Skip to main content

Thank you for visiting nature.com. You are using a browser version with limited support for CSS. To obtain the best experience, we recommend you use a more up to date browser (or turn off compatibility mode in Internet Explorer). In the meantime, to ensure continued support, we are displaying the site without styles and JavaScript.

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

Nature Electronics volume 4, pages 134–142 (2021)Cite this article

Subjects

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.

This is a preview of subscription content, access via your institution

Relevant articles

Open Access articles citing this article.

Access options

Rent or buy this article

Prices vary by article type

from$1.95

to$39.95

Learn more

Prices may be subject to local taxes which are calculated during checkout

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

    Article  Google Scholar 

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

    Article  Google Scholar 

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

    Article  Google Scholar 

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

    Article  Google Scholar 

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

    Article  Google Scholar 

  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).

    Article  Google Scholar 

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

    Article  Google Scholar 

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

    Article  Google Scholar 

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

    Article  Google Scholar 

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

    Article  Google Scholar 

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

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

    Article  Google Scholar 

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

    Article  Google Scholar 

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

    Article  Google Scholar 

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

    Article  Google Scholar 

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

    Article  Google Scholar 

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

    Article  Google Scholar 

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

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

    Article  Google Scholar 

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

    Article  Google Scholar 

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

    Article  Google Scholar 

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

    Article  Google Scholar 

  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).

    Article  Google Scholar 

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

    Article  Google Scholar 

  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).

    Article  Google Scholar 

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

    Article  Google Scholar 

  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).

    Article  Google Scholar 

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

    Article  Google Scholar 

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

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

  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).

    Article  Google Scholar 

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

    Article  Google Scholar 

  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).

    Article  Google Scholar 

  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).

    Article  Google Scholar 

  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).

    Article  Google Scholar 

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

    Article  Google Scholar 

  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).

    Article  Google Scholar 

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

    Article  Google Scholar 

  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).

    Article  Google Scholar 

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

    Article  Google Scholar 

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

    Article  Google Scholar 

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

    Article  Google Scholar 

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

    Article  Google Scholar 

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

    Article  Google Scholar 

Download references

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.

Author information

Authors and Affiliations

  1. Innovative Center for Flexible Devices (iFLEX), Max Planck–NTU Joint Lab for Artificial Senses, School of Materials Science and Engineering, Nanyang Technological University, Singapore, Singapore

    Wenlong Li, Naoji Matsuhisa, Zhiyuan Liu, Ming Wang, Yifei Luo, Pingqiang Cai, Geng Chen, Feilong Zhang, Chengcheng Li, Zhihua Liu, Zhisheng Lv, Wei Zhang & Xiaodong Chen

  2. NTU Institute for Health Technologies, Interdisciplinary Graduate Programme, Nanyang Technological University, Singapore, Singapore

    Wenlong Li

Authors
  1. Wenlong Li
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Naoji Matsuhisa
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Zhiyuan Liu
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Ming Wang
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Yifei Luo
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Pingqiang Cai
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Geng Chen
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Feilong Zhang
    View author publications

    You can also search for this author in PubMed Google Scholar

  9. Chengcheng Li
    View author publications

    You can also search for this author in PubMed Google Scholar

  10. Zhihua Liu
    View author publications

    You can also search for this author in PubMed Google Scholar

  11. Zhisheng Lv
    View author publications

    You can also search for this author in PubMed Google Scholar

  12. Wei Zhang
    View author publications

    You can also search for this author in PubMed Google Scholar

  13. Xiaodong Chen
    View author publications

    You can also search for this author in PubMed Google Scholar

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.

Ethics declarations

Competing interests

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.

Publisher’s note Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

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.

Rights and permissions

Reprints and Permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

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

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1038/s41928-020-00530-4

This article is cited by

Search

Advanced search

Quick links

Nature Briefing

Sign up for the Nature Briefing newsletter — what matters in science, free to your inbox daily.

Get the most important science stories of the day, free in your inbox. Sign up for Nature Briefing