Enzyme cum pH dual-responsive controlled release of avermectin from functional polydopamine microcapsules

Colloids and Surfaces B: Biointerfaces 186 (2020) 110699

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Enzyme cum pH dual-responsive controlled release of avermectin from functional polydopamine microcapsules

T

Hongjian Wena, Hongjun Zhoua,b,*, Li Haoa, Huayao Chenb, Hua Xub, Xinhua Zhoua,b,* a b

School of Chemistry and Chemical Engineering, Zhongkai University of Agriculture and Engineering, Guangzhou, PR China Key Laboratory of Agricultural Green Fine Chemicals of Guangdong Higher Education Institution, Guangzhou, PR China

A R T I C LE I N FO

A B S T R A C T

Keywords: Polydopamine (PDA) Polyethyleneimine (PEI) Urease and urea bonds Adhesion and wettability Insecticidal activity

Novel enzyme cum pH dual-responsive microcapsule were prepared with an aim to enhance the utilization of pesticides and reduce environmental pollution. The synthetic procedure involved the introduction of urea bonds by forming a covalent bond between isocyanate–functionalized polydopamine (PDA) microcapsules and polyethyleneimine (PEI). The prepared AVM@PDA-IPTS-PEI microcapsules could effectively protect avermectin (AVM) from ultraviolet radiation, and thus decelerate the decomposition rate; the cumulative release showed positive correlations with pH and the urease activity. The AVM release rate was highest at pH 10. At pH 7, the release rate was enhanced after addition of urease, showing improved urease-responsive property under neutral or weak base condition. Especially at pH 7 in presence of urease, the release behavior was in agreement with the Logistic model and able to describe the S-shaped/sigmoidal release profiles, whereas Korsmeyer–Peppas model was better suited in the absence of urease, as the value of K1 was smaller than 0.45, suggesting that the behavior was controlled by Fick’s diffusion. AVM@PDA-IPTS-PEI displayed better adhesion property than AVM, and the microcapsule ameliorated foliage wettability. AVM@PDA-IPTS-PEI exhibited the insecticidal property similarly with AVM, which can be used for reducing the applied quantity of pesticides and improving their efficacy.

1. Introduction Pesticides are extensively used in agriculture for controlling insects, plant diseases, and weeds and increasing the yield and quality of crop production [1]. However, most of the pesticides are lost during application due to volatilization, degradation, photolysis, leaching, and runoff, and extremely less quantity finally reaches the targets [2–4]. Nanotechnology is increasingly applied for reducing the pollution of agricultural chemicals and solving other agricultural problems. The “nano-transporting system” can solve the problems of traditional pesticides, such as environmental pollution, bioaccumulation and pest resistance [5–7]. The high-efficiency deposition and strong adhesion properties are important for reducing the loss of pesticides and improving the utilization of pesticides, which can be prevented by encapsulating and adsorbing pesticides with some suitable carriers for imparting controlled release behavior and improving environmental sensitivity properties [2]. PDA has received extensive attention due to its great biocompatibility, environmental responsiveness and easy functionalization [8–11]. Reports show that polydopamine can assimilate UV light, and

therefore is widely used in preparing UV-shielding composites. PDA nanoparticles are easily deposited on the surface of hydrophobic or hydrophilic silicon wafers or leaves for effectively preventing slippage because PDA has abundant O-benzene bisphenol groups, which enhances its agglutination on the surface. The PDA carrier and the pesticide molecules interact via π-π stacking or electrostatic forces; both forces are weak physical interactions, and therefore, the release rate and duration are not well controlled for long-term applications [12]. Currently, stimuli-responsive microcapsules are promising choices for improving the sustained release performance of pesticides. Some researchers have reported that the stimulation responsiveness factors can be triggered by pH, enzyme, redox, temperature, and ultrasound [13–17]. In these types of stimulation responses, enzymes cause different types of stimuli. Enzymes show good performances for targeting and providing high specificity, accuracy, and efficiency for certain substances [18,19]. Many active enzymes can be found in the plant growth system, including cellulase, hemicellulase, pectinase, protease, lignin-degrading enzyme and urease [20–26]. In the dynamic system of soil, many free enzymes, including urease, alkaline phosphatase, dehydrogenase, and

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Corresponding authors at: School of Chemistry and Chemical Engineering, Zhongkai University of Agriculture and Engineering, Guangzhou, PR China. E-mail addresses: [email protected] (H. Wen), [email protected] (H. Zhou), [email protected] (L. Hao), [email protected] (H. Chen), [email protected] (H. Xu), [email protected] (X. Zhou). https://doi.org/10.1016/j.colsurfb.2019.110699 Received 5 September 2019; Received in revised form 15 November 2019; Accepted 29 November 2019 Available online 30 November 2019 0927-7765/ © 2019 Elsevier B.V. All rights reserved.

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continuously stir for 24 h, then filter, wash, and dry at 60 ℃. The synthesized sample was marked as AVM@PDA. PDA microcapsules were synthesized in the same method without adding AVM.

catalase are derived from bacteria or fungi, which show similar properties to plant-based enzymes. These enzymes stimulate the release of drugs in microcapsules, which can control many plant diseases and pests. The reaction rates of these enzymes are positively correlated with the soil temperature, moisture and pH values. When the roots of plants are affected by pests and diseases, the stable urease can trigger the rapid release of the pesticide, kill the pests and protect the plants from many diseases [27]. Hence, urease was selected as a stimuli-responsive enzyme in this study. Also, urea group can be smartly designed and broken by urease. Avermectin (AVM), a natural macrocyclic lactone biopesticide isolated from soil microorganisms, exhibits broad-spectrum activity and high insecticidal and acaricidal properties. It is toxic to humans and animals. The molecule has a weak fumigating effect but no internal suction effect [28,29]. However, AVM easily decomposes in light and features a very short half-life. Furthermore, conventional AVM microcapsules exhibit a sudden initial release [30]. Thence, a novel formulation of AVM should be designed for promoting its utilization, decreasing the loss of volatilization and photodegradation, and achieving sustained drug release. In this study, AVM was used as a model pesticide for preparing enzyme-responsive microcapsules, which can degrade microcapsules by urease and release active ingredients in situ for effectively controlling pests and diseases. By introducing urea bonds between isocyanatefunctionalized a urease-responsive delivery system of AVM was developed [31]. Polyethyleneimine (PEI) is a water-soluble high molecular polymer; each of the two carbon atoms in its structural monomer is bonded to the amino group, which is highly reactive and widely used for preparing microcapsules [32,33]. First, PDA-coated AVM microcapsules were prepared by in-situ polymerization and modified with 3Isocyanatopropyltriethoxysilane (IPTS) to obtain isocyanate-functionalized PDA microcapsules. Finally, PEI was bonded to an isocyanatefunctionalized PDA microcapsule to obtain PDA microcapsules based on PDA-IPTS-PEI, namely AVM@PDA-IPTS-PEI. The sustained release properties of these microcapsules were investigated at different pH and different urease concentrations. Additionally, stability, adhesion property, leaf affinity and insecticidal activity of the microcapsules were determined.

2.2.2. Preparation of isocyanate-functionalized AVM@PDA microcapsules (AVM@PDA-IPTS) Five hundred milligrams of as-synthesized AVM@PDA and 50 mL of anhydrous toluene were ultrasonically dispersed. Then, put 1 mL of 3isocyanatopropyltriethoxysilane in beaker and stir for 24 h at room temperature, then wash once with anhydrous toluene and at least twice with tetrahydrofuran, and dry under vacuum at 60 ℃. The AVM@PDAIPTS was obtained. 2.2.3. Preparation of PEI-conjugated AVM@PDA-IPTS microcapsules (AVM@PDA-IPTS-PEI) Two hundred milligrams of as-synthesized AVM@PDA-IPTS and 50 mL of DMF were ultrasonically dispersed after cooling with ice-bag for 30 min. Then, the mixture was heated on an oil bathing at 50 ℃, and a mixture of 0.2 g of PEI and 20 mL DMF was added dropwise to the beaker using a burette. The system was stirred for another 24 h, and the mixture was washed once with anhydrous toluene and at least twice with tetrahydrofuran and dried under vacuum at 60 ℃. This sample was denoted as AVM@PDA-IPTS-PEI. 2.3. Characterization The structures of AVM@PDA, AVM@PDA-IPTS, and AVM@PDAIPTS-PEI were analyzed by Fourier transform infrared spectroscopy (FTIR, Spectrum 100, Perkin-Elmer Co., USA) using the KBr squash technique at the wavelength range of 4000 − 450 cm−1. A thermogravimetric analyzer (TGA, TGA 2, Mettler-Toledo Co., USA) was used for analyzing the thermal stability of the particles over the heating range of 40 ∼ 700 ℃ at a heating rate of 10 ℃/min under a nitrogen atmosphere of 50 mL/min. The zeta potential and particle size of the samples were investigated using a Zetasizer Nano ZS (Bruker Corporation, Germany) in the water at pH 7 through ultrasonic dispersion. Gold particles were sprayed onto the surface of the samples under an N2 environment and the test voltage of 5 kV, and the surface topography of the samples was observed under a scanning electron microscope (SEM, HD, ZEISS, Germany). X-ray photoelectron spectroscopy (XPS) was conducted on an X-ray spectrometer (K-Alpha, Thermo Fisher Scientific, USA) equipped with a monochromatic Al Kα X-ray source (1486.6 eV) operating at 100 W under a vacuum of P < 10−8 mba with a pass energy of 150 eV (survey scans) or 25 eV (high-resolution scans). All peaks were calibrated with C1 s peak binding energy at 284.8 eV for adventitious carbon. The experimental peaks were fitted with Avantage software. The shape and surface morphology of the microcapsules were observed under a transmission electron microscope (TEM, talosf200 s, FEI Company, USA). For TEM, appropriate amounts of particles were suspended in distilled water. After sonication, a drop of the suspension was deposited onto a carbon-coated copper grid and dried overnight before observation.

2. Materials and methods 2.1. Materials Dopamine hydrochloride (DA) and polyethyleneimine (PEI, MW =600 Da) were purchased from Shanghai Macklin Biochemical Reagents (Shanghai, China). Also, 1-butanol, N, N-dimethylformamide (DMF), 3-isocyanatopropyltriethoxysilane (IPTS) and Trishydroxymethylaminomethane (Tris) were supplied by Shanghai Aladdin Biochemical Reagent (Shanghai, China). Anhydrous toluene and tetrahydrofuran were procured from Tianjin Chenmao Chemical Reagent Factory (Tianjin, China). Avermectin (AVM, 97 wt.%) was bought from Henan Kai Rui Biotechnology Development Co. (Henan, China). Urease (from Canavalia ensiformis (Jack bean), 34,310 units/g) was purchased from SIGMA-ALDRICH Co. (St Louis, America). Ethanol and hydrochloric acid were supplied by Tianjin Damao Chemical Reagent Factory (Tianjin, China). All the chemicals were of analytical grade and used as received without any further purification.

2.4. Loading content test

2.2. Methods

According to the literature [35], the AVM drug loading rate (DLR) of AVM@PDA was determined as follows: 50 mg of AVM@PDA was dispersed in a flask containing 50 mL of ethanol solution at 25 ℃ for 24 h with magnetic stirring. Then, the absorbance was measured using an ultraviolet-visible spectrometer (UV Lambda 365, Perkin Elmer), and the amount of AVM was calculated by the standard curve [A = 0.03437C−0.00023, R2 = 0 9997] at λ =245 nm. The percentage of AVM loading was calculated from the following equations:

2.2.1. Preparation of polydopamine-coated avermectin microcapsules (AVM@PDA) According to the literature [34], 250 mL (10 mM) of Tris buffer (pH = 8.5) and five hundred milligrams of DA were placed in a beaker and stirred at 500 rpm at room temperature. Then, add 20 mL of 1-butanol containing two hundred milligrams AVM to the system and 2

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DLR =

massofavermectinloadedinPDA × 100% massofAVM @PDA

deionized water to remove dust from foliage surface very carefully so that the structure of the foliage was not damaged. Aqueous suspensions of AVM@PDA, AVM, AVM@PDA-IPTS, and AVM@PDA-IPTS-PEI were prepared, and the foliage was immersed into the solution for 0.5 h, dried in the air, then each of the samples was divided into two halves, respectively. One half was washed with deionized water for 0.5 h, while the other half was left unwashed. Both were dried under vacuum at 45 ℃ for 6 h and observed under a scanning electronic microscope (SEM, HD, ZEISS, Germany). Some parts of the foliage were cut and adhered smoothly to glass slides for using as the experimental foliage surface. The glass slides were placed on the object stage of a contact angle (CA) instrument (Theta, Biolin Scientific Co. Ltd., Sverige), and AVM@PDA, AVM@ PDA-IPTS, and AVM@PDA-IPTS-PEI microcapsules were added dropwise onto the foliage. Images of each droplet on the foliage surface were captured, and the corresponding CA values were calculated. Given the data reliability and complexity of a cucumber leaf surface, measurements were repeated at least five times, and the average values are reported. The CA of deionized water was determined for comparison.

2.5. Anti-UV property The anti-UV property of AVM@PDA, AVM@PDA-IPTS or AVM@ PDA-IPTS-PEI was evaluated as follows: 50 mg of the sample was weighed and mixed with ethanol/water (40: 60, V/V) mixture into a 100-mL test tube and then, exposed to a 300 W UV lamp (Emax = 365 nm) at a distance of 25 cm with stirring, and keeping at room temperature by the recirculating water during the experiment. At intervals, 2.0 mL of the solution was withdrawn, centrifuged, and 2.0 mL of the mixture was added to replenish the volume. The absorbance of AVM was measured using an ultraviolet-visible spectrometer (UV Lambda 365, Perkin Elmer), and calculated from the equation [A = 0.03462C0.05808, R2 = 0.9992]. The release amount of AVM was monitored using its absorbance at 245 nm. 2.6. Enzyme and pH dual-responsive sustained-release property

2.9. Toxicity study

The sustained release profiles of AVM in the presence of the enzyme or at different pH values were determined following a previously reported method [36]. The pH of the medium was adjusted with hydrochloric acid or sodium hydroxide solution, and urease was dissolved at a concentration of 1 mg/mL. A certain mass of the sample was loaded into a dialysis bag with 5 mL pH-medium or 1 mg/mL urease solution, and placed in a conical flask with 45 mL of an ethanol/water (40: 60, V/ V) for triggering the release of AVM at 35 ℃. At interval at t, 1 mL of the solution was transferred and an equal volume of corresponding medium was added to the conical flask to replace the withdrawn sample. A standard curvilinear equation [A = 0.03462C-0.05808, R2 = 0.9992] was applied for determining the concentration of the solution from absorbance value. The amount of released AVM was determined, and cumulative drug release percentage (Ei) was calculated from equation [37]: n−1

Ei (%) =

Ve ∑1

Ci + V0 Cn

M × LC

AVM or AVM@PDA-IPTS-PEI was dissolved in ethanol and made up to 200 mg L−1 with water and then diluted in gradient to 100, 50, 25, 12.5 and 6.25 mg L−1. Leaves of flowering cabbage (2 cm × 2 cm in size) were dipped in the study material suspensions at concentrations of 6.25, 12.5, 25, 50, 100 and 200 mg L−1 for 30 min. After that, the leaves were removed and dried at the room temperature for 1 h. A filter paper was placed at the bottom of a 5-cm petri dish with a certain quantity of dried leaves, and then ten second-instar-diamondback moths were placed into each dish in triplicate. Those petridishes were placed in an insect incubator. The death rate of the diamondback moths was evaluated after 48 h. 3. Results and discussion 3.1. Synthesis processes of microcapsules

× 100%(i = 1, 2, 3...) Fig. 1A shows the preparation processes of microcapsules. Avermectin was dissolved in 1-butanol, and dopamine hydrochloride in TrisHCl buffer and these two solutions were mixed with stirring at 500 rpm. The AVM@PDA microcapsules were formed during the stirring. The microcapsules were dispersed in toluene for the modification with IPTS, which could generate an isocyanate group (−N = C]O) on the AVM@ PDA. Hereafter, the isocyanate-functionalized microcapsules conjugated with the amino group of polyethyleneimine (PEI) to form the urea group (−NH − CO − NH−), and PEI-conjugated isocyanatefunctionalized microcapsules (AVM@PDA-IPTS-PEI) were obtained.

Where M is the amount of AVM@PDA, Ve and V0 represent the volume of displaced solution (1 mL) and the whole volume of the release medium (50 mL), Ci represents the concentration of AVM in the tth sample, and n is the replacing number. 2.7. Statistical analysis The sustained release parameters were analyzed by analysis of variance (ANOVA) using the SPSS software package. In addition, the model-independent method was adopted for analyzing the curve differences. The difference factor (f1) was calculated using the equation, and the similarity factor (f2) was calculated using the equation as follows [30]: n ⎛ ∑i = 1

f1 = 100 ⎜ ⎝

3.2. Characterization 3.2.1. Fourier transform infrared spectroscopy (FT-IR) analysis FTIR spectroscopy was applied for characterizing the structure of the samples (Fig. 2A). For DA (Ab), the bands located at 3343 cm−1 and 1615 cm−1 were attributed to the stretching vibration of catechol groups and the aromatic ring, respectively, and 1497 cm−1 was the inplane bending vibration peak of C–H. These still existed in the polymer PDA (Ac) to confirm the formation of polydopamine that were also observed at AVM@PDA [34]. The multiple peaks in AVM (Aa) at 2972 cm−1, 2929 cm-1, and 2882 cm−1were stretching vibration band of CH, and 1739 cme−1 belonged to stretching vibration of − CO], which were observed in the spectral lines of AVM@PDA (Af), AVM@PDA-IPTS (Ag) and AVM@PDA-IPTS-PEI (Ah), indicating that the AVM was successfully loaded onto the carriers. The band that appeared at 2272 cm−1 was the stretching vibration peak of isocyanate group (−N = C]O) in IPTS (Ad) with a blue shift to 2366 cm−1 of AVM@PDA-IPTS

|Ei − Ti | ⎞ ⎟ ⎠

n

∑i = 1 Ei

⎧⎡⎛ 1 f2 = 50 log ⎢ ⎜1 + ⎛ ⎞ ⎨⎢ n⎠ ⎝ ⎩⎣⎝

n

∑ i=1

−0.5

⎞ (Ei − Ti )2⎟ ⎠

⎫ ⎤ ⎥ × 100⎬ ⎥ ⎦ ⎭

Where n is the number of experimental intervals, Ei is the release rate from the reference sample at a specific time interval, and Ti is the release rate from the control sample at a specific time interval. 2.8. Adhesive property and contact angle measurement of microcapsules Foliage obtained from a light incubator was flushed gently with 3

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Fig. 1. (A) Synthetic processes of microcapsules and (B) the responsive avermectin release performance.

(Ag) [38]. The peaks at 2948 cm−1 and 2827 cm−1were the multiple stretching vibration peaks of CHe in PEI, and 1466 cm−1 was the stretching vibration peak of C − N and in-plane bending vibration of CHe, those which were the structure of PEI (Ae). After isocyanate − functionalized microcapsules interacted with PEI, the spectrum of AVM@PDA-IPTS-PEI (Ah) exhibited a urea linkage (−NH − CO − NH−) peak at 1662 cm−1. Meanwhile, the absorption band of the isocyanate group (−N = C]O) at 2366 cm−1 peaks disappeared, which proved that PEI was conjugated with the AVM@PDA-IPTS microcapsules [38].

at 538 ℃ under air. The residual of PDA, AVM@PDA, AVM@PDA-IPTS and AVM@PDA-IPTS-PEI was 54.24 %, 33.08 %, 52.97 % and 46.16 %, respectively, at 700 ℃. The sample of PDA was decomposed at 355 ℃ and due to the modification, the decomposition temperatures of PDA in AVM@PDA, AVM@PDA-IPTS and AVM@PDA-IPTS-PEI have varying degrees of changes. Contrasted to samples under air, the decomposition temperatures of AVM in AVM@PDA-IPTS and AVM@PDA-IPTS-PEI were 219 ℃ and 207 ℃, respectively. However, with comparing to the sample under the atmosphere of nitrogen, we have found that AVM@ PDA-IPTS has one more peak belonged to avermectin, possibly indicating the conjugation of IPTS and PDA.

3.2.2. Zeta (ζ) potential As shown in Fig. 2B, the ζ potentials of AVM and PDA were −10.66 ± 0.72 and -22.31 ± 1.94 mV, respectively. The potential of AVM@PDA changed to -31.24 ± 1.49 mV and was lower than that of the AVM and PDA. It increased to -27.47 ± 1.14 mV after grafting with IPTS. As expected, the zeta potential of AVM@PDA-IPTS-PEI showed a greater change than those of AVM@PDA and AVM@PDA-IPTS, reached to 37.23 ± 1.55 mV. This may be explained by the fact that PEI was positively charged [33].

3.2.4. Scanning ＆ transmission electron microscopy and X-ray photoelectron spectroscopy analysis Scanning electron microscopy (SEM) and Transmission electron microscopy (TEM) were utilized for characterizing the morphologies of PDA, AVM@PDA, AVM@PDA-IPTS, and AVM@PDA-IPTS-PEI (Fig. 3). It can be seen from Fig. 3A－D that the PDA microcapsules are spherical and tend to agglomerate due to the adhesion of the PDA [14]. After the encapsulation of AVM and modification of IPTS and PEI, the samples still retained their same shape with the PDA microcapsules, but their surface was rough. The particle sizes of the microcapsules (The particle size is calculated according to image-pro plus, and its particle size distribution is shown in Fig. 3K.) of PDA, AVM@PDA, AVM@PDA-IPTS and AVM@PDA-IPTS-PEI were determined approximately to be 227 nm, 284 nm, 308 nm and 352 nm, respectively, which confirmed that the particle sizes of microcapsules increased along with AVM-loading and IPTS and PEI-conjugation. The transmission electron microscopy (Fig. 3E－J) showed a spherical in shape, and the particle sizes of the microcapsules increased due to the modification, similar to the SEM analysis. The surface became smoother after the grafting of IPTS. However, a film of PEI can be clearly seen on the surface of the AVM@ PDA-IPTS-PEI microcapsules, which indicated that PEI was successfully conjugated on the surface of the AVM@PDA-IPTS. As seen in Fig. 3L and M, the XPS spectrums of N and Si were carried out to investigate the composition of the microcapsules. Fig. 3L shows the spectrum of N 1s, which possessed peaks of AVM@PDA-IPTS and AVM@PDA-IPTS-PEI at 532.71 eV and 531.44 eV, respectively. With the modification of PEI, the intensity of AVM@PDA-IPTS was strengthened. The spectrum of Si is shown in Fig. 3M with two significant peaks, which belonged to Si 2p and Si 2 s, respectively and as can be seen, the PEI-graft reduced the intensity of the Si spectrum. The atomic of N has increased, meanwhile, Si was decreased, indicating that PEI was grafted.

3.2.3. Thermogravimetric (TGA) analysis Fig. 2C shows the TGA and DTG thermograms of the microcapsules under the atmosphere of nitrogen. For all the samples, the loss of mass at the range of 40 − 100 ℃ was due to the elimination of residual surface water. No sharp peaks of thermal decomposition were observed during the subsequent heating, which indicated that the dopamine molecules were polymerized into PDA forming covalent bonds [36,39]. For AVM, AVM has four different stages of decomposition peaks, of which 90 ℃ and 162 ℃ are two smaller peaks, and 224 ℃ and 403 ℃ are sharper peaks. PDA has a wide peak at 359 ℃ with remaining of 56.20 % at 700 ℃. PDA is easy to carbonize at high temperature under a nitrogen atmosphere, so the residual amount is larger than that of AVM [40,41]. The thermal decomposition peak of the AVM@PDA was sharp and significant, indicating that AVM was coated by PDA compared to the pure PDA. AVM@PDA-IPTS has three decomposition peaks, of which 154 ℃ and 226 ℃ are belonged to avermectin, and 359 ℃ belonged to PDA-IPTS conjugate. For AVM@PDA-IPTS-PEI, avermectin reached the decomposition temperature at 133 ℃, while the PDA-IPTSPEI conjugate was at 327 ℃. The weight loss of AVM@PDA-IPTS was significantly lower than that of AVM@PDA because 3-Isocyanatopropyltriethoxysilane was thermally decomposed to silica, and compared to it, the weight loss rate of AVM@PDA-IPTS-PEI was increased due to the conjugation of PEI. These suggest that the modification can improve the thermal stability of AVM, as it avoids direct contact between AVM and the external environment [42]. The TG and DTG curves under the atmosphere of air has shown in Figure D, and the loss of mass at the range of 40 − 100 ℃ was also due to the elimination of residual surface water. Compared to AVM under atmosphere of nitrogen, the residual rate of avermectin has become 0 %

3.3. Study of anti-UV performance Fig. 3N shows the curves of AVM release residual with the microcapsules of AVM@PDA, AVM@PDA-IPTS, and AVM@PDA-IPTS-PEI. After being irradiated with UV light for 22 min, the degradation rate of 4

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Fig. 2. (A) Fourier-transform infrared spectroscopy (FTIR) of (Aa) AVM, (Ab) DA, (Ac) PDA, (Ad) IPTS, (Ae) PEI, (Af) AVM@PDA, (Ag) AVM@PDA-IPTS, (Ah) AVM@PDA-IPTS-PEI. (B) Zeta potential of (Ba) AVM, (Bb) PDA, (Bc) AVM@PDA, (Bd) AVM@PDA-IPTS, (Be) AVM@PDA-IPTS-PEI (the error bars have provided in the attachment of numerical data; SD, n = 3). TGA and DTG thermograms under the atmosphere of nitrogen (C) and air (D) of (a) AVM, (b) PDA, (c) AVM@PDA, (d) AVM@PDA-IPTS, (e) AVM@PDA-IPTS-PEI. (The inserted tables below the figures are the thermal decomposition temperature of the sample under different conditions and the parameters of DTG curves in the figures are magnified to find the peak.).

The comparison indicated that the special structural PDA shell could improve the UV resistance of AVM, and it also modified the UVshielding effect [42].

AVM exceeded 50 %, with the residual rate of 32.31 %, and the decomposition dynamic equilibrium was reached at 100 min. Moreover, the residual rate of AVM@PDA was 78.79 % at 100 min and less than 50 % at 580 min. The introduction of IPTS-PEI further improved the UV resistance of the material due to its isolation function. The residual rates of AVM, AVM@PDA, AVM@PDA-IPTS, and AVM@PDA-IPTS-PEI at 580 min were 9.52 %, 40.73 %, 74.57 %, and 79.96 %, respectively.

3.4. Controlled release behavior of AVM Fig. 1B shows the synthetic route of the microcapsules and the 5

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Fig. 3. Scanning electron microscopy (SEM) of (A) PDA, (B) AVM@PDA, (C) AVM@PDA-IPTS and (D) AVM@PDA-IPTS-PEI. Transmission electron microscopy (TEM) of (E, F) AVM@PDA, (G, H) AVM@PDA-IPTS and (I, J) AVM@PDA-IPTS-PEI. (K) Topography of the nanoparticles size in SEM images. XPS spectrum of N 1s (L) and Si (M). (The inserted tables below the figures are the binding energy and atomic of AVM@PDA-IPTS and AVM@PDA-IPTS-PEI.) (N) Residual rate of AVM rate after UV irradiation.

which limited the growth of the release rate, so that its cumulative release would be lower than AVM@PDA and AVM@PDA-IPTS. As the covalent bond was formed due to the reaction of －N－H group in the PEI and isocyanate (－N＝C＝O) on the IPTS due to the interaction between the electrostatic attraction and hydrogen bond, and the binding force became large, resulting in the lowest release at pH 7. Under the acidic or alkaline condition, the π–π stacking effect in PDA, the covalent bonds between PEI and PDA were possibly destroyed like AVM@PDA to result in a faster release rate than pH 7. Moreover, at pH 3, the protonated －N－H group was positively charged, and superimposed with the original positive charge to produce a strong electrostatic interaction with the negatively charged PDA shell, which was accompanied by protonation and electrostatic interaction; the release rate was slower than pH 10.

release performance of avermectin. The reaction between PEI and isocyanate-functionalized polydopamine produces a urea linkage, which acts as an enzymatic degradation site, and the urea bond is easily destroyed by urease to respond to the release of avermectin. 3.4.1. Effects of pH Fig. 4A shows the pH-responsive release of the microcapsules. AVM@PDA and AVM@PDA-IPTS showed significant pH response, with the fastest release at pH 10 and the slowest release at pH 7. The samples reached equilibrium at different times. At 246 h, the cumulative release of AVM@PDA at pH 3, 7, and 10 reached 41.18 %, 33.22 %, and 66.69 %, respectively. At pH 7, the π-π stacking structure and hydrogen bonding can be formed between AVM and PDA, because AVM contains heteroaromatic rings and hydroxyl groups, and PDA has aromatic rings and amino groups, thereby, PDA can effectively encapsulate AVM [43]. When the release environment was acidic or alkaline, the π–π stacking and hydrogen bonding were destroyed, and the release became faster than pH 7. PDA is usually positively charged under the acidic condition as the amino group is protonated at acidic condition, so the negatively charged AVM can be tightly bound to PDA. However, PDA was negatively charged at pH 10 and was mutually exclusive with the negatively charged AVM during the release process to increase the cumulative release compared to the sample at pH 3. So, the cumulative release rate at pH 3 was faster than that at pH 7 but slower than that at pH 10. AVM@PDA-IPTS was grafted the 3-Isocyanatopropyltriethoxysilane (IPTS) on the outer surface of the PDA vehicle that slowed the release rate of AVM, but the main controlled release mechanism was same as AVM@PDA, and at 246 h, the cumulative release rate of AVM@PDAIPTS at pH 3, 7, and 10 reached to 30.41 %, 17.97 %, and 46.29 %, respectively. A responsive cumulative release profile of AVM@PDA-IPTS-PEI at different pH is shown in Fig. 4B. The release equilibrium reached at 174 h, and the cumulative release capacities at 246 h in pH 3, 7 and 10 reached 29.00 %, 11.19 %, and 40.69 %, respectively, which was slower than that of AVM@PDA and AVM@PDA-IPTS. Due to the conjugation of PEI, the surface of AVM@PDA microcapsules formed a shell,

3.4.2. Effects of urease In contrast, a 1 mg/mL urease solution was added to the dialysis bag along with AVM@PDA-IPTS-PEI at different pH conditions, and the release condition was changed to facilitate enzyme-responsive release at different pH. The release comparison data are shown in Figure 7B. In 246 h, the cumulative release capacities at pH 3, 7 and 10 increased to 25.42 %, 16.42 %, and 42.03 %, respectively. At pH 7 and pH 10, the cumulative release capacities were increased by 46.74 % and 3.29 %, respectively, compared to the sample without urease. However, the capacity at pH 3 was reduced. According to the literature, the pH value could affect the activity of urease, which was completely inactivated at pH 4, 40 % of normal activity was achieved at pH 5, and the maximum activity was restored at pH 6.5. The urease activity decreased with the increase in pH [27,44,45]. Because the urease was inactivated at pH 3, part of urease protein was coated on the surface of AVM@PDA-IPTS-PEI microcapsules, which slowed the release down at pH 3, and a reduction in the activity at pH 10 produced a smaller effect than that at pH 7. Under the weakly alkaline or neutral condition, the enzyme of urease can decompose the urea bond (－NH－CO－NH－) and break the segment of polymer PEI down [36]. The entire release process of 0－246 h can be divided into three stages, a) the first stage of the rapid release 6

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Fig. 4. (A, B) Effects of pH and urease at different pH on the sustained-release performance of AVM (the error bars have provided in the attachment of numerical data. (C, D, E, F, G and H) Fitting models of AVM@PDA-IPTS-PEI and AVM@PDA-IPTS-PEI with urease.

between 0－23 h, b) the second of slow-release in 23－174 h, and c) the third of the balanced release in 174－246 h. At the first and second stages, due to electrostatic interaction, hydrogen bonding, intermolecular forces and the enzymatic hydrolysis of the －NH－CO－NH － bonding, the release velocity of AVM@PDA-IPTS-PEI in presence of urease was faster than that in absence of the enzyme. At the third stage, it reached to the release equilibrium status.

Table 1 Statistical variability results of AVM@PDA-IPTS-PEI under the different release conditions.

3.4.3. Statistical analysis of AVM@PDA-IPTS-PEI microcapsules For comparing the differences of the sustained release curves at different pH values and enzyme of urease, the dissimilarity factor f1 and the similarity factor f2 were employed for evaluating the difference and similarity between the two curves [46]. Compared to the difference of the two curves by the model-independent method, if f1 > 15 and f2 < 50, the two curves did not exhibit systematic similarity, and if f1 < 15 or f2 > 50, then the two curves would exhibit systematic similarity. The sustained release curve of AVM@PDA-IPTS-PEI at pH 7 was used as a reference sample, while other sustained release curves were used as the control. Table 1 shows that the factor of f1 was higher than 15 and f2 lower than 50 at pH 3, pH 10 and pH 10 in the presence of urease, indicating that the sustained release curve at pH 3, pH 10 and

Reference

Control

f1

f2

pH 7

pH pH pH pH

161.6 171.8 34.6 204.7

42.6 38.5 72.6 35.5

3 10 7 with urease 10 with urease

pH 10 with urease exhibited significant differences compared to that at pH 7. However, at pH 7 with urease, f2 = 72.6, i.e. higher than 50, and the latter finding indicated that the two curves exhibited systematic similarities. 3.4.4. Release kinetics of microcapsules The release kinetics of AVM@PDA-IPTS-PEI were studied under different conditions, and the models of release kinetics such as Zeroorder, First-order, Higuchi, Hixson-Crowell, Korsmeye-Peppas and Logistic model [47,48] were introduced to fit the data of the cumulative release. The results are shown in Fig. 4C－H and Table 2. R-square was 7

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Table 2 Fitting results for release curves of AVM@PDA-IPTS-PEI and AVM@PDA-IPTS-PEI with urease. Release model

pH

AVM@PDA-IPTS-PEI K1

Zero-order y = K1 t First-order y = K2 [1 − exp(−K1 t )] Higuchi

y = K1 t 1

2

Hixson-Crowell

y = (K2 − K1 t )3 Korsmeyer-Peppas

y = K2 t K1 Logistic

y=

K3 1 + exp[−K2 (t − K1 )]

3 7 10 3 7 10 3 7 10 3 7 10 3 7 10 3 7 10

0.311 0.090 0.208 0.131 0.440 0.018 2.926 1.230 2.880 −0.006 −0.003 −0.005 0.256 0.206 0.404 8.097 4.113 54.845

K2

AVM@PDA-IPTS-PEI with urease K3

R

25.461 9.612 40.913

0.889 0.406 0.925 0.934 0.711 0.945 0.730 0.788 0.973 0.684 0.649 0.828 0.981 0.992 0.991 0.953 0.949 0.990

25.104 7.898 40.166

2.396 1.689 2.376 8.362 3.848 4.688 0.101 0.093 0.026

2

used to define the suitability of fitting models. For determining the exponent K1, the only portion of the release curve where M / M < 60 % was used [49]. At pH 3 and pH 10, the R-square values were greater than 0.95, and the release process of AVM@PDA-IPTS-PEI in presence and absence of urease followed the Korsmeyer–Peppas model, and the values of K1 were smaller than 0.45, illustrating that the behavior of AVM@PDA-IPTS-PEI in presence or absence of urease was controlled by Fick’s diffusion [50]. Moreover, a one-way release pattern can describe the AVM@PDA-IPTS-PEI release system at pH 3 and 10. The result also showed an exponentially decreasing concentration gradient from the center of the vehicle to the surrounding environment during the release of AVM, and the PDA chains were closely bound to each other. At pH 7, the emancipation behavior of AVM@PDA-IPTS-PEI without urease agreed with the Korsmeyer–Peppas model, whereas the logistic model was better suited for AVM@PDA-IPTS-PEI with urease. When the correlation coefficient was greater than 0.95, the release behavior was able to describe the S-shaped/sigmoidal release profiles [51].

K1 0.249 0.217 0.341 0.192 0.081 0.024 2.703 1.691 3.446 −0.004 −0.004 −0.004 0.264 0.262 0.359 6.215 10.115 31.532

K2

K3

R2

20.535 13.589 40.037

0.647 0.959 0.976 0.905 0.910 0.938 0.550 0.559 0.915 0.468 0.518 0.688 0.962 0.942 0.987 0.950 0.977 0.948

19.790 12.868 38.085

2.301 2.118 2.792 7.001 4.420 6.556 0.135 0.060 0.027

AVM@PDA-IPTS-PEI were less than AVM@PDA microcapsules, but they still showed better adhesion property than pure avermectin. Probably the adhesion was reduced because the bonding of IPTS and PEI resulted in reduced exposure of catechol groups. The contact angle (CA) of deionized water was considered as the control. The CA images are shown in Fig. 5J, K, L and M. The calculated CA mean values of the water droplets were 80.78 ± 0.65°, 64.10 ± 0.93° and 71.15 ± 1.04° for AVM@PDA, AVM@PDA-IPTS, and AVM@PDA-IPTS-PEI, respectively. Meanwhile, under the same conditions, the CAs of the deionized water droplet on foliage was 93.19 ± 0.85°. The surface of the leaves contained a waxy layer of different higher fatty acids, higher fatty alcohols, and higher aliphatic aldehydes. AVM@PDA bound to the foliage surface by hydrogen bond through the hydroxyl groups on PDA and hydroxyl or carboxylic acid groups on the foliage surface. However, the isocyanate group in AVM@ PDA-IPTS also can form hydrogen bonds with foliage surface. Besides hydrogen bond, AVM@PDA-IPTS-PEI also can form electrostatic interaction with the foliage to enhance force with the foliage surface. These multimodal interactions between AVM@PDA-IPTS-PEI and the foliage surface resulted in higher wettability between them [53]. These results indicated that the avermectin microcapsules have improved wettability to foliage compared to that of water.

3.5. Adhesion and wettability of microcapsules The efficient deposition and strong adhesion of pesticides on the surface of foliage are very important for minimizing the loss of the pesticides and raise utilization efficiency. To prove that AVM@PDA microcapsules have better adhesion behavior than AVM and to evaluate the effect of modified microcapsules on adhesion properties, the amounts of AVM, AVM@PDA, AVM@PDA-IPTS, and AVM@PDA-IPTSPEI were sprayed on the foliage and a half with 0.5 h water washing, respectively. For identification of the residual microcapsules on the leaves, the SEM image of the blank leaf was put in Fig. 5A. First, the retained amount of AVM on leaves without or with water washing was measured (shown in Figs. 5B, C). Only a small amount of AVM was detected on the unwashed leaves, and extremely few residues on the washed leaves (circled small particles in Fig. 5C), which indicated that AVM adhered to the leaves. The adhesion behaviors of the microcapsules with the same processing on the foliage are shown in Fig. 5D－ I. Fig. 5D－E shows many remaining particles in the texture of the leaves and only a slight decrease in the amount of the AVM@PDA microcapsules on the washed and unwashed leaves, as PDA possesses many catechol groups, which enhanced its adhesion performance on the surfaces of the leaves [42,52]. Conversely, Fig. 5F－I revealed that the quantity of AVM@PDA-IPTS and AVM@PDA-IPTS-PEI microcapsules was slightly reduced on the washed and unwashed leaves. These results indicated that the adhesion of AVM@PDA-IPTS and

3.6. Insecticide test LC50 is a basic parameter for evaluating the effect of insecticides. The lethal concentrations of the individual insecticides for second-instar-diamondback moths are shown in Table 3. The observed effects are expressed as LC50 values derived from prohibiting analysis with 95 % confidence limit. In to second-instar-diamondback moths, the LC50 value of AVM was 14.33 mg L−1, whereas that of AVM@PDA-IPTS-PEI was 9.60 mg L−1. The 95 % confidence limit ranges of AVM and AVM@ PDA-IPTS-PEI were 6.93－29.64 and 2.63－34.99, respectively, and the range of AVM was inside the AVM@PDA-IPTS-PEI. The result corroborated that AVM@PDA-IPTS-PEI showed a similar insecticidal activity like AVM, and it can reduce the use of insecticides and improve pest control efficacy. 4. Conclusions A urease-responsive microcapsule was synthesized by the conjugation between PEI and isocyanate-functionalized microcapsule via urea bond. The prepared microcapsules could effectively protect AVM 8

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Fig. 5. SEM images of the microcapsules on leaves: (A) blank; (B) AVM, (D) AVM@PDA, (F) AVM@PDA-IPTS and (H) AVM@PDA-IPTS-PEI; (C) AVM, (E) AVM@ PDA, (G) AVM@PDA-IPTS and (I) AVM@PDA-IPTS-PEI with water washing. Contact angle images of (J) deionized water, (K) AVM@PDA, (L) AVM@PDA-IPTS and (M) AVM@PDA-IPTS-PEI (the error bars have provided in the attachment of numerical data).

Author contributions

Table 3 Results of the toxicity study. Treatment

Toxicological regression equation

LC50 (mg·L−1) (95 % CL)a

SE

R2

AVM

y = 1.3461x+3.4434

5.31

0.9839

AVM@PDAIPTS-PEI

y = 0.8239x+4.1907

14.33 (6.93－29.64) 9.60 (2.63－34.99)

6.33

0.9303

a

Hongjian Wen and Hongjun Zhou conceived and designed the experiments; Hongjian Wen performed the experiment; Hongjian Wen, Hongjun Zhou and Xinhua Zhou analyzed the data; Li Hao, Hua Xu and Huayao Chen contributed the reagents/materials; Hongjian Wen, Hongjian Wen, Hongjun Zhou and Xinhua Zhou wrote/edited the paper. Declaration of Competing Interest

LC50 values and 95 % confidence limits (CL).

The authors declare no conflict of interest.

against the UV light. In addition, the release of AVM@PDA and AVM@ PDA-IPTS could be triggered by pH change, while AVM@PDA-IPTS-PEI exhibited a positive correlation with pH as well as urease. Under weak acid or base conditions, the AVM release rates from the three types of microcapsules were all higher than those under neutral conditions. Meanwhile, the urease-responsive controlled release performance was observed in AVM@PDA-IPTS-PEI microcapsules. Especially at pH 7, the emancipation behavior of AVM@PDA-IPTS-PEI in absence of urease followed the Korsmeyer–Peppas model, whereas the logistic model better suited for the AVM@PDA-IPTS-PEI in the presence of urease. The value K1 of AVM@PDA-IPTS-PEI was smaller than 0.45 in absence of urease, illustrating that the behavior was controlled by Fick’s diffusion, and the behavior of AVM@PDA-IPTS-PEI in presence of urease could be described by the S-shaped/sigmoidal release profiles. For AVM@PDAIPTS-PEI, the deposition adhesion property was better than pure avermectin and it also improved the wettability on foliage compared to that of water. AVM@PDA-IPTS-PEI showed an insecticidal activity similarly to AVM, which can be used for reducing the application of pesticides and improving the pesticidal effect. This pesticide delivery system with a controlled release property possesses a great potential in agricultural applications and shows the performance depending on soil environment changes or stimulation caused by changes in pest physiological systems.

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