The seed-bearing scales of pinecone plants disperse the seeds by opening the scales at dry conditions and keep the scales closed at wet conditions [26]. Notably, the opening and closing of scales can be repeated many times at alternating humidity levels. Such reversible opening/closing behavior is highly related to the structural assembly of the scales rather than cellular activity [9]. Pinecone has two types of scales: larger ovuliferous scale and smaller bract scale Figure 2a(i). The ovuliferous scale responds to humidity change, while the bract scale is humidity-inert. Located in the inner surface of the ovuliferous scale are bundled sclerenchyma fibers (8–12 mm in diameter and 150–200 mm long), while the outer surface are sclerids (20–30 mm diameter and 80–120 mm long), as shown in Figure 2a(i). The ovuliferous scale moves towards the center of the cone in high relative humidity and away from the center in low relative humidity, generating a bending angle up to 55°. Such a drastic change of bending angle during the opening/closing process of pinecone scales is believed to be associated with the orientation difference of cellulose microfibrils (CMFs) in the inner fibers and outer sclerids [9,27]. As shown in Figure 2a(ii), Figure 2a(iii), the angle of winding of microfibrils (θ) relative to the long axis of the cell in sclerids (74 ± 5°) is much higher than that of fibers (30 ± 2°). This winding angle difference results in different coefficients of hygroscopic expansion of the cells in fibers (0.06 ± 0.02) and sclerids (0.20 ± 0.04). The higher hygroscopic expansion coefficient of outer sclerids enables the longitudinal expanding/shrinking of ovuliferous scales at wet/dry conditions, while the inner fibers with lower hygroscopic expansion coefficients do not respond as strongly as the outer sclerids to humidity change but resist the expanding/shrinking [28,29,30]. Therefore, the key to opening/closing of pinecone scales lies in the CMFs with different orientations Figure 2a(iv), leading to anisotropic expanding/shrinking while being resisted [9,27,28].

Wild wheat has bundles of seed dispersal units composed of two pronounced awns that balance the unit as it falls to the ground. The wheat awn plays a crucial role in the seed dispersing process. The awns bend inward when the air is wet (at nighttime) and bend outward to release seeds when the air is dry (at daytime). The bending process is reversible as humidity changes alternatively. The underlying humidity-responsive and reversible actuation mechanism is related to the special structural configuration of the awn [10]. The awn has a wide cap and a relatively narrow ridge facing to the same direction along the awn Figure 2b(i). Though the cap and the ridge show no significant difference in chemical composition, they display distinct stiffnesses as revealed by scanning acoustic microscopy Figure 2b(iii) and nanoindentation test. The cap has a much higher local effective Young’s modulus (20.5 ± 2.6 GPa) than that of ridge (10.0 ± 2.8 GPa). Such stiffness variation is mainly attributed to the orientation of cellulose microfibrils (CMFs) or microfibril angle (MFA). As revealed by the wide-angle X-ray scattering, the cap has an MFA close to 0, meaning that the CMFs are well-aligned along the axis of awn. However, the CMFs in the ridge are randomly oriented Figure 2b(iv). Notably, such difference of CMF orientation only occurs in the lower part of the awn (2 cm below the seed). Though the humidity-responsive actuation of wheat awn resembles that of pinecone scale [9], there is still a slight difference in the specific actuation mechanism. In response to the humidity rise, the cap region expands laterally, while the ridge region expands longitudinally, pushing the awns together. When the humidity drops, the region contracts, pulling the awns apart.

Bauhinia seed pod remains closed at wet conditions yet opens to release the seeds at dry conditions [27,32]. The seed pod has two pod valves which are initially flat at wet conditions. When the air is dry, the pod valves twist into helical strips of opposite handedness, during which the pod opens to release the seeds. The seed dispersal process is, therefore, a chirality-creating process [32,33]. The underlying mechanism behind this flat-to-helical transition during pod opening is again associated with the orientation of cellulose microfibrils (CMFs) in pod valves [27,32]. Oriented at an angle of +45° and −45° with respect to the longitudinal axis of the pod Figure 2c(i), CMFs in the inner and outer layers of the pod valve act as a scaffold resisting the contraction of the round parenchyma cells in which they are embedded. When the pod gets dried by the air with a low humidity, the two juxtaposing fibrous layers shrink perpendicularly to its orientation, inducing mirror-image saddle-like curvatures an eventually a dramatic opening [34]. Note that such twisting behavior of pod valves can turn into coiling when the ratio between the valve’s width and thickness exceeds a certain value, which is seen in the pod of Bauhinia galpinii [35].

Erodium gruinum (also known as stork’s bill) is one of the species in the Geraniaceae plant family featured with beak-like fruits that are composed of five seeds appended by long tapering awns [36]. Prior to ripening, five awns are connected to a central column in one fruit (Figure 2d(i)). As the seeds mature, the awns dry out and contract. In this process, elastic energy builds up to the breaking point. The extreme torque generated by the twisting awn catapults the ripened seeds away from the parent plant [37]. Once on the ground, the awns respond to humidity and quickly change its shape with the assistance from the hygroscopic cells. The awn would coil tightly at low humidity and uncoil at high humidity. Such an alternating coiling/uncoiling process helps the awn to locomote on the ground until a safe germination site is found [38]. The underlying mechanism for this reversible coiling/uncoiling is different from the bending wheat awn and twisting pod valve where a bilayer structure is involved. Instead, a specialized single layer consisting of a mechanically uniform tissue is responsible for the hygroscopic coiling/uncoiling movement of stork’s bill. Though the awn also has an inner layer and an outer layer with different morphologies Figure 2d(ii), each layer displays similar coiling behaviors even when they are split lengthwise along the awn [31]. Revealed by scanning electron microscopy, the inner layer of the awn shows a group of coiling cells behind a single coiled cell connected to the tissue at one end Figure 2d(iii). Furthermore, cryo-scanning electron images show the change in microfibril angle in a single cell Figure 2d(iv). Therefore, coiling of the stork’s bill awn arises from an intrinsic property of the cells in the inner layer. Single cells cooperate with each other to produce a macroscopic coil. As the awn dries, its main longitudinal axis is bending and twisting at the same time. This distortion is manifested as coiling of the entire bundle of cells [31,36,39].

Living in arid and semi-arid habitats, the Aizoaceae (also known as ice plant) has developed a unique seed dispersal strategy different from other plants [40]. Rather than releasing the seeds at dry conditions, ice plant has protective valves surrounding the seed capsules. The valves remain folded when the air is dry and will only unfold to release the seeds when they get hydrated by water (from rain) [41]. Such a folding/unfolding behavior in ice plants is supported by a different mechanism from the bending, twisting, and coiling mechanism mentioned previously. Responsible for the folding/unfolding valves of ice plant is the sophisticated hierarchical structure of the seed capsules, which allows for a more complex origami-like unfolding movement that incorporates an effective flexing-and-packing mechanism [11]. The seed capsule of ice plant is partitioned by five septa lying beneath the center of each valve Figure 2e(i). Buried along the center of inner valve surface is a hygroscopic keel consisting of two separated halves Figure 2e(i). As shown in Figure 2e(ii), the two halves only come into contact when hydrated, creating a bridge-like structure with an empty space between the upper portion of the keel and valve backing [11]. At dry conditions, the five valves curve upwards to lock the hygroscopically active hinge Figure 2e(iii). With rain, the valves straighten, the hinge hydrates and the compact tissue in its inner side expands. The cells pre-arranged as a collapsed honeycomb swell to form an open honeycomb structure Figure 2e(iv). Such expansion is attributed to the highly hygroscopic cellulosic inner layer in the cell wall. The extension of the inner layer in relation to the outer backing resistance layer pushes the valve open. Thus, the capsule opens to disperse the seeds by the striking raindrops. Once dry again, the hinges bend to curl the valves, locking the capsule until the next rain comes. The specialized tissue involved in the construction of the hinges allows this movement to repeat with little distortion [42].

Living in poor soil, the carnivorous plant Dionaea muscipula (also known as Venus flytrap) gets nutrients from captured preys by its touch-sensitive bivalved leaves [43]. Protruding from the upper leaf epidermis are six tiny hairs known as trigger hairs Figure 3a(i). Once these highly sensitive trigger hairs have been continuously stricken by any visiting insect, an electrical impulse is triggered, causing the leave to snap shut within 0.1 s [12]. After the prey is digested by the secreted enzyme, the trap reopens for the next hunting. This rapid snaping behavior induced by mechanical stimulation is driven by the propagation of action potentials in the leaves [44,45,46,47], which results in a simultaneous expansion of the outer epidermis and a lower shrinkage of the inner epidermis Figure 3a(ii). Though the underlying bio-mechanical principles are not yet fully understood [48], the snap-bulking instability Figure 3a(iii) is involved in the trapping mechanics where an elaborate interplay between swelling/shrinking processes of the various tissue layers and the release of trap-internal prestress is involved [12,48,49,50,51]. Specifically, the traps are in a state of ready-to-snap which is enabled by the internal hydraulic pressure differences between layers (i.e., prestress) before it is mechanically stimulated. Once the snapping is triggered, the prestress is released.

Another carnivorous plant living in nutrient-poor soil is sundew. It also has a prey-capturing organ featured with long tentacles protruding from its leaf, each having a sticky gland at the tip [49]. These glands produce nectar to attract small insects. Once stuck by the viscous adhesive, the insect is trapped by the closing leaf with fibrillar tentacles. During this enclosing process, chemical substances, such as jasmonates, are accumulated, triggering the bending of sundew leaves [13]. It is later revealed that recepwtor potentials and a series of action potentials are generated in the tentacles by the mechanical stimulation [50], which causes the bending to trap the insect Figure 3b(i). Importantly, chemical substances from the entrapped insect trigger the accumulation of jasmonates and digestive enzymes [50,51]. Unfortunately, the mechanical principles underlying the trapping of sundew tentacles remain poorly understood. Two possible mechanisms have been proposed [52]: (1) rapid water transport from cells in the adaxial half of the tentacle to cells in the abaxial half, resulting in adaxial contraction and abaxial extension Figure 3b(ii); (2) a sudden loss of turgor pressure in adaxial cells followed by tentacle bending owing to prestress of the abaxial surface to release the elastic energy stored in the epidermal cells on the adaxial side.

Mimosa pudica plant has very sensitive leaves. A gentle touch on the leaf would trigger the self-defending response in the plant: rapid folding up its leaves (or leaflets as they are small). Located at the base of each leaflet is a pulvinus (Figure 3c(i)) responsible for the rapid and touch-sensitive folding behavior [54]. Pulvinus contains cells full of water which pushes against the cell walls, during which turgor pressure is generated. More specifically, the pulvinus has two groups of specialized parenchymatous cells called motor cells arranged in two opposite zones Figure 3c(ii/iii): the flexor or ventral zone and the extensor or dorsal zone [55]. These motor cells can rapidly change their volume and shape induced by changes in turgor pressure. As shown in Figure 3c(iv), upon mechanical stimulation of the plant, an action potential is initiated which propagates a signal from the site of the stimulus to the pulvinus. This results in another action potential which initiates the differential transport of K⁺ and Cl⁻, leading to a change in turgor pressure in the cells. Consequently, the water potential in the extensor cells increases, resulting in loss of water and shrinkage of the cells. Whereas the water potential in the flexor cells drops, leading to swell of cells to a turgid state. As a result, the leaflet folds up [53,55].