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Sensors and Materials, Vol. 35, No. 10 (2023) 4751–4760
MYU Tokyo
S & M 3427

Continuous Extraction and Electrochemical Monitoringof Potassium Ions in a Plant Leaf Using a Wearable Ion Sensor
Kuniaki Nagamine,1,2* Natsuki Kudo,2 Hajime Sasaki,1
Arina Asano,2 and Shigeyuki Iwasa1
1Graduate School of Organic Materials Science, Yamagata University,

4-3-16 Jonan, Yonezawa, Yamagata 992-8510, Japan

2Faculty of Engineering, Department of Polymeric and Organic Materials Engineering, Yamagata University,

4-3-16 Jonan, Yonezawa, Yamagata 992-8510, Japan.

(Received April 17, 2023; accepted July 27, 2023; online published August 24, 2023)

Keywords: plant, biosensor, smart agriculture

To the best of our knowledge, this is the first study to show the minimally invasive extraction
and continuous monitoring of potassium ions (K+) in a plant leaf, which is one of the mostimportant electrolytes in plant cells. By utilizing the leaching phenomenon, K+ in a leaf was
extracted using an extraction solution, which is composed of phosphate-buffered saline and asurfactant, TritonX-100. K+ sensor films were placed in contact with the leaf surface via a
membrane soaked in the extraction solution to detect K+ extracted from the leaf into theextraction solution. This novel plant-wearable sensor is expected to enable the minimallyinvasive daily monitoring of the chemical compounds in leaves for advancements in plant
healthcare in future agriculture.

1.

Introduction

Recent developments in sensing technologies have enabled the development of various
sensors for achieving smart agriculture. Useful data detected by such sensors include
environmental data, such as temperature, humidity, and carbon dioxide levels; soil data, such as
pH and ion conductivity; and crop image data.(1,2) These data are analyzed and fed back to
cultivation management and harvest timing to improve the productivity and quality of crops.
However, presently, it is difficult to constantly and noninvasively or minimally invasively
monitor the chemical components inside plants, and to the best of our knowledge, no previous
studies on the use of such data have been reported. If the chemical components inside plants canbe constantly monitored, this would enable a more accurate quality control of crops and an early
detection of plant diseases before they become apparent.
Spectroscopic analyses, such as fluorescent spectroscopy,(3) Raman spectroscopy,(4) and nearinfrared spectroscopy,(5,6) have been utilized for the nondestructive detection of chemicalcomponents in plants. Although these analytical techniques are highly sensitive and quantitative,
they require large and expensive analytical systems and a high degree of user expertise.
Recently, the development of miniaturized and wearable sensors for human healthcare has been
*Corresponding author: e-mail: nagamine@yz.yamagata-u.ac.jp

https://doi.org/10.18494/SAM4431

ISSN 0914-4935 © MYU K.K.
https://myukk.org/

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applied in the field of smart agriculture.(7–9) Thin, light-weight, and flexible devices can beplaced on the surfaces of plant leaves and stems to monitor their growth using strain sensors,(10)water loss from plants using humidity sensors,(11) and volatile organic compound emissions fromplants using gas sensors.(12,13) Some chemicals in plants have also been monitored destructively
using chemical sensors, which are inserted into the plant body(14–20) and attached to artificiallyinjured areas of plants.(21–25) Incorporating nanomaterial-based sensors into plant bodies isanother strategy for monitoring the chemicals in plants.(26) However, there have been few studies
on wearable sensors capable of noninvasively or minimally invasively and continuously
monitoring chemical components in plants.
In our previous study, we proposed a new method for the noninvasive detection of bluefluorescent substances in plant leaves.(27) Blue and green fluorescence in intact leaves is emitted
by cinnamic acids, mainly ferulic acid, which are covalently bound to the cell walls of theepidermis, and other fluorescent secondary metabolites. Changes in the fluorescence intensity of
blue-fluorescent substances have been utilized as indicators of plant stress and disease.(3) In ourprevious study, blue-fluorescent substances, including chlorogenic acid, were noninvasively
extracted by placing a hydrogel film on the leaves of a cherry tomato plant, and we found that
their fluorescence intensity increased owing to Ralstonia solanacearum infection. The
mechanism of the release of blue-fluorescent substances from the inside of plants into thehydrogel was based on the leaching phenomenon, where the substances inside plants can bereleased externally through defects, such as micropores, micro-damaged areas, trichome bases,
leaf tips, and edges.(28) The components extracted into the hydrogel using this technique include
blue-fluorescent substances and a variety of chemicals within the plant.
In this study, we demonstrated the feasibility of extracting a potassium ion (K+), which is oneof the most important electrolytes in plant cell physiology, using the leaching phenomenon.
Additionally, a wearable K+ sensor film was placed in contact with the leaf surface via a
membrane soaked with a phosphate-buffered saline (PBS)-based extraction solution to show theminimally invasive extraction and continuous monitoring of K+ in a plant leaf for the first time.

2.

Materials and Methods

2.1

Extraction of K+ in a leaf

A branch of cherry tomatoes (“yellow-mimi”, Solanum lycopersicum cv, or TY Chika;
TTM106) was cut and placed in tap water. To evaluate the effects of the composition of theextraction solution on the efficiency of K+ extraction from a leaf, a tomato leaf was immersed in
0.5 mL of the following extraction solutions for 1 h: ultrapure water (UW), 20 µM PBS (16.2 µM
Na2HPO4, 2.9 µM KH2PO4, 274.0 µM NaCl, and 5.4 µM KCl; pH 7.4) (PBS), ultrapure watercontaining a surfactant, namely, 0.3 mg mL−1 TritonX-100 (Nacalai Tesque, Inc) (UW+T100),
and 20 µM PBS containing 0.3 mg mL−1 TritonX-100 (PBS+T100). To extract K+ absorbed into
the leaf via the foliar absorption pathway, two adjacent leaves were used for subsequent
extraction experiments. One leaf was immersed in 300 µL of extraction solution containing
PBS+T100 and the other leaf was immersed in a foliar absorption solution composed of 0.3 mg

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mL−1 TritonX-100 in 100 mM KCl aqueous solution. The extraction solution was collected every
hour and replaced with a fresh solution. K+ concentrations in the collected extraction solutions
from both experiments were quantified using a K+ meter (LAQUAtwin K-11, Horiba).
2.2

Cytotoxicity test of extraction solution

Cellulose membranes (Whatman™ 3001-861, cytiva) containing the extraction solution (PBS
or PBS+T100) were attached to the surfaces of tomato leaves randomly selected in one tomato
strain for 5 h. After detaching the membranes, the growth of each leaf was monitored bymeasuring the maximum vertical length and maximum width of the leaf. The test was performed
using three different tomato strains (n = 3).
2.3

Fabrication of K+ sensor film

A silver paste (TYPE; FA-323, FUJIKURA KASEI Co., Ltd.) was printed as a lead pattern ona polyethylene naphthalate (PEN; thickness: 125 μm) substrate using a stencil sheet and bakedfor 30 min at 150 °C to evaporate the silver paste solvent. Carbon–graphite ink, including aredox compound of Prussian blue (PB-carbon) (C2070424P2, SunChemical Co.), was painted on
the active area using a stencil sheet, followed by drying at 60 °C for 30 min. A total of 1 μL ofpoly(3,4-ethylenedioxythiophene):polystyrene sulfonate (PEDOT:PSS; Clevious P Jet700,
Heraeus) was drop-casted onto the PB-carbon area as an interfacial ion–electron transducer tominimize the potential drift of the sensors, followed by annealing at 80 °C for 15 min. Finally, 10µL of mixture solution for the K+-selective membrane was drop-casted on the PEDOT:PSS/PBcarbon area and dried for 15 min at 60 °C. The mixture solution for the K+-selective membrane
was prepared by dissolving 2 mg of valinomycin (Nacalai Tesque), 0.25 mg of potassium tetrakis(4-chlorophenyl)borate (Sigma-Aldrich), 16.35 mg of poly(vinyl chloride) (Sigma-Aldrich), and35.5 µL of bis(2-ethylhexyl) sebacate (Tokyo Chemical Industry) in 275 μL of tetrahydrofuran(Tokyo Chemical Industry). The resulting sensor electrode was immersed in a conditioning
solution (100 mM KCl aqueous solution) for 1 h before use.
A liquid-junction silver (Ag)/silver chloride (AgCl) reference electrode was fabricated on thesame substrate as the K+-selective electrode by screen printing. The silver paste (TYPE; FA-323,
FUJIKURA KASEI Co., Ltd.) was printed on a PEN substrate as a lead pattern and baked for 30
min at 120 °C to evaporate the silver paste solvent. Subsequently, Ag/AgCl paste (Code No.
C2130809D5, Sun Chemical) was printed on the active area of the Ag-lead pattern and baked for
30 min at 120 °C. The internal electrolyte paste, 50 wt% of polyvinylpyrrolidone (molecularweight is 40,000; Kanto Kagaku), was mixed in a saturated KCl aqueous solution withdimethyl sulfoxide (Fujifilm Wako Pure Chemical) in a 1:3 ratio and screen-printed over the
Ag/AgCl active layer and baked for 30 min at 30 °C in vacuum. Next, a nitrocellulose membrane
was placed as a liquid junction on the internal electrolyte layer and the entire structure wascovered, except for the tip of the liquid junction, with a screen-printed ultraviolet (UV)-curable
insulator paste (JELCON, No. IN-15M, Jujo Chemical Co., Ltd.) and irradiated with 302 nm UV
for 15 min.

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The potentiometric response of the resulting K+ sensor film was measured using themeasurement solutions. Concentrated KCl solution was periodically added into the measurement
solution and continuously stirred at 200 rpm while monitoring the potential difference between
the working and reference electrodes using the electrochemical analyzer (ALS model 602E, BAS
Inc.) operated in the open-circuit potential mode (input impedance: 1 × 1012 Ω).
2.4

Extraction and detection of K+ in a leaf using K+ sensor film

Tobacco (Nicotiana tabacum L. cv., Tsukuba ichi-gou, Japan tobacco) was grown indoors
under illumination of a light-emitting diode (approximately 3000 lx) for 12 h per day in pots
containing commercial potting soil (Tachikawa Heiwa Nouen). A tobacco leaf was cut, and two
K+ sensor films were placed on it separately. A cotton cellulose fiber (BEMCOT™ M-1, Asahi
Kasei) containing 0.3 mg mL−1 TritonX-100 and 100 mM KCl aqueous solution was wrappedaround the petiole of the tobacco leaf to introduce K+ into the leaf. The K+ sensor film was
attached to the tobacco leaf such that the K+-selective membrane was in contact with the leaf
surface via a cellulose membrane (Whatman™ 3001-861, cytiva) containing the extraction
solution. Each sensor was connected to different electrochemical analyzers to simultaneously
detect the extracted K+ in each area.

3.

Results and Discussion

First, the effects of the composition of the extraction solution on the efficiency of K+
extraction from leaves were investigated by immersing the tomato leaves in the extraction
solutions for 1 h [Fig. 1(a)]. The concentration of K+ in the PBS (8.3 µM) was designed to be lessthan the concentrations of K+ in the tomato xylem sap (30–40 mM)(29) to maintain aconcentration gradient that allows K+ to diffuse out of the leaf. The extraction solutions werecollected to quantify the extracted K+ concentration using a commercially available potassium
ion meter. Figure 1(b) shows the concentration of the extracted K+ normalized by the weight of
the leaf (indicated as µM/mg-leaf). The average values of the normalized K+ concentrationslightly increased when PBS was used instead of UW. Considering the high ion concentration in
the leaf, when ultrapure water was used as the extraction solution, the ultrapure water would
move into the leaf because the osmotic pressure was higher in the leaf, and this might prevent theextraction of K+ using the concentration gradient. The use of PBS as an extraction solution
slightly increased the amount of the extracted K+ probably because of the slightly smallerdifference in osmotic pressure between the leaf and the extraction solution.
Adding TritonX-100 into the extraction solution also caused a slight increase in the averagevalues of the normalized K+ concentration. TritonX-100 is a surfactant that can cause a cytotoxic
effect on the cell membrane. Therefore, we tested the cytotoxicity of TritonX-100 by comparing
the growth of the tomato leaves untreated and treated with the extraction solution as follows. The
cellulose membranes containing the extraction solution (PBS or PBS+T100) were attached to thesurfaces of tomato leaves randomly selected in one tomato strain for 5 h. After detaching themembranes, the growth of each leaf was monitored by measuring the maximum vertical length

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Fig. 1. (Color online) (a) Photograph of a tomato leaf immersed in extraction solution: ultrapure water (UW), 20µM PBS (PBS), UW containing 0.3 mg mL−1 TritonX-100 (UW+T100), and 20 µM PBS containing 0.3 mg mL−1
TritonX-100 (PBS+T100). (b) Concentrations of extracted potassium ions normalized by the weight of the leaf
(indicated as µM/mg-leaf) (n = 3). (c) Rates of changes in maximum vertical length and maximum width in tomato
leaves before and eight days after detaching the membrane containing PBS or PBS+T100 (n = 3).

and the maximum width as shown in the photograph in Fig. 1(c). Figure 1(c) shows the rates ofchanges in maximum vertical length and maximum width in tomato leaves before and eight days
after detaching the membrane containing PBS or PBS+T100. As a control experiment, the leaf
without membrane treatment was also observed. In the Y-axis, 1.0 means no change in leaf
length eight days after the treatment. There was little difference in leaf growth rate under all
conditions (Rate = 1.2–1.4), suggesting the minimal cytotoxicity of TritonX-100. However, thisneeds further study. Therefore, we called this extraction technique “minimally invasive
extraction”. On the basis of these results, we used PBS+T100 as the extraction solution in thenext experiments.
Figure 2(a) shows the setup for extracting K+ from tomato leaves via leaching. Two adjacent
leaves were used for this extraction experiment. One leaf was immersed in the extraction
solution, PBS+T100, and the other leaf was in the foliar absorption solution containing 0.3 mg

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Fig. 2. (Color online) (a) Setup for potassium ion (K+) extraction absorbed into leaf by foliar absorption pathway.
(b) Change in K+ concentration extracted into extraction solution with and without foliar absorption in a differentleaf.

mL−1 TritonX-100 and 100 mM KCl aqueous solution. In this configuration, we expected that
the K+ absorbed by the leaf would be transported to the next leaf through the foliar fertilization
pathway(30,31) and then extracted into the extraction solution. The extraction solution wascollected every hour and replaced with a fresh solution. The K+ concentration in the collected
extraction solution was quantified using a commercially available potassium ion meter. Figure2(b) shows the time course against the detected concentration of K+ in the extraction solution.
The concentration of the extracted K+ gradually increased. However, when the next leaf was not
immersed in the foliar absorption solution, no marked change in the concentration of theextracted K+ was observed. This result suggested that the K+ absorbed into the plant by the
aforementioned pathway was extracted into the extraction solution via leaching. In other words,
the K+ extracted into the extraction solution was suggested to be derived from the K+ in a tomato
leaf.
The K+ extracted into the extraction solution was continuously monitored using a wearable K+
sensor film. Figures 3(a) and 3(b) show the structure and photograph of the K+ sensor film,
respectively. The valinomycin-based K+-selective membrane was used to cover the active area ofthe carbon electrode via a PEDOT:PSS-based interfacial ion–electron transducer layer, which
had the same structure as in our previous study.(32) The liquid-junction Ag/AgCl referenceelectrode composed of a Ag/AgCl electrode pattern covered with an internal electrolyte layer
and an insulation layer was fabricated on the same substrate. The internal electrolyte layer wasconnected to the outer measurement solution through a nitrocellulose-membrane-based liquidjunction. Figure 3(c) shows the representative potentiometric responses of the K+ sensor film in
the KCl aqueous solution and the extraction solution (PBS+T100). Both graphs were obtainedusing the same sensor film. The sensor showed a quick and stable response regarding the change
in K+ concentration in the concentration range from 0.1 to 10 mM even in the extraction solution.
Figure 3(d) shows the relationship between the K+ concentration and the detected potential. In

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Fig. 3. (Color online) (a) Structure of potassium ion (K+) sensor film. (b) Photograph of K+ sensor film. (c)Potentiometric responses of K+ sensor film in potassium chloride (KCl) aqueous solution and extraction solution. (d)Potentials against K+ concentration were detected in the KCl aqueous solution and extraction solution. (e) Potential
stability of liquid-junction Ag/AgCl electrode against a commercially available Ag/AgCl reference electrode.

the KCl aqueous solution, the slope was 52.2 ± 4.7 mV/dec (n = 4), which is almost the same as
the theoretical Nernst slope. When TritonX-100 was added to the KCl aqueous solution, theslope decreased to 90.2% of that within the KCl aqueous solution. Additionally, in the extraction
solution, the slope decreased to 73.5% of that within the KCl aqueous solution probably because
the surfactant-mediated extraction of interfering ions affected the interfacial K+ selectivity of thesensor membrane.(33). Figure 3(e) shows the potential stability of the liquid-junction Ag/AgClelectrode against a commercially available Ag/AgCl reference electrode in 20 µM PBS. Afterapproximately 15 min of setup, when the measurement solution gradually entered into theinternal electrolyte layer through the liquid junction to ionically connect the inside and outsideof the reference electrode, the electrode showed a stable potential for more than 3 h. The potential
drift from 1 to 3 h was 2.1 mV/h, which is a sufficient operational time for the experimentdescribed in Fig. 4.
The minimally invasive extraction and continuous monitoring of K+ in plant leaves were
demonstrated using a wearable K+ sensor film. Figure 4(a) shows a photograph of theexperimental setup. Two K+ sensor films were separately placed on a tobacco leaf via a
membrane containing the extraction solution. Tobacco leaves were used in this study because of
their large surface area for examining the distribution of K+ introduced into the leaves. A cotton
cellulose fiber containing 0.3 mg mL−1 TritonX-100 and 100 mM KCl aqueous solution was
wrapped around the petiole of the tobacco leaf to introduce K+ from the cut surface of the petiole

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Fig. 4. (Color online) (a) Photograph of experimental setup. (b) Time courses of K+ concentration detected at
positions (i) and (ii) in (a) after introducing K+ into leaf.

into the leaf. Each sensor was connected to different electrochemical analyzers to simultaneously
detect the extracted K+ in each area. Figure 4(b) shows the time course of the detected K+
concentration after introducing K+ into the leaf. The potentials were converted into K+
concentrations using a calibration curve obtained from the extraction solution. The response of
the sensor at position (i) increased gradually, suggesting the continuous extraction and detectionof the K+ introduced in the leaf. The response of the sensor at position (ii) showed a slow change
probably because of the slow diffusion of K+ in the complex transport pathways.(30) The slopes of
the two sensors were evaluated in the KCl aqueous solution before and after the measurementsof 51.9 and 55.5 mV/dec for position (i) and 53.4 and 54.6 mV/dec for position (ii), suggesting thestability of the sensor response during these experiments. To the best of our knowledge, this is
the first study to show the minimally invasive extraction and continuous monitoring of chemicalcompounds in plant leaves utilizing the leaching phenomenon.

4.

Conclusions

In this study, we found that K+ in plant leaves can be extracted in a minimally invasive
manner by utilizing the leaching phenomenon. The extracted K+ was successfully andcontinuously detected using a K+ sensor film that was in contact with the plant leaf via an
extraction solution-soaked membrane. However, the present sensor has some limitations
regarding long-term monitoring because the soaked extraction solution in the membrane
gradually evaporated during measurements. Furthermore, it is unclear whether theconcentrations of the extracted compounds quantitatively reflect their chemical composition in
the leaves. Our further studies are focused on improving the wet interfacing materials andanalyzing the relationship of the extracted (in the extraction solution) and unextracted
compounds of the plant leaves to open up opportunities for the digital management of thecultivation and harvesting of crops in future agriculture.

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Acknowledgments
This research was supported by JSPS KAKENHI, Grant Number JP23736844.

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