Implantable Organic Electronic Ion Pump Enables ABA Hormone Delivery for Control of Stomata in an Intact Tobacco Plant

Abstract

Organic bioelectronic devices comprise advanced tools for monitoring and controlling physiology. [1] Such devices are based upon organic electronic materials that offer efficient signal transduction from electronic input to ionic output and vice versa, while the toolbox of organic chemistry enables design and tailoring of active materials with desired characteristics, such as functionality, processability, and biocompatibility. [2] Organic bioelectronic devices and materials have been applied in a variety of settings with most of the technologic development focused on neuroscience applications such as high resolution recordings of brain activity, [3] inhibition of neuropathic pain, [4] control of epileptic seizures, [5] and understanding of memory consolidation [6] in animal models. While the field of organic bioelectronics has traditionally targeted biomedical applications, its usefulness and applicability in plants has begun to be explored. Glucose export from isolated chloroplasts was monitored in real time using an organic electrochemical transistor, [7] while the growth of a plant was controlled via the organic electronic ion pump (OEIP). [8] The OEIP is an electrophoretic delivery device that converts electronic addressing signals into ionic fluxes offering precise and dynamic delivery of ions and charged biomolecules. [9] In contrast to other drug delivery devices, the OEIP has a simple design, forgoes flow pumps, and delivers only the ion or drug of interest, and not the solvent or dissolved coions. Drug delivery in the absence of fluid flow eliminates convective disturbances of the target fluidic system, such as shear stress, local pressure increases, and excessive perturbation of native ionic concentration gradients. The OEIP technology is based on a polyelectrolyte channel that provides charge selective electrophoretic delivery thanks to its high fixed ionic charge concentration that suppresses the transport of coions. When voltage is applied across the polyelectrolyte channel of an OEIP device, ions of a specific charge are transported selectively through the channel from the source to the target. Conventional OEIP devices have typically utilized planar geometries and have been manufactured using standard microfabrication techniques. [10] The delivery channel Electronic control of biological processes with bioelectronic devices holds promise for sophisticated regulation of physiology, for gaining fundamental understanding of biological systems, providing new therapeutic solutions, and digitally mediating adaptations of organisms to external factors. The organic electronic ion pump (OEIP) provides a unique means for electronically-controlled, flow-free delivery of ions, and biomolecules at cellular scale. Here, a miniaturized OEIP device based on glass capillary fibers (c-OEIP) is implanted in a biological organism. The capillary form factor at the sub-100 µm scale of the device enables it to be implanted in soft tissue, while its hyperbranched polyelectrolyte channel and addressing protocol allows eff...

Diurnal in vivo xylem sap glucose and sucrose monitoring using implantable organic electrochemical transistor sensors

“…Organic electronic devices can be advantageous when applied in the biological milieu since organic electronic materials support sufficient electronic and ionic transport ( Paulsen et al, 2020 ), in a highly coupled manner, and thus enable efficient signal transduction. While the majority of efforts lie within the animal kingdom, applying bioelectronics to other biological organisms has emerged with successful demonstrations of sensing and actuation in bacteria ( He et al., 2012 ; Pitsalidis et al, 2018 ; Zajdel et al., 2018 ; Demuru et al., 2019 ; Di Lauro et al, 2020 ) and plants ( Stavrinidou et al., 2015 , 2017 ; Coppedè et al., 2017 ; Poxson et al., 2017 ; Bernacka-Wojcik et al, 2019 ; Janni et al, 2019 ; Kim et al., 2019 ; Vurro et al, 2019 ; Diacci et al, 2020 ). Recently, we presented an implantable organic electronic ion pump for in vivo delivery of abscisic acid, one of the main hormones involved in plant stress responses ( Bernacka-Wojcik et al, 2019 ), and subsequently the electronic control of physiology in intact plants.…”

Organic Bioelectronics: From Functional Materials to Next‐Generation Devices and Power Sources

“…[90] For each electronic charge that goes through the external circuit, one ionic charge (i.e., a drug) is driven through the membrane. OEIPs enable the voltage-controlled delivery of small metal cations, neurotransmitters (glutamate, [107] aspartate, [107] salicylic acid, [108] γ-amino butyric acid-GABA, [92,93,109] acetylcholine, [93,96,107,109] dopamine [110] ) and hormones (abscisic acid) [111] to induce neural activity, that can suppress epileptiform activity, treat pain-causing neurons locally, and even regulate the physiology of plants. Thanks to the large volumetric capacitance of PEDOT:PSS and the processability of their associated components, OEIPs can be made in microscale configurations.…”

Targeted Chemotherapy of Glioblastoma Spheroids with an Iontronic Pump

“…To date, this technology has been successfully applied to the delivery of neurotransmitters in vitro and in vivo, [ 11 ] plant hormones, [ 12,13 ] and modulators of inflammation in vitro, [ 14 ] though not, to our knowledge, to the delivery of anti‐cancerous chemotherapeutics. OEIP‐based delivery has the potential to create high drug concentrations in a controllable manner, precisely at the site of tumor resection with high spatiotemporal resolution.…”

“…OEIP delivery, which comprises electrophoresis through a cation or anion-exchange membrane (CEM or AEM, respectively), ensures that the electronic current precisely corresponds to the ionic (drug) delivery current and thus provides precise dosage control. [10] To date, this technology has been successfully applied to the delivery of neurotransmitters in vitro and in vivo, [11] plant hormones, [12,13] and modulators of inflammation in vitro, [14] though not, to our knowledge, to the delivery of anti-cancerous chemotherapeutics. OEIP-based delivery has the potential to create high drug concentrations in a controllable manner, precisely at the site of tumor resection with high spatiotemporal resolution.…”