graphite strain sensor for real-time monitoring of plant growth

Accepted Manuscript Rapid fabrication of wearable carbon nanotube/graphite strain sensor for real-time monitoring of plant growth Wenzhi Tang, Tingting Yan, Fei Wang, Jingxian Yang, Jian Wu, Jianlong Wang, Tianli Yue, Zhonghong Li PII:

S0008-6223(19)30225-8

DOI:

https://doi.org/10.1016/j.carbon.2019.03.002

Reference:

CARBON 14007

To appear in:

Carbon

Received Date: 13 December 2018 Revised Date:

16 February 2019

Accepted Date: 1 March 2019

Please cite this article as: W. Tang, T. Yan, F. Wang, J. Yang, J. Wu, J. Wang, T. Yue, Z. Li, Rapid fabrication of wearable carbon nanotube/graphite strain sensor for real-time monitoring of plant growth, Carbon (2019), doi: https://doi.org/10.1016/j.carbon.2019.03.002. This is a PDF file of an unedited manuscript that has been accepted for publication. As a service to our customers we are providing this early version of the manuscript. The manuscript will undergo copyediting, typesetting, and review of the resulting proof before it is published in its final form. Please note that during the production process errors may be discovered which could affect the content, and all legal disclaimers that apply to the journal pertain.

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ACCEPTED MANUSCRIPT Rapid fabrication of wearable carbon nanotube/graphite strain sensor for real-time monitoring of plant growth Wenzhi Tang,1,2,3 Tingting Yan,1,2,3 Fei Wang,1,2,3 Jingxian Yang,1,2,3 Jian Wu,4

College of Food Science and Engineering, Northwest A&F University, Yangling,

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Jianlong Wang,1 Tianli Yue, 1,2,3 Zhonghong Li 1,2,3*

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Shaanxi 712100, China

Laboratory of Quality & Safety Risk Assessment for Agro-products (Yangling),

Ministry of Agriculture, Yangling, Shaanxi 712100, China 3

National Engineering Research Center of Agriculture Integration Test (Yangling),

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Yangling, Shaanxi 712100, China

College of Biosystems Engineering and Food Science, Zhejiang University, 866

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Yuhangtang Road, Hangzhou 310058, China

* Corresponding author. Tel: +86 29 87038857. E-mail: [email protected]; [email protected] (Zhonghong Li) 1

ACCEPTED MANUSCRIPT Abstract Quantitative and precise measurement of plant growth is the foundation for the understanding of mechanisms that regulate the growth of plant. Plant growth is a

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highly dynamic process that could start/stop within seconds, but existing methods provide little information on the dynamic growth due to insufficient resolution. Here, we report on a simple manufacturing process and materials for wearable strain sensor,

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and a highly sensitive, automatic and real-time approach to assess the growth of plant

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in the range from nanometer level to centimeter level. By taking the synergistic reinforcement between graphite and carbon nanotube (CNT) membranes, a flexible, stretchable and wearable carbon nanotube/graphite sensor was obtained by simply depositing a graphite ink, a CNT ink and solidifying under ambient environment. An

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all-in-one device composed of the sensor and a home-made readout circuit was used to make the real-time measurement of plant growth. The monitoring of Solanum melongena L. and Cucurbita pepo captured the evidence of a rhythmic growth pattern

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for the fruits: the fruits grow rapidly for seconds and then rest for seconds. This

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approach simplified the procedure, reduced the cost, enhanced the speed, and provided nanoscale sensitivity for plant, presenting promising potentials in plant growth measurement.

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ACCEPTED MANUSCRIPT 1. Introduction Global issues such as the forecast of ~10 billion people by the year 2050, the threat of climate change on crop yields are putting heavy pressure on world food supplies [1-3].

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Hence, there is an urgent requirement to ensure the sustainable growth of crop yields to feed the large population. However, the bottleneck in the measurement of plant growth slows down the progress in developing high-yielding crops. Plant growth is a

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key foundation to understand the effects of biological/environmental factors on plant

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growths. It is a highly dynamic process determined by cell division and expansion, which could start/stop within seconds [4-8]. Methods with spatial resolution of nm-scale precision are required to measure the in-depth details on plant growth. Many techniques (e.g., image and image processing, linear variable differential transformers,

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dendrometers) can achieve continuous and non-destructive measurement [9-15]. However, most of them only reach the resolution of micron level, and require complicated instruments, sophisticated data analysis algorithms and frequent reset.

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Although more sensitive devices (i.e., scanning electron microscopies) provide

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nm-scale resolution, they are only suitable for small samples such as cell walls or organelles within the cell, and may require complicated and destructive pre-treatment of plants. So, in-depth and continuous measurements of whole plant/organ growth at nanometer level still remain challenging. Strain sensors are devices to transform mechanical deformations into the change of electrical characteristics (e.g., resistance, capacitance). The development of flexible and stretchable electronics has brought about the wearable strain sensor, which has 3

ACCEPTED MANUSCRIPT drawn tremendous attentions in continuous monitoring of human motions without disturbing or limiting the user’s activities [16-25]. By in-situ fabrication of a strain sensor on plants using graphite powder and chitosan [26], we demonstrated the

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possibility to detect whether a plant was growing at a time scale of seconds. Although this approach was sensitive, the qualitative result limited its application. Besides, the in-situ fabrication was only suitable for hydrophilic plant surfaces. Therefore, strain

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sensors that can be worn on the plant may provide a potential and more general

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approach to realize in-depth and continuous measurements. For this purpose, it is highly desirable to make wearable strain sensors with high sensitivity, broad sensing range, and easy manufacturing process.

Among available sensors, carbon-based strain sensors show great potential to meet

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these requirements. For instance, carbon nanotube (CNT), a flexible 1D nanomaterial, could accommodate to large strain, thereby providing excellent stretchability [25, 27, 28]. Sensors made by 2D carbon materials (e.g., grapheme, graphite) generally

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possess high sensitivities [29-35]. In addition, the sensor could be obtained by simply

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writing on a paper with a pencil [33]. The easy manufacture without the customized equipment, additional chemicals or energy-consuming post-treatments would facilitate the design of diverse configurations and accelerate sensor fabrication for specific requirements [17, 36, 37], which is particularly attractive for plants with different shapes and sizes. Hence, a strategy that combines the excellent stretchability, high sensitivity and the simple fabrication of carbon-based sensors would contribute to the development of wearable sensors for plant measurements. 4

ACCEPTED MANUSCRIPT In this study, we propose an approach that allows the end-user to rapidly fabricate high-performance wearable strain sensor. The sensor was obtained by simply depositing a graphite ink, a CNT ink and curing naturally. The synergistic

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reinforcement between graphite and CNT significantly improved the mechanical stability and stretchability of the sensor. An all-in-one device composed of the sensor and a readout circuit was developed to measure the growths of Solanum melongena L.

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and Cucurbita pepo. The resolution of the device reached nanometer scale and

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revealed that the growth rates were rhythmic at the time scale of seconds. This approach opens up an attractive avenue for quantitative measurement of dynamic plant growth and development of wearable electronics. 2. Experimental

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2.1 Sensor fabrication

Firstly, the outline of a sensor was drawn on a disposable latex glove (Shanghai AMMEX Trade Co., Ltd., China) using the ruler-guided lines by a mark pen, and was

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cut off with a scissors. Then, graphite membrane (GM) was fabricated by depositing

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the graphite ink on the latex piece with a Chinese writing brush or a micropipette. The graphite ink was made by modifying our previous researches [26, 38]. Briefly, 0.058 mL acetic acid and 0.1 g chitosan were mixed with water to a volume of 10 mL. The solution was then mixed with graphite powder (size ≤ 30 µm) at the ratio 4:1 (v: w) for ~1 min. The graphite ink was deposited at 1.6 µL cm-2. GM was obtained by drying naturally for ~12 min. After that, CNT ink (Nanjing XFNANO Materials TECH Co., Ltd, China) was deposited (5 µL cm-2) on the top of GM and curing 5

ACCEPTED MANUSCRIPT naturally to obtain the CNT membrane (CNTM). Copper wires were immobilized with the double side tape (Deli group Co., Ltd, China) to establish electrical contact. The double side tape at one end of the sensor was used to worn the sensor on the plant.

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The design of the readout circuit was shown in Fig. 1D. It used the sensor as a resistor in the oscillator circuit based on a 555 timer working at the astable mode [39], converting the resistance value to a frequency output. A microcontroller (STCmicro

2.2 Characterization of the sensor

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measured resistance on a 1602LCD display.

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Technology Co,.Ltd, China) processed the frequency output and presented the

Microstructures of GM, CNTM and GM/CNTM were characterized with a Nova NanoSEM 450 (FEI, Netherlands). The SEM images of the sensor under strain were

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obtained by stretching the sensor and then immobilizing it on a PVC substrate with the double side tape. The Movie of GM/CNTM under strain loads was recorded by a digital microscope (Andonstar Tech. Co., Ltd., China). Both a LCR (inductance,

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capacitance and resistance) meter (Agilent, the USA) and a CHI 840D

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electrochemical analyzer (CH Instruments, the USA) were used to evaluate the responses of the strain sensors. A computer was used to control the LCR meter and the electrochemical analyzer, and to record the data. Sensor responses to strains were obtained by attaching the sensor (1 × 0.5 cm) on a digital micrometer (Micro Measuring Technology GmbH, Germany). 2.3 Plant growth monitoring Plants were grown in a greenhouse at 20 ± 2 °C. For wearable measurement, the 6

ACCEPTED MANUSCRIPT sensors were worn on the fruits by peeling off the release paper of the adhesive tape at one end of the sensor and pressing the other end on it. Manual measurements of the fruit diameters were performed with a vernier caliper. The data sets collected at

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intervals of seconds were smoothed with a central moving average method to reduce random fluctuations, which was the mean of 7 data points taken from 3 data points on both sides of a central value. To measure the stepwise growth at the nanometer scale,

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wind should be avoided.

3.1 The all-in-one device

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3. Results and discussion

The plant growth measurement was achieved by a strain sensor that transformed mechanical deformations into the change of resistance (R). To overcome the

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technological gap between the electric output of the sensor and the readable result for human, we developed an all-in-one device that was capable to display the real time growth information. As shown in Fig. 1A, the device was composed of a wearable

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strain sensor (Fig. 1B) and a home-made readout circuit (Fig. 1C). The strain sensor

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consisted of a flexible and stretchable substrate obtained from a latex glove, a GM and a CNTM for strain sensing, two copper wires for electrical connection, and adhesive tapes to immobilize copper wires and to wear the sensor on a plant by adhering the two ends (Fig. 1B). Plant growth increased its dimension to deform the worn sensor, leading to the resistance (R) increment. To make the sensor outputs readable, we used the 555 timer as an analog-to-digital converter (ADC). Thus, the sensor response could be recognized and analyzed by the single-chip microcomputer 7

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to facilitate the growth monitoring.

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Fig. 1. Images and schematic illustration of the all-in-one wearable device for plant growth measurement. (A) Photograph of the device for plant growth monitoring. (B) Photograph of a wearable strain sensor. (C) Photograph of the home-made readout circuit. The main components were: (1) Sensor interface, (2) 555 Timer, (3)

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Single-chip microcomputer, (4) LCD1602 display and (5) Power switch and interface. (D) System-level block diagram of the all-in-one device. TRIG (Trigger), OUT

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(Output), THR (Threshold) and DIS (Discharge) were pinouts of the 555 timer.

Fig. 1C presented a readout circuit designed for this aim, consisting of a 555 timer-based oscillator circuit, a single-chip microcomputer and a LCD1602 display. The system-level overview for the wearable sensing system was presented in Fig. 1D. The strain sensor was used as a resistor in the oscillator circuit that put out a continuous stream of rectangular pulses with a specified frequency (f) consistent with 8

ACCEPTED MANUSCRIPT the Eq. (1): =

(

×

(1)

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where Rsensor was the resistance value of the sensor, Rc and Cc were constant values of

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the resistor and the capacity in the oscillator circuit, respectively. Growth of plant exerted tensile stress on the wearable sensor to increase Rsensor, leading to synchronously changes of frequency outputs. The single-chip

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microcomputer then converted the frequency inputs into the resistance values

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according to Eq. (2), and displayed Rsensor on the LCD screen. = (

× ×

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(2)

This all-in-one device provided a packed solution to measure plant growth, process the growth information and provide readable results.

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3.2 Fabrication of the GM/CNTM strain sensor

To measure the plant growth, we developed a facile method to fabricate the wearable and highly stretchable GM/CNTM strain sensor. The sensor was composed of a latex

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substrate at the bottom, a GM in the middle and a CNTM on the top. Fig. 2A

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schematically illustrated the two key steps for the fabrication. The first step was to deposit the graphite ink on the substrate, obtaining a flexible GM after evaporation of water naturally. CNT ink was then deposited on the GM and dried in air to make the CNTM. These processes resulted in a substrate/GM/CNTM structure with an excellent stretchability. As shown in Fig. 2B, the GM/CNTM responded to all strain loads in the range 0-150%. The GM was capable to detect strain loads within 50%, but the response overloaded under a larger strain (Inset of Fig. 2B). As for CNTM, it 9

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was not able to work as a strain sensor since it was broken under stretching (Fig. 2C).

Fig. 2. Fabrication of the GM/CNTM strain sensor. (A) Key steps in sensor fabricaton.

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(B) Responses of GM and GM/CNTM to strain loads. Inset showed the responses at 70% strain. (C) Photographs of a CNTM before stretching and after releasing. (D) Top view of an as-deposited CNTM. (E) SEM image of a CNTM after a stretching/relaxing cycle. (F) Photographs of a GM under stretching/relaxing cycles. (G) Top view of an as-deposited GM. (H) SEM image of a GM after a stretching/relaxing cycle. Inset showed the crack (marked with the dash rectangle). (I) Photographs of a GM/CNTM under stretching/relaxing cycles. (J) An as-deposited GM/CNTM. (K) GM/CNTM after stretching/relaxing cycles.

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ACCEPTED MANUSCRIPT According to the scanning electron microscope (SEM) image, the as-deposited CNTM was a continuous membrane (Fig. 2D). After a stretching and releasing cycle, CNTM broke into pieces and peeled off from the substrate, and the residual pieces

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were weakly adhered on the substrate (Fig. 2E). In contrast, the GM deposited on the substrate presented much better stability under strain loads (Fig. 2F). The GM narrowed its width and prolonged its length in response to the tension stress in the

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perpendicular direction of stretch and tensile stress oriented with the direction of

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stretch, which was attributed to Poisson effect [17, 40]. The deformation was highly reversible, for the relaxed GM exhibited no visible changes to the naked eye. The SEM image showed that the as-deposited GM was a continuous and flat membrane composed of overlapped flakes (Fig. 2G). After stretching/releasing cycles, the GM

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still remained a flat membrane without significant detachment (Fig. 2H). The cracks (marked with a rectangle and in the Inset of Fig. 2H) indicated that the GM also fractured into pieces under strain. However, these GM pieces returned to their original

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positions instead of peeling off from the substrate, explaining the reversible

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deformation of GM. More importantly, the GM was able to stabilize the CNTM, for the deformation of GM/CNTM was reversible as well (Fig. 2I). The stretchability of GM/CNTM were also showed in Movie S1 that GM/CNTM fractured into pieces in response to the applied strains (50%, 100% and 150%) and recovered after releasing. The as-deposited CNTM presented an entangled network structure on the surface of GM (Fig. 2J). Strain-induced deformation led to cracks in the GM at the bottom (Fig. 2K). CNTM on the top layers fractured into pieces as well, but were still 11

ACCEPTED MANUSCRIPT interconnected by the flexible CNTs. Hence, the combination of GM and CNTM provide a simple way to fabricate a high-performance strain sensor. The graphite ink and CNT ink could be easily deposited by a writing brush or

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micropipette in the range 1.6 to 5 µL cm-2. To understand the effect of different graphite and CNT membranes on sensing range, GM/CNTM strain sensors fabricated with different amount of inks (1.6, 3.2 and 5 µL cm-2) were subjected to a series of

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strain loads (10%, 20%, 30%, 50%, 70%, 90%, 110%, 130% and 150%) to evaluate

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their abilities for maintaining the electrical pathways in the deformed membranes. The sensing range decreased with the amount of graphite ink (Fig. S1A). As for CNTM, more CNT inks would contribute to a broader sensing range (Fig. S1B). These results suggested that a thinner GM and thicker CNTM would be preferable to broaden the

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sensing range. Thus, 1.6 µL cm-2 graphite ink and 5 µL cm-2 CNT ink were used to fabricate GM/CNTM strain sensors, and the morphologies of an obtained sensor were shown in Fig. S2.

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3.3 Sensor characterization

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Fig. 3A showed the current-voltage curves of the GM/CNTM sensor upon applying strains in the range of 0 to 20%. The current monotonically decreased with the increase of strain, demonstrating the ohmic behavior of the sensor. Fig. 3B was the hysteresis curve obtained by applying a stretching and releasing cycle on the sensor. The sensors response was expressed as its relative resistance (∆R/R0), where ∆R was the increment of resistance between the relaxed state (R0) and stretched state (R). In the stretching/releasing process, the applied strain increased/decreased step by step, 12

ACCEPTED MANUSCRIPT and ∆R/R0 increased/decreased synchronously, presenting a stepwise response curve (Inset of Fig. 3B). The almost overlapping ∆R/R0 in the stretching and releasing processes suggested a well recovering performance and no hysteresis of sensor

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response (Fig. 3B). The gauge factor (GF) was 48 at 50% strain and reached 352 for 150% strain, which showed comparable stretchability and improved sensitivity to the CNT strain sensor (up to 150% strain and ~6 of GF) [28, 41]. To evaluate the

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sensitivity to a small strain, the GM/CNTM sensor with the length of 1 cm was

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stretched and prolonged by 50 µm, i.e., a 0.5% strain (Fig. 3C). The sensor remained at a relaxed state (∆R/R0 = 0) before applying the strain. Then the tensile load applied on the GM/CNTM strain sensor resulted in an increment of ∆R/R0 with a rapid response time (~ 0.05 s). CNT-based strain sensors often showed low sensitivity and

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might even not respond to strains lower than 6% due to the increased contact areas between straightened and flattened CNTs [17, 41]. In comparison, the response of GM/CNTM sensor to a 0.5% strain indicates a high sensitivity. Fig. 3D showed the

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multicycle tests of the relative resistance variations upon stretching to strains of 10%,

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50%, 100% and 150%. The ∆R/R0 quickly jumped up upon stretching and recovered after releasing, presenting reproducible responses to each strain load. Fig. 3E presented the strain sensor performance in stretching/releasing cycles of 10% strain. The stable response to stretching/releasing cycles indicated the sufficient fatigue of the sensor, which was enough to measure plant growth that almost exerted monotonically increasing tensile on the sensor.

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Fig. 3. Characterizations of the GM/CNTM strain sensor. (A) Current-voltage curves of the sensor by applying strains in the range of 0 to 20%. (B) Hysteresis curve for the sensor with a maximum strain of 150%. Inset showed the real time response of the sensor to the strains. (C) Relative change of resistance to a 0.5% strain. Data were

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recorded with an interval of 0.01 s. (D) Multicycle tests of relative resistance variations upon stretching to strains of 10%, 50%, 100% and 150%. (E) Cycling

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stability of the sensors by stretching/releasing cycles to 10% strain.

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3.4 Mechanism of the GM/CNTM strain sensor To investigate the sensing mechanism of the GM/CNTM strain sensor, the microstructures of the GM and GM/CNTM under tensile strains were characterized. According to the SEM image under the 50% strain (Fig. 4A), GM exhibited herringbone configurations (illustrated using dash lines). The strain exerted on such structure could be as small as 5 to 10% of the applied strain [42], explaining the excellent deformation of GM.

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Fig. 4. Mechanism of the GM/CNTM strain sensor. (A) SEM image of the GM at 50%

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strain. Dash lines illustrated the herringbone configurations. (B) and (C) The 50% strain created gaps and islands in the GM. (D) SEM image of the GM/CNTM under 100% strain. (E) and (F) The flexible CNTs in the CNTM were bridging the gaps between islands.

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However, the rigid graphite flakes were not able to maintain the interconnections under a strain larger than 50%. As shown in Fig. 4B, tensile strain on GM created gaps to reduce the number density of connections between islands. The gap (~ 4 µm)

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between two islands was weakly jointed by a few graphite flakes, and was likely to

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rupture at a larger strain (Fig. 4C), resulting in limited sensing range. GM/CNTM also showed herringbone configurations under 100% strain (Fig. 4D). Although the gaps were larger than those of GM at 50% strain, the bilayer configuration of GM/CNTM was still able to connect the islands due to the entangled networks of CNTs (Fig. 4E and 4F). Thus, there was a synergistic reinforcement between the GM and CNTM to achieve a highly stretchable strain sensor. Small GM/CNTM islands and the herringbone configurations significantly improved the strechability of CNTM, which 15

ACCEPTED MANUSCRIPT was schematically illustrated with A4 papers (Fig. S3). In addition, the flexible CNTs in the entangled networks of CNTM bridged the gaps among islands to broaden the sensing range, which was illustrated with a simplified model in Fig. S4. Generally,

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strain sensors made by graphite often present high sensitivity but poor sensing range due to the low strechability of graphite sheet. Strain sensors made by 1D nanowires were typically characterized with broad sensing range, but might require complicated

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treatments to ensure the reversible deformation of the flexible nanowires. Taking the

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advantages of both materials (i.e., the bridging ability of CNTM and the herringbone configurations of GM), the bilayer structure of GM/CNTM achieved a highly stretchable and sensitive strain sensor.

3.5 Wearable measurements of plant growths

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The wearable device was used to monitor the growth of Solanum melongena L. (Fig. 5A). The growth of the fruit expanded its perimeter and exerted tensile stress on the sensor, leading to the increase of ∆R/R0. Fig. 5B showed the sensor response to the

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fruit growth over a period of 9 days, during which the fruit diameter (D) increased by

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11.36 mm. The increasing ∆D/D0 (where D0 was the initial diameter and ∆D was the diameter increment) and ∆R/R0 illustrated that the fruit of Solanum melongena L. was growing, and the sensor successfully detected the growth. The empirical formula of sensor readouts vs. fruit diameters was D = 17.798R0.1024 with a determination coefficient (R2) of 0.989 (Inset of Fig. 5B), indicating the applicability for quantitative measurement of plant growth.

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Fig. 5. Wearable monitoring of plant growths. (A) The fruit growth of Solanum melongena L. was being measured. (B) Growth measurement over a period of 9 days by the wearable device (●) and by manual measurements (▲). Inset showed the readouts of the wearable device v.s. fruit diameters. (C) Diel growth curves of the fruit measured over two successive days. (D) Growth curve of Solanum melongena L with a sampling interval of 1 min. Inset was the growth curve with a sampling interval of 5 s, which was shown in Movie S2. (E) The fruit growth of a Cucurbita pepo was being measured. (F) Stepwise growth captured by the wearable sensor.

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ACCEPTED MANUSCRIPT The curves in Fig. 5C showed the diel growth over two successive days, which were calculated using the equation in Fig. 5B. Obviously, the growth rate was rapid from 0 to ~ 6 a.m., decreased at daytime and then accelerated again after ~6 p.m.. The

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phenomenon that the fruit mainly grew at night was almost identical to the diel growth cycles of Arabidopsis thaliana and grape (Vitis vinifera × V. labrusca, cv. kyoho) [43, 44]. Fig. 5D showed the growth curve collected with a sampling interval

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of 1 min, obtaining an average growth rate of 3 µm/min (50 nm/s). Besides, the

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growth was not continuous but stepwise at a time scale of minutes. The D rapidly increased by 17.8 µm in 0 to 4 min, and almost remained stable in the next 5 min. After that, the fruit started to grow again. The fluctuation of growth rate was similar to the growth patterns of Phycomyces sporangiophores observed with a microscope

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[45], where the growth alternated between rapid and decreased rates with intervals minutes. Analysis of the growth with a shorter sampling interval of 5 s revealed that the growth rate was also stepwise at a time scale of seconds (Inset of Fig. 5D and

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Movie S2). The D almost remained stable for ~20 s, and rapidly increased in the next

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~25 s. Then, the stepwise growth was repeated. The results revealed that the growth rate was not constant but oscillated in seconds. Such phenomenon has been observed in researches on cell growth [4, 8]. The extension process of plant cell is stepwise [7, 46], could start/stop within a minute [7], and progresses at dynamic rates in the range of seconds to hours [47]. The similarity between the growth of Solanum melongena L. and the reported growth pattern of plant cells suggested high spatial and temporal solutions of the developed method, which was capable to measure the plant growth at 18

ACCEPTED MANUSCRIPT the cellular level. To the best of our knowledge, reports on such oscillatory growth patterns are limited to micron-size samples (e.g. pollen tubes, plant root hairs and hyphae), and our method presented the oscillatory growth of a centimeter-size sample.

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To evaluate the adaptability of the GM/CNTM strain sensor for other fruit, the sensor was used to measure the fruit growth of Cucurbita pepo (Fig. 5E), obtaining similar growth patterns. The growth fluctuated at a time scale of minutes with an average

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growth rate of 5.9 µm/min (Fig. S5). As for the growth occurred in seconds (Fig. 5F),

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the diameter of Cucurbita pepo increased by 12 µm in 70 s, presenting a rhythmic growth pattern (illustrated with dash lines): a growth period of ~10 s with an average growth rate of 300 nm/s, and a stagnating period of ~10 s. The developed wearable strain sensor device verified that the plant growth was a discontinuous process and the

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growth rate rapidly changed in seconds/minutes.

Compared with the traditionally method using scanning electron microscopies, the wearable detection avoided the destructive pre-treatment of plants for the dynamic

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measurement of plant growth at the nanometer scale, and presented attractive

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potential for continuous measurement. On the other hand, some aspects for its outdoor application should be considered. Firstly, water (rain) and other contaminants would affect the performance of sensor. Besides, the potential toxicity of CNT and the risk of its ingestion by the plant may lead to new challenges. A solution for these problems would be a sensor with the sandwich structure that embeds the sensing membrane between two elastic layers. However, an additional elastic layer would exert more stress to compromise the plant, which is undesirable. Hence, further work could be 19

ACCEPTED MANUSCRIPT concentrated on the development of thinner sealing layers or materials with smaller Young's modulus to provide comfortable sensors for plants. 4. Conclusion

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In summary, we demonstrated a user-friendly method to fabricate wearable strain sensors, and a non-destructive method for real time measurement of plant growth. The synergistic reinforcement between the graphite and carbon nanotube provided a rapid

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manufacturing technique for high-performance wearable strain sensor without

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dedicated equipment or complicated post-treatment procedures. The high spatial and temporal resolutions of the sensor were capable to quantitatively acquire growth information, and the sensor outputs, R, can be easily converted by the readout circuit to provide readable results. Thus, the all-in-one device provides a packaged solution

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for plant growth measurement. The simple procedures to fabricate the sensor and to measure the growth of plant would open up a new avenue for the application of

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wearable devices in plant science and development of wearable electronics.

Acknowledgements

This work is supported by the National Natural Science Foundation of China (31801628), Fundamental Research Funds for the Central Universities (2452016172 and 2452017144) and the Basic Work of Science and Technology of Ministry of Science and Technology of China (2013FY113400).

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