Dandelion pappus morphing is actuated by radially patterned material swelling

ARTICLE https://doi.org/10.1038/s41467-022-30245-3 OPEN Dandelion pappus morphing is actuated by radially patterned material swelling 1234567890():,; Madeleine Seale Arezki Boudaoud 1,2,3, Annamaria Kiss 4, Simone Bovio 4,5 ✉ & Naomi Nakayama 1,6 ✉ 4, Ignazio Maria Viola 2, Enrico Mastropaolo2, Plants generate motion by absorbing and releasing water. Many Asteraceae plants, such as the dandelion, have a hairy pappus that can close depending on moisture levels to modify dispersal. Here we demonstrate the relationship between structure and function of the underlying hygroscopic actuator. By investigating the structure and properties of the actuator cell walls, we identify the mechanism by which the dandelion pappus closes. We developed a structural computational model that can capture observed pappus closing and used it to explore the critical design features. We find that the actuator relies on the radial arrangement of vascular bundles and surrounding tissues around a central cavity. This allows heterogeneous swelling in a radially symmetric manner to co-ordinate movements of the hairs attached at the upper flank. This actuator is a derivative of bilayer structures, which is radial and can synchronise the movement of a planar or lateral attachment. The simple, materialbased mechanism presents a promising biomimetic potential in robotics and functional materials. 1 School of Biological Sciences, University of Edinburgh, Edinburgh EH9 3BF, UK. 2 School of Engineering, University of Edinburgh, Edinburgh EH9 3FF, UK. 3 Department of Plant Sciences, University of Oxford, South Parks Road, Oxford OX1 3RB, UK. 4 RDP, ENS de Lyon, Université de Lyon, UCB Lyon 1, INRAE, CNRS, 69364, Lyon, Cedex 07, France. 5 LadHyX, CNRS, Ecole Polytechnique, Institut Polytechnique de Paris, 91128, Palaiseau Cedex, France. 6 Department of Bioengineering, Imperial College, South Kensington, London SW7 2AZ, UK. ✉email: ; NATURE COMMUNICATIONS | (2022)13:2498 | https://doi.org/10.1038/s41467-022-30245-3 | www.nature.com/naturecommunications 1 ARTICLE M NATURE COMMUNICATIONS | https://doi.org/10.1038/s41467-022-30245-3 ovement of body parts are typically mediated by specialised hinge structures - actuators - in biological and engineered systems. Biological actuators consist of continuous structures, and differential expansion within the actuator drives reversible movement and morphing. A thematic example is bilayer structure, in which two sides of a planar or cylindrical body expand or shrink more to cause bending or twisting. Inspired by the plethora of examples from nature, diverse designs have been developed for bilayer soft robotic actuators. Hygroscopic plant movements have been particularly relevant for biomimetic engineering and design as some of them do not rely on inherently biologically active processes1. Instead, they can highlight structural features that have been tuned by evolution to optimise mechanical efficiency or use of materials. Plant movements and morphing are generally driven by changes in hydration2. This can be actively regulated by altering solute concentrations to manipulate osmotic gradients or by increasing water uptake and the prevalence of aquaporins2,3. Active water movement occurs in the opening and closing of stomata and the leaf curling of Mimosa plants4,5. Similarly, turgor pressure can allow rapid movements by exploiting mechanical instabilities of precisely formed tissues such as in the Venus fly trap and in the explosive dispersal of Cardamine hirsuta6,7. Alternatively, plant cell walls can passively absorb and release water to cause morphology changes8,9. These hygroscopic movements have been demonstrated, for example, in pine cones, wheat awns and ice plant seed capsules10–12. Directed hygroscopic movements often arise from the differential expansion of cells within a tissue or parts of cell walls with different material properties. These materials respond to water in different ways to allow, for instance, anisotropic swelling typically resulting in bending or coiling motions8. For example, adjacent tissue types with alternating cellulose microfibril orientations generate a bilayer structure to cause bending or twisting motions13–15. This can be combined with differential deposition of phenolics. In the curling stems of the resurrection plant, Selaginella lepidophylla, different amounts of lignin are deposited on each side of the stem with increased hydrophobicity and elastic modulus observed for tissues where lignin is present. The non-lignified side can therefore absorb more water and deform more easily allowing the plant to unfurl its stems when wet and initiate photosynthesis16,17. Similarly, Erodium gruinum awns exhibit differential deposition of phenolic compounds in distinct tissue parts affecting the rate of curling along the length of the awn18. In addition to material composition, the geometry of cells and tissues can contribute to controlling hygroscopic movements. S. lepidophylla cells that swell less tend to have thicker cell walls16,17. In the seed capsules of the ice plant, Delosperma nakurense, cells with a honeycomb structure expand anisotropically due to their elongated geometry and the arrangement of cell wall layers within them12. These examples illustrate that both structural and compositional features are combined to facilitate appropriate and efficient hygroscopic motions, but all rely on heterogeneity of adjacent materials. The haired fruit of the common dandelion undergoes morphing to open or close its flight-enabling pappus19–21. When the hairs are drawn together and the pappus is closed, the fluid dynamics around the pappus are dramatically altered and the dispersal capacity is modified22. This allows the plant to tune dispersal by optimising timing and distances in response to environmental conditions. The dandelion pappus changes shape via a hygroscopic actuator at the apical plate of the achene (fruit) that swells on contact with water19–21. In addition to hygroscopic absorption of water by cell walls in the apical plate, an alternative pappus morphing mechanism 2 occurs in dandelion pappi relying on the cohesive properties of water droplets. Fine hairs that easily bend are particularly sensitive to the cohesion forces generated by water when it forms a contact point with the solid hairs23. Bending of dandelion pappus hairs has been observed before in response to water droplets and may be useful inspiration for engineering precision liquid handling devices24,25. While the hygroscopic actuator function of the apical plate has been observed before, its mode of action remains unclear. This actuator is composed of distinct domains originating from the floral podium, vascular bundles and surrounding cortex tissue. We have found that it generates a sophisticated and precisely patterned radial geometry of at least four different tissue types, differential swelling of which enables the reversible angular movement of the pappu (...truncated)