide-band tracheids, which form a net of vascular bundles, are regarded as paedomorphic tracheids, which are specialised to prevent cell collapse under drought stress and allow for building growth-induced mechanical pre-stresses.

Self-Repair in Cacti Branches: Comparative Analyses of Their Morphology, Anatomy, and Biomechanics

“…), and impedes further fissure propagation. The driving forces involved are mostly physical reactions such as the swelling of cells, the melting of waxes, and the deformation of wound tissues or entire organs [ 6 ]. Subsequently, during the long-lasting self-healing phase, the damage is structurally repaired by a process characterized by cell division and tissue regeneration, both of which restore (at least partly) mechanical properties and functions [ 7 ].…”

Comparative Analyses of the Self-Sealing Mechanisms in Leaves of Delosperma cooperi and Delosperma ecklonis (Aizoaceae)

“…), a rapid self-sealing phase initiates self-repair and restores the functional integrity of the leaf preventing any further loss of stored water from the system. Subsequently, a comparatively slow self-healing phase restores structural integrity and, hence, in part the mechanical properties of the leaf [ 8 , 15 , 16 ]. The quick initial self-sealing phase is of particular interest, as it involves a deformation of the entire leaf rapidly bringing the wound edges into contact and preventing further water loss.…”

“…The deformation of D. cooperi leaves during self-sealing differs dependent on the type of wound applied to the leaf. If a longitudinal or transversal cut is applied unilaterally, i.e., only on one side of the leaf, the leaf will bend towards the side of the incision leading to the sealing of the wound [ 15 , 16 ]. If an injury is applied around the circumference of the leaf, the entire leaf will perform a contraction along the leaf axis [ 15 , 16 ].…”

“…If a longitudinal or transversal cut is applied unilaterally, i.e., only on one side of the leaf, the leaf will bend towards the side of the incision leading to the sealing of the wound [ 15 , 16 ]. If an injury is applied around the circumference of the leaf, the entire leaf will perform a contraction along the leaf axis [ 15 , 16 ]. The findings of Dumais and Forterre [ 20 ] (also see Skotheim and Mahadevan [ 21 ]) suggest two mechanisms acting as possible driving forces behind the self-sealing kinematics: hydraulic movements or mechanical instabilities.…”

Wound reactions in stems of Leonurus cardiaca: a morphological, anatomical, and biomechanical study

“…Comparative studies of artificially injured plant organs have revealed various wound reactions that can be subdivided into a fast selfsealing phase followed by a markedly slower self-healing phase, both being included under the umbrella term of self-repair (Harrington et al 2015). Mechanical damage is immediately followed mainly by physical reactions causing rapid self-sealing that include: (i) tissue deformation in the wounded region (Anandan et al 2018;Speck et al 2018), and (ii) discharge of mucilage (Zimmermann and Granata 2002;Anandan et al 2018). During the subsequent self-healing phase, chemical reactions and more complex biological responses dominate such as: (i) coagulation of latex (Bauer and Speck 2012), (ii) local lignification of tissues (Paul-Victor et al 2017), (iii) formation of a (ligno-suberized) boundary layer (Rittinger et al 1987;Evert 2006), and (iv) development of a wound periderm (Evert 2006).…”