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Hydration-induced reversible deformation of biological materials

Nature Reviews Materials volume 6, pages 264–283 (2021)Cite this article

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Abstract

The influx and efflux of water in biological structures actuates reversible deformation and recovery processes that are crucial for mechanical functions in plants and animals. These processes utilize various mechanochemical mechanisms: swelling directed by the arrangement of cellulosic microfibrils in a bilayer construct, which generates different deformation patterns; lignification gradients; hierarchical foam-like inner structures, some of which also include swelling by hygroscopic cellulose inner cell layer; turgor pressure, which is activated by osmosis and acts at the cellular level, generating reversible motions. In this Review, we present representatives of each of these four mechanisms: pine cones, wheat awns, the twisted opening of Bauhinia pods and the seed of the stork’s bill; the resurrection plant; ice plant seed capsules and carrotwood seed pod; the wilting and redressing of plant stems. Natural polymeric materials produced by animals can also exhibit hydration-driven shape and strength recovery: bird feathers and hair are prime examples. Spider silk — a non-keratinous biopolymer — also exhibits humidity-driven reversible deformation. After describing these animal-based mechanisms, we outline bioinspired applications to actuate multifunctional and biocompatible smart materials, and indicate future directions of research with potential for new bioinspired designs.

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Fig. 1: Mechanisms of hydration-induced movement.
Fig. 2: Hygroscopic movements that enable plants to disperse or self-bury their seeds.
Fig. 3: Hygroscopic movements induced by gradient lignification in resurrection plant Selaginella lepidophylla.
Fig. 4: Hygroscopic structure in an ice plant seed capsule and the porous structure in a carrotwood seed pod.
Fig. 5: Effect of hydration on turgor pressure in a plant stem.
Fig. 6: Principal mechanisms operating in bilayer-based deformation of plants.
Fig. 7: Hydration-induced shape and strength recovery of bird feathers.
Fig. 8: Hydration-induced shape memory effect in animal hairs.
Fig. 9: Humidity-driven reversible supercontraction of spider silk as an artificial muscle.
Fig. 10: Bioinspired self-shaping materials manufactured by magnetic-field-controlled reinforcement and 4D printing.
Fig. 11: Plant-inspired soft responsive materials fabricated by controlled molecular self- assembly.
Fig. 12: Reversible hydration-induced motion in synthetic systems inspired by either skin or silk.

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Acknowledgements

This work was supported by a Multi-University Research Initiative (MURI) through the United States Air Force Office of Scientific Research (AFOSR-FA9550-15-1-0009). The input provided by our colleagues in the MURI Program, Horacio Espinosa, Robert Ritchie, Pablo Zavattieri and Joanna McKittrick, is appreciated. We gratefully acknowledge Arnaud Pirosa for preparing the pine-cone specimens and Wen Yang for help on the pine-cone project. Eduard Arzt (INM) and Shengqiang Cai (UCSD) provided valuable help with our Outlook section and we are grateful for his suggestions. Yang Wang, Zhijian Wang and Qiguang He helped with the set-up for photographing some plant tissues. We appreciate Nicole Shen for helping us to collect resurrection plants. Discussions with Xudong Liang on hydroelasticity were also important for preparing the manuscript. The pioneering work on carrotwood seed pod by Audrey Velasco-Hogan is also appreciated. We are grateful to Xuan Zhang at Leibniz Institute for New Materials for help with the schematic drawing for plant-movement mechanisms.

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  1. Materials Science and Engineering Program, University of California, San Diego, San Diego, CA, USA

    Haocheng Quan & Marc André Meyers

  2. Department of Materials Science and Engineering, University of California, Irvine, Irvine, CA, USA

    David Kisailus

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H.Q. wrote the first draft of the paper and developed the figures. D.K. provided advice in bioinspired applications. M.A.M. conceived the structure and focus of this paper and participated actively in the writing and illustrations.

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Quan, H., Kisailus, D. & Meyers, M.A. Hydration-induced reversible deformation of biological materials. Nat Rev Mater 6, 264–283 (2021). https://doi.org/10.1038/s41578-020-00251-2

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