Hygroscopic movements in Geraniaceae: the structural variations that are responsible for coiling or bending

Abstract

Summary The family Geraniaceae is characterized by a beak‐like fruit, consisting of five seeds appended by a tapering awn. The awns exhibit coiling or bending hygroscopic movement as part of the seed dispersal strategy. Here we explain the variation in the hygroscopic reaction based on structural principles. We examined five representative species from three genera: Erodium, Geranium, and Pelargonium. Using X‐ray diffraction, and electron and polarized light microscopy, we measured the cellulose microfibril angles in relation to the cell and cellulose helix axes. The behavior of separated single cells during dehydration was also examined. A bi‐layered structure characterizes all the representative genera studied, with a hygroscopically contracting inner layer, and a stiff outer layer. We found that the cellulose arrangement in the inner layer is responsible for the type of awn deformation (coiling or bending). In three of the five awns examined, we identified an additional coiling outer sublayer, which adds coiling deformation to the awn. We divide the movements into three types: bending, coiling, and coiled‐bending. All movement types are found in the Geranium genus. These characteristics are of importance for understanding the evolution of seed dispersal mechanisms in the Geraniaceae family.

Pneumatic Coiling Actuator Inspired by the Awns of Erodium cicutarium

“…That is, the walls of the Erodium awn cells have reinforcing cellulose fibers arranged in a tilted helical pattern ( Figure 1B) so that the longitudinal axis of the helical fibers does not align with the cell axis. As a result, when the ambient humidity drops, plant tissues in the Erodium awn would shrink in volume due to hygroscopy, and their tilted helical fibers can direct this shrinking into a coiling motion Aharoni et al, 2012;Abraham and Elbaum, 2013;Elbaum and Abraham, 2014;Jung et al, 2014;Zhao et al, 2017). Similarly, the awn would uncoil when humidity increases, essentially creating a "drill bit" in the plant kingdom.…”

Reduction of granular drag inspired by self-burrowing rotary seeds

“…Some Erodium and Pelargonium species, flowering plants belonging to a genus of the family Geraniaceae, produce seeds with an appendage that is used for the seed dispersal and burial. [8][9][10][11][12] Fig. 1 (Multimedia view) shows the seed awns of three Pelargonium species.…”

“…Each awn is composed of materials with different hygroscopic expansiveness and thus responds to a change in humidity. 11,12 In a humid environment at night time or after a rain fall, a helically coiled awn deforms to a linear configuration, and the deformation can create thrust against the soil when one end of the awn is anchored. 8 Owing to the helical shape of the awn, the hygroscopic expansion entails a rotary motion during the extension.…”

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“…Plant motions are driven by (a combination of) several means of actuation, which are summarized in the following. The resulting organ deformation include—among other types—uniaxial bending (e.g., pine cone seed scale bending, Figure b,c), multiaxial bending (e.g., “waving” leaflet motion in the Telegraph plant), coiling (e.g., in Stork's Bill fruits), flat‐to‐helical transitions (e.g., the opening of seed pods in many species from the legume family), rapid curvature inversions of shell‐like structures (e.g., trap closure in the Venus flytrap, Figure d), explosive bursts (e.g., seed pods in Touch‐Me‐Nots), torsional buckling (e.g., petal movement in the Bird‐Of‐Paradise, Figure a), and complex folding processes incorporating kinematic amplification mechanisms (e.g., trap closure in the Waterwheel plant) …”