Graphical Abstract
![](https://wqketang.oss-cn-beijing.aliyuncs.com/unzip/large-zip/zip-2a02756c-9a3e-46eb-b900-8aa2a7a59dfe/5621/files/5621-TOC.jpg?Expires=1725757723&OSSAccessKeyId=STS.NT5eViCkqzTYdbfdqxMkjpyyq&Signature=0v6ZaOWiZk%2F0Ki6yb%2FysuyemqjE%3D&security-token=CAISywJ1q6Ft5B2yfSjIr5eALuzdrrRQzZayZkTXgHEtQeRGn7zSkzz2IHtKenhsBOsbtfk1mG5W5%2FgZlqJ9SptIAEfJa9d99MzUP%2FpFltCT1fau5Jko1beHewHKeTOZsebWZ%2BLmNqC%2FHt6md1HDkAJq3LL%2Bbk%2FMdle5MJqP%2B%2FUFB5ZtKWveVzddA8pMLQZPsdITMWCrVcygKRn3mGHdfiEK00he8TouufTinpHMskGA1Aell7Mvyt6vcsT%2BXa5FJ4xiVtq55utye5fa3TRYgxowr%2Fwo0v0YpGya5YzHXwcPskvdKZbo78UqLQlla6w%2BGqFJqvPxr%2Fp8t%2Fx5fWJKAezhVgs8cVM8JOjIqKOscIsiJsO71SmqFV55c8Fdm%2BgUooJVgIMhTnduUfAPJAGOxzJitP%2BUVGGphr60TEnBL4rB5MUctfzRp75SXVPUTzDnGoABjuNLcf76FQN6p3t%2BSlCg%2FxR5C72RIk78k%2BUi44L9ZBmFT6F8GV7aXA52D1Ps56knKF6PAnhRivwyTxgsolycBfvccb3t5jGJ24SgY0aYosAECutxAo7sJhSwlwZvGwGDZJsop1vGiZ8eN1MbtZeRRuMeaZ2I%2BQo%2BnVP6Cf%2F0pDsgAA%3D%3D)
Discover the SciOpen Platform and Achieve Your Research Goals with Ease.
Because of its adaptive interfacial property, soft sensors/actuators can be used to perform more delicate tasks than their rigid counterparts. However, plant epidermis with a waxy cuticle layer challenges stable and high-fidelity non-invasive electrophysiology since the conventional electrodes are invasive, easily detached from plants, and require complicated setup procedures. Here, we report a bioinspired sensor and actuator created by using a conformable electrode interface as an electrical modulation unit on a Venus flytrap. Our conformable electrode, by employing an adhesive hydrogel layer, can achieve the merits of low impedance, stretchable, biocompatible, reusable, and transparent enough for normal chlorophyll activity to occur. Owing to the high sensitivity of a flytrap to a triggering mechanical stimulation, a plant sensor matrix based on flytraps has been demonstrated by capturing the stimulated action potential (AP) signals from upper epidermis, which can orient honeybee colonies by their touch during collecting nectar. Moreover, via frequency-dependent AP modulation, an autonomous on-demand actuation on a flytrap is realized. The flytrap actuator can be controlled to responsively grasp tiny objects by the modulated signals triggered by a triboelectric nanogenerator (TENG). This work paves a way of developing autonomous plant-based sensors and actuators toward smart agriculture and intelligent robots.
Tonn, N.; Greb, T. Radial plant growth. Curr. Biol. 2017, 27, R878–R882.
Dresselhaus, T.; Sprunck, S.; Wessel, G. M. Fertilization mechanisms in flowering plants. Curr. Biol. 2016, 26, R125–R139.
Luo, Y. F.; Li, W. L.; Lin, Q. Y.; Zhang, F. L.; He, K.; Yang, D. P.; Loh, X. J.; Chen, X. D. A morphable ionic electrode based on thermogel for non-invasive hairy plant electrophysiology. Adv. Mater. 2021, 33, 2007848.
Xie, J. J.; Wu, Y. Y.; Xing, D. K.; Li, Z. Y.; Chen, T.; Duan, R. R.; Zhu, X. X. A comparative study on the circadian rhythm of the electrical signals of Broussonetia papyrifera and Morus alba. Plant Signal. Behav. 2021, 16, 1950899.
Awan, H.; Adve, R. S.; Wallbridge, N.; Plummer, C.; Eckford, A. W. Communication and information theory of single action potential signals in plants. IEEE Trans. NanoBiosci. 2019, 18, 61–73.
Li, J. H.; Fan, L. F.; Zhao, D. J.; Zhou, Q.; Yao, J. P.; Wang, Z. Y.; Huang, L. Plant electrical signals: A multidisciplinary challenge. J. Plant Physiol. 2021, 261, 153418.
Najdenovska, E.; Dutoit, F.; Tran, D.; Plummer, C.; Wallbridge, N.; Camps, C.; Raileanu, L. E. Classification of plant electrophysiology signals for detection of spider mites infestation in tomatoes. Appl. Sci. 2021, 11, 1414.
Novacky, A.; Karr, A. L.; van Sambeek, J. W. Using electrophysiology to study plant disease development. BioScience 1976, 26, 499–504.
Ochatt, S. Plant cell electrophysiology: Applications in growth enhancement, somatic hybridisation and gene transfer. Biotechnol. Adv. 2013, 31, 1237–1246.
Lin, V. S. Interrogating plant-microbe interactions with chemical tools: Click chemistry reagents for metabolic labeling and activity-based probes. Molecules 2021, 26, 243.
Griffiths, C. A.; Sagar, R.; Geng, Y. Q.; Primavesi, L. F.; Patel, M. K.; Passarelli, M. K.; Gilmore, I. S.; Steven, R. T.; Bunch, J.; Paul, M. J. et al. Chemical intervention in plant sugar signalling increases yield and resilience. Nature 2016, 540, 574–578.
Mousavi, S. A. R.; Chauvin, A.; Pascaud, F.; Kellenberger, S.; Farmer, E. E. GLUTAMATE RECEPTOR-LIKE genes mediate leaf-to-leaf wound signalling. Nature 2013, 500, 422–426.
Markin, V. S.; Volkov, A. G.; Jovanov, E. Active movements in plants: Mechanism of trap closure by Dionaea muscipula Ellis. Plant Signal. Behav. 2008, 3, 778–783.
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 2019, 5, 670–675.
Hedrich, R.; Neher, E. Venus flytrap: How an excitable, carnivorous plant works. Trends Plant Sci. 2018, 23, 220–234.
Li, W. L.; Matsuhisa, N.; Liu, Z. Y.; Wang, M.; Luo, Y. F.; Cai, P. Q.; Chen, G.; Zhang, F. L.; Li, C. C.; Liu, Z. H. et al. An on-demand plant-based actuator created using conformable electrodes. Nat. Electron. 2021, 4, 134–142.
Volkov, A. G. Signaling in electrical networks of the Venus flytrap (Dionaea muscipula Ellis). Bioelectrochemistry 2019, 125, 25–32.
Dechiraju, H.; Jia, M. P.; Luo, L.; Rolandi, M. Ion-conducting hydrogels and their applications in bioelectronics. Adv. Sustain. Syst. 2022, 6, 2100173.
Miyamoto, A.; Lee, S.; Cooray, N. F.; Lee, S.; Mori, M.; Matsuhisa, N.; Jin, H.; Yoda, L.; Yokota, T.; Itoh, A. et al. Inflammation-free, gas-permeable, lightweight, stretchable on-skin electronics with nanomeshes. Nat. Nanotechnol. 2017, 12, 907–913.
Liu, Y. X.; Liu, J.; Chen, S. C.; Lei, T.; Kim, Y.; Niu, S. M.; Wang, H. L.; Wang, X.; Foudeh, A. M.; Tok, J. B. H. et al. Soft and elastic hydrogel-based microelectronics for localized low-voltage neuromodulation. Nat. Biomed. Eng. 2019, 3, 58–68.
Stavrinidou, E.; Gabrielsson, R.; Gomez, E.; Crispin, X.; Nilsson, O.; Simon, D. T.; Berggren, M. Electronic plants. Sci. Adv. 2015, 1, e1501136.
Wong, M. H.; Giraldo, J. P.; Kwak, S. Y.; Koman, V. B.; Sinclair, R.; Lew, T. T. S.; Bisker, G.; Liu, P. W.; Strano, M. S. Nitroaromatic detection and infrared communication from wild-type plants using plant nanobionics. Nat. Mater. 2017, 16, 264–272.
Adeel Zafar, S.; Uzair, M.; Ramzan Khan, M.; Patil, S. B.; Fang, J. J.; Zhao, J. F.; Singla-Pareek, S. L.; Pareek, A.; Li, X. Y. DPS1 regulates cuticle development and leaf senescence in rice. Food Energy Secur. 2021, 10, e273.
Harikesh, P. C.; Yang, C. Y.; Tu, D. Y.; Gerasimov, J. Y.; Dar, A. M.; Armada-Moreira, A.; Massetti, M.; Kroon, R.; Bliman, D.; Olsson, R. et al. Organic electrochemical neurons and synapses with ion mediated spiking. Nat. Commun. 2022, 13, 901.
Volkov, A. G.; Adesina, T.; Jovanov, E. Closing of Venus flytrap by electrical stimulation of motor cells. Plant Signal. Behav. 2007, 2, 139–145.
Volkov, A. G.; Adesina, T.; Jovanov, E. Charge induced closing of Dionaea muscipula Ellis trap. Bioelectrochemistry 2008, 74, 16–21.
Karban, R. Plant communication. Annu. Rev. Ecol. Evol. Syst. 2021, 52, 1–24.
Mousavi, S. A. R.; Nguyen, C. T.; Farmer, E. E.; Kellenberger, S. Measuring surface potential changes on leaves. Nat. Protoc. 2014, 9, 1997–2004.
Pavloviič, A.; Jakšová, J.; Novák, O. Triggering a false alarm: Wounding mimics prey capture in the carnivorous Venus flytrap (Dionaea muscipula). New Phytol. 2017, 216, 927–938.
Zhou, P. D.; Lin, J.; Zhang, W.; Luo, Z. L.; Chen, L. Z. Pressure-perceptive actuators for tactile soft robots and visual logic devices. Adv. Sci. 2022, 9, 2104270.
Liao, X. Q.; Wang, W. S.; Wang, L.; Jin, H. R.; Shu, L.; Xu, X. M.; Zheng, Y. J. A highly stretchable and deformation-insensitive bionic electronic exteroceptive neural sensor for human-machine interfaces. Nano Energy 2021, 80, 105548.
Zhou, P. D.; Zhang, W.; Chen, L. Z.; Lin, J.; Luo, Z. L.; Liu, C. H.; Jiang, K. L. Monolithic superaligned carbon nanotube composite with integrated rewriting, actuating and sensing multifunctions. Nano Res. 2021, 14, 2456–2462.
Meder, F.; Saar, S.; Taccola, S.; Filippeschi, C.; Mattoli, V.; Mazzolai, B. Ultraconformable, self-adhering surface electrodes for measuring electrical signals in plants. Adv. Mater. Technol. 2021, 6, 2001182.
Kim, D. H.; Lu, N. S.; Ma, R.; Kim, Y. S.; Kim, R. H.; Wang, S. D.; Wu, J.; Won, S. M.; Tao, H.; Islam, A. et al. Epidermal electronics. Science 2011, 333, 838–843.
Kim, J. J.; Allison, L. K.; Andrew, T. L. Vapor-printed polymer electrodes for long-term, on-demand health monitoring. Sci. Adv. 2019, 5, eaaw0463.
Rohaizad, N.; Mayorga-Martinez, C. C.; Novotný, F.; Webster, R. D.; Pumera, M. 3D-printed Ag/AgCl pseudo-reference electrodes. Electrochem. Commun. 2019, 103, 104–108.
Li, G. J.; Hu, S. Q.; Yang, J. J.; Schultz, E. A.; Clarke, K.; Hou, H. W. Water-Wisteria as an ideal plant to study heterophylly in higher aquatic plants. Plant Cell Rep. 2017, 36, 1225–1236.
Yang, Y.; Zhang, H. L.; Chen, J.; Jing, Q. S.; Zhou, Y. S.; Wen, X. N.; Wang, Z. L. Single-electrode-based sliding triboelectric nanogenerator for self-powered displacement vector sensor system. ACS Nano 2013, 7, 7342–7351.
Wang, Z. L. On the first principle theory of nanogenerators from Maxwell's equations. Nano Energy 2020, 68, 104272.
Fan, F. R.; Tian, Z. Q.; Wang, Z. L. Flexible triboelectric generator. Nano Energy 2012, 1, 328–334.
Wang, Z. L.; Wang, A. C. On the origin of contact-electrification. Mater. Today 2019, 30, 34–51.