Biohybrid Energy Storage Circuits Based on Electronically Functionalized Plant Roots.

Biohybrid systems based on plants integrate plant structures and processes into technological components targeting more sustainable solutions. Plants' biocatalytic machinery, for example, has been leveraged for the organization of electronic materials directly in the vasculature and roots of living plants, resulting in biohybrid electrochemical devices. Among other applications, energy storage devices were demonstrated where the charge storage electrodes were seamlessly integrated into the plant tissue. However, the capacitance and the voltage output of a single biohybrid supercapacitor are limited. Here, we developed biohybrid circuits based on functionalized conducting roots, extending the performance of plant based biohybrid energy storage systems. We show that root-supercapacitors can be combined in series and in parallel configuration, achieving up to 1.5 V voltage output or up to 11 mF capacitance, respectively. We further demonstrate that the supercapacitors circuit can be charged with an organic photovoltaic cell, and that the stored charge can be used to power an electrochromic display or a bioelectronic device. Furthermore, the functionalized roots degrade in composting similarly to native roots. The proof-of-concept demonstrations illustrate the potential of this technology to achieve more sustainable solutions for powering low consumption devices such as bioelectronics for agriculture or IoT applications.

Plant electrophysiology with conformable organic electronics: Deciphering the propagation of Venus flytrap action potentials.

Electrical signals in plants are mediators of long-distance signaling and correlate with plant movements and responses to stress. These signals are studied with single surface electrodes that cannot resolve signal propagation and integration, thus impeding their decoding and link to function. Here, we developed a conformable multielectrode array based on organic electronics for large-scale and high-resolution plant electrophysiology. We performed precise spatiotemporal mapping of the action potential (AP) in Venus flytrap and found that the AP actively propagates through the tissue with constant speed and without strong directionality. We also found that spontaneously generated APs can originate from unstimulated hairs and that they correlate with trap movement. Last, we demonstrate that the Venus flytrap circuitry can be activated by cells other than the sensory hairs. Our work reveals key properties of the AP and establishes the capacity of organic bioelectronics for resolving electrical signaling in plants contributing to the mechanistic understanding of long-distance responses in plants.

Flexible Organic Electronic Ion Pump for Flow-Free Phytohormone Delivery into Vasculature of Intact Plants.

Plant vasculature transports molecules that play a crucial role in plant signaling including systemic responses and acclimation to diverse environmental conditions. Targeted controlled delivery of molecules to the vascular tissue can be a biomimetic way to induce long distance responses, providing a new tool for the fundamental studies and engineering of stress-tolerant plants. Here, a flexible organic electronic ion pump, an electrophoretic delivery device, for controlled delivery of phytohormones directly in plant vascular tissue is developed. The c-OEIP is based on polyimide-coated glass capillaries that significantly enhance the mechanical robustness of these microscale devices while being minimally disruptive for the plant. The polyelectrolyte channel is based on low-cost and commercially available precursors that can be photocured with blue light, establishing much cheaper and safer system than the state-of-the-art. To trigger OEIP-induced plant response, the phytohormone abscisic acid (ABA) in the petiole of intact Arabidopsis plants is delivered. ABA is one of the main phytohormones involved in plant stress responses and induces stomata closure under drought conditions to reduce water loss and prevent wilting. The OEIP-mediated ABA delivery triggered fast and long-lasting stomata closure far away from the delivery point demonstrating systemic vascular transport of the delivered ABA, verified delivering deuterium-labeled ABA.

Benchmarking organic electrochemical transistors for plant electrophysiology.

Plants are able to sense and respond to a myriad of external stimuli, using different signal transduction pathways, including electrical signaling. The ability to monitor plant responses is essential not only for fundamental plant science, but also to gain knowledge on how to interface plants with technology. Still, the field of plant electrophysiology remains rather unexplored when compared to its animal counterpart. Indeed, most studies continue to rely on invasive techniques or on bulky inorganic electrodes that oftentimes are not ideal for stable integration with plant tissues. On the other hand, few studies have proposed novel approaches to monitor plant signals, based on non-invasive conformable electrodes or even organic transistors. Organic electrochemical transistors (OECTs) are particularly promising for electrophysiology as they are inherently amplification devices, they operate at low voltages, can be miniaturized, and be fabricated in flexible and conformable substrates. Thus, in this study, we characterize OECTs as viable tools to measure plant electrical signals, comparing them to the performance of the current standard, Ag/AgCl electrodes. For that, we focused on two widely studied plant signals: the Venus flytrap (VFT) action potentials elicited by mechanical stimulation of its sensitive trigger hairs, and the wound response of Arabidopsis thaliana. We found that OECTs are able to record these signals without distortion and with the same resolution as Ag/AgCl electrodes and that they offer a major advantage in terms of signal noise, which allow them to be used in field conditions. This work establishes these organic bioelectronic devices as non-invasive tools to monitor plant signaling that can provide insight into plant processes in their natural environment.

Organic electrochemical neurons and synapses with ion mediated spiking.

Future brain-machine interfaces, prosthetics, and intelligent soft robotics will require integrating artificial neuromorphic devices with biological systems. Due to their poor biocompatibility, circuit complexity, low energy efficiency, and operating principles fundamentally different from the ion signal modulation of biology, traditional Silicon-based neuromorphic implementations have limited bio-integration potential. Here, we report the first organic electrochemical neurons (OECNs) with ion-modulated spiking, based on all-printed complementary organic electrochemical transistors. We demonstrate facile bio-integration of OECNs with Venus Flytrap (Dionaea muscipula) to induce lobe closure upon input stimuli. The OECNs can also be integrated with all-printed organic electrochemical synapses (OECSs), exhibiting short-term plasticity with paired-pulse facilitation and long-term plasticity with retention >1000 s, facilitating Hebbian learning. These soft and flexible OECNs operate below 0.6 V and respond to multiple stimuli, defining a new vista for localized artificial neuronal systems possible to integrate with bio-signaling systems of plants, invertebrates, and vertebrates.