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An on-demand plant-based actuator created using conformable electrodes

Abstract

Owing to their adaptive interfacial properties, soft actuators can be used to perform more delicate tasks than their rigid counterparts. However, traditional polymeric soft actuators rely on energy conversion for actuation, resulting in high power input or slow responses. Here we report an electrical plant-based actuator that uses a conformable electrical interface as an electrical modulating unit and a Venus flytrap as an actuating unit. Using frequency-dependent action-potential modulation, accurate on-demand actuation is possible, with response times that can be tuned to 1.3 s and a power input of only 10−5 W. The actuator can be wirelessly controlled using a smartphone. It can also be installed on a range of platforms (including a finger and a robotic hand) and can be used to grasp thin wires and capture moving objects.

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Fig. 1: Electrically modulated biohybrid phytoactuator.
Fig. 2: Flytrap stimulation by d.c. voltage.
Fig. 3: Frequency-dependent modulation of flytrap actuation.
Fig. 4: Integration of a modular electrical phytoactuator with other platforms.

Data availability

The data that support the plots in this paper and other findings of this study are available from the corresponding author upon reasonable request.

Code availability

The code to program the ESP8266 Wi-Fi module in the Blynk IoT platform is available at https://github.com/Wenlong0-0/Wireless-control-of-phytoactuator.

References

  1. 1.

    Rus, D. & Tolley, M. T. Design, fabrication and control of soft robots. Nature 521, 467–475 (2015).

    Google Scholar 

  2. 2.

    Walsh, C. Human-in-the-loop development of soft wearable robots. Nat. Rev. Mater. 3, 78–80 (2018).

    Google Scholar 

  3. 3.

    Rich, S. I., Wood, R. J. & Majidi, C. Untethered soft robotics. Nat. Electron. 1, 102–112 (2018).

    Google Scholar 

  4. 4.

    McEvoy, M. A. & Correll, N. Materials that couple sensing, actuation, computation, and communication. Science 347, 1261689 (2015).

    Google Scholar 

  5. 5.

    Kim, Y., Parada, G. A., Liu, S. & Zhao, X. Ferromagnetic soft continuum robots. Sci. Robot. 4, eaax7329 (2019).

    Google Scholar 

  6. 6.

    Li, S., Vogt, D. M., Rus, D. & Wood, R. J. Fluid-driven origami-inspired artificial muscles. Proc. Natl Acad. Sci. USA 114, 13132–13137 (2017).

    Google Scholar 

  7. 7.

    Yang, H. et al. 3D printed photoresponsive devices based on shape memory composites. Adv. Mater. 29, 1701627 (2017).

    Google Scholar 

  8. 8.

    Vatankhah-Varnoosfaderani, M. et al. Bottlebrush elastomers: a new platform for freestanding electroactuation. Adv. Mater. 29, 1604209 (2017).

    Google Scholar 

  9. 9.

    Morimoto, Y., Onoe, H. & Takeuchi, S. Biohybrid robot powered by an antagonistic pair of skeletal muscle tissues. Sci. Robot. 3, eaat4440 (2018).

    Google Scholar 

  10. 10.

    Li, Z. et al. Biohybrid valveless pump-bot powered by engineered skeletal muscle. Proc. Natl Acad. Sci. USA 116, 1543–1548 (2019).

    Google Scholar 

  11. 11.

    Ricotti, L. et al. Biohybrid actuators for robotics: a review of devices actuated by living cells. Sci. Robot. 2, eaaq0495 (2017).

  12. 12.

    Cai, P. et al. Biomechano-interactive materials and interfaces. Adv. Mater. 30, 1800572 (2018).

    Google Scholar 

  13. 13.

    Feinberg, A. W. et al. Muscular thin films for building actuators and powering devices. Science 317, 1366–1370 (2007).

    Google Scholar 

  14. 14.

    Appiah, C. et al. Living materials herald a new era in soft robotics. Adv. Mater. 31, 1807747 (2019).

    Google Scholar 

  15. 15.

    Trewavas, A. Plant intelligence: mindless mastery. Nature 415, 841 (2002).

    Google Scholar 

  16. 16.

    Trewavas, A. What is plant behaviour?. Plant Cell Environ. 32, 606–616 (2009).

    Google Scholar 

  17. 17.

    Skrzypczak, T. et al. Plant science view on biohybrid development. Front. Bioeng. Biotechnol. 5, 46 (2017).

    Google Scholar 

  18. 18.

    Baluška, F., Gagliano, M. & Witzany, G. Memory and Learning in Plants (Springer, 2018).

  19. 19.

    Boudaoud, A. An introduction to the mechanics of morphogenesis for plant biologists. Trends Plant Sci. 15, 353–360 (2010).

    Google Scholar 

  20. 20.

    Qi, J. et al. Mechanical regulation of organ asymmetry in leaves. Nat. Plants 3, 724–733 (2017).

    Google Scholar 

  21. 21.

    Chen, H. et al. Ultrafast water harvesting and transport in hierarchical microchannels. Nat. Mater. 17, 935–942 (2018).

    Google Scholar 

  22. 22.

    Barthlott, W., Mail, M., Bhushan, B. & Koch, K. Plant surfaces: structures and functions for biomimetic innovations. Nano-Micro Lett. 9, 23 (2017).

    Google Scholar 

  23. 23.

    Mousavi, S. A. R., Chauvin, A., Pascaud, F., Kellenberger, S. & Farmer, E. E. GLUTAMATE RECEPTOR-LIKE genes mediate leaf-to-leaf wound signalling. Nature 500, 422–426 (2013).

    Google Scholar 

  24. 24.

    Markin, V. S., Volkov, A. G. & Jovanov, E. Active movements in plants. Plant Signal Behav. 3, 778–783 (2008).

    Google Scholar 

  25. 25.

    Scherzer, S., Federle, W., Al-Rasheid, K. A. S. & Hedrich, R. Venus flytrap trigger hairs are micronewton mechano-sensors that can detect small insect prey. Nat. Plants 5, 670–675 (2019).

    Google Scholar 

  26. 26.

    Hedrich, R. & Neher, E. Venus flytrap: how an excitable, carnivorous plant works. Trends Plant Sci. 23, 220–234 (2018).

    Google Scholar 

  27. 27.

    Volkov, A. G., Adesina, T. & Jovanov, E. Closing of Venus flytrap by electrical stimulation of motor cells. Plant Signal Behav. 2, 139–145 (2007).

    Google Scholar 

  28. 28.

    Volkov, A. G., Adesina, T. & Jovanov, E. Charge induced closing of Dionaea muscipula Ellis trap. Bioelectrochemistry 74, 16–21 (2008).

    Google Scholar 

  29. 29.

    Grimnes, S. & Martinsen, Ø. G. Bioimpedance and Bioelectricity Basics 3rd edn, (Elsevier, 2015).

  30. 30.

    Volkov, A. G. Plant Electrophysiology: Theory and Methods (Springer, 2006).

  31. 31.

    Salvador-Recatalà, V., Tjallingii, W. F. & Farmer, E. E. Real-time, in vivo intracellular recordings of caterpillar-induced depolarization waves in sieve elements using aphid electrodes. N. Phytol. 203, 674–684 (2014).

    Google Scholar 

  32. 32.

    Volkov, A. G. et al. Memory elements in the electrical network of Mimosa pudica L. Plant Signal Behav. 9, e982029 (2014).

    Google Scholar 

  33. 33.

    Mousavi, S. A. R., Nguyen, C. T., Farmer, E. E. & Kellenberger, S. Measuring surface potential changes on leaves. Nat. Protoc. 9, 1997–2004 (2014).

    Google Scholar 

  34. 34.

    Kim, J. J., Allison, L. K. & Andrew, T. L. Vapor-printed polymer electrodes for long-term, on-demand health monitoring. Sci. Adv. 5, eaaw0463 (2019).

    Google Scholar 

  35. 35.

    Naficy, S., Razal, J. M., Whitten, P. G., Wallace, G. G. & Spinks, G. M. A pH-sensitive, strong double-network hydrogel: poly(ethylene glycol) methyl ether methacrylates–poly(acrylic acid). J. Polym. Sci. B 50, 423–430 (2012).

    Google Scholar 

  36. 36.

    Ramanath, G. et al. Templateless room-temperature assembly of nanowire networks from nanoparticles. Langmuir 20, 5583–5587 (2004).

    Google Scholar 

  37. 37.

    Ho, M. D., Liu, Y., Dong, D., Zhao, Y. & Cheng, W. Fractal gold nanoframework for highly stretchable transparent strain-insensitive conductors. Nano Lett. 18, 3593–3599 (2018).

    Google Scholar 

  38. 38.

    Trebacz, K. & Sievers, A. Action potentials evoked by light in traps of Dionaea muscipula Ellis. Plant Cell Physiol. 39, 369–372 (1998).

    Google Scholar 

  39. 39.

    Volkov, A. G., Adesina, T., Markin, V. S. & Jovanov, E. Kinetics and mechanism of Dionaea muscipula trap closing. Plant Physiol. 146, 694–702 (2008).

    Google Scholar 

  40. 40.

    Miyamoto, A. et al. Inflammation-free, gas-permeable, lightweight, stretchable on-skin electronics with nanomeshes. Nat. Nanotechnol. 12, 907–913 (2017).

    Google Scholar 

  41. 41.

    Yuk, H., Lu, B. & Zhao, X. Hydrogel bioelectronics. Chem. Soc. Rev. 48, 1642–1667 (2019).

    Google Scholar 

  42. 42.

    Liu, Y. et al. Soft and elastic hydrogel-based microelectronics for localized low-voltage neuromodulation. Nat. Biomed. Eng. 3, 58–68 (2019).

    Google Scholar 

  43. 43.

    Stavrinidou, E. et al. Electronic plants. Sci. Adv. 1, e1501136 (2015).

    Google Scholar 

  44. 44.

    Wong, M. H. et al. Nitroaromatic detection and infrared communication from wild-type plants using plant nanobionics. Nat. Mater. 16, 264–272 (2016).

    Google Scholar 

  45. 45.

    Stavrinidou, E. et al. In vivo polymerization and manufacturing of wires and supercapacitors in plants. Proc. Natl Acad. Sci. USA 114, 2807–2812 (2017).

    Google Scholar 

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Acknowledgements

We acknowledge financial support from the National Research Foundation (NRF), Prime Minister’s Office, Singapore, under its NRF Investigatorship (NRF-NRFI2017-07) and the Agency for Science, Technology and Research (A*STAR) under its AME Programmatic Funds (project no. A18A1b0045) on Cyber-Physiochemical Interfaces (CPI) Programme. N.M. was supported by the Japan Society for the Promotion of Science (JSPS) overseas research fellowship. Finally, we thank A. L. Chun for critically reading and editing the manuscript.

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Authors

Contributions

W.L., N.M. and X.C. designed the project and experiments. Zhiyuan Liu assisted with the conformable electrode design, fabrication and characterization. W.L. and M.W. synthesized and characterized the adhesive hydrogel. Y.L. and W.L. prepared the cross-section of the plant and hydrogel for the optical microscope. P.C. assisted with the fabrication of the conformable electrode. G.C. and W.L. designed and performed the adhesive strength measurement of the electrode. W.L., F.Z. and C.L. performed the flytrap electrical signal measurement, flytrap mechanical and electrical stimulation, and phytoactuator implementation. Zhihua Liu designed and manufactured the LabVIEW-controlled motorized device for the accurate capture of moving objects. Z.Lv and W.L. fabricated the AgNW and CNT conductors. W.Z. performed the transmission electron microscopy investigation for the Au nanomesh. W.L., N.M. and X.C. wrote the manuscript. All the authors read and revised the manuscript.

Corresponding author

Correspondence to Xiaodong Chen.

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The authors declare no competing interests.

Additional information

Peer review information Nature Electronics thanks Ingrid Graz, Alexander Volkov and the other, anonymous, reviewer(s) for their contribution to the peer review of this work.

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Supplementary information

Supplementary Information

Supplementary Figs. 1–30, Tables 1–3 and refs. 1–28.

Supplementary Video 1

Integration of a modular electrical phytoactuator with other platforms.

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Li, W., Matsuhisa, N., Liu, Z. et al. An on-demand plant-based actuator created using conformable electrodes. Nat Electron 4, 134–142 (2021). https://doi.org/10.1038/s41928-020-00530-4

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